With Fronds Like These

I'm sure pretty much anyone who's spent time looking into rock pools along the coast will be familiar with sea anemones. These sessile animals with their squidgy bodies and crown of tentacles can be seen almost anywhere there's a rock for them to stand on and a tide to cover them. As a kid, I used to amuse myself by poking them with a finger, noting the slight velcro-ish feel as the harassed anemone would vainly attempt to sting its attaker as it withdrew for protection. In hindsight, I was perhaps just fortunate that New Zealand anemones lacked the strength of venom to affect a human.

Waratah anemones Actinia tenebrosa, copyright John Turnbull.

Many of the anemones I was encountering as a child probably belong to a particular clade known as the Actinioidea. As recognised by Rodríguez et al. (2014), familiar members of this group include the beadlet anemone Actinia equina* from the Atlantic coasts of Europe and Africa, the red sea anemone Actinia tenebrosa of eastern Australia and New Zealand, and the aggregating anemone Anthopleura elegantissima and giant green anemone Anthopleura xanthogrammica of the Pacific coast of North America. Wikipedia informs me that another actinioid, the snakelocks anemone Anemonia viridis, is eaten after being marinated in vinegar and fried in parts of the Mediterranean. Rodríguez et al. recognised their Actinioidea primarily on the basis of molecular phylogenetic analysis but most members of this group had previously been recognised as relatives due to their possession of a sphincter muscle around the edge of the gastric cavity near the top of the column. This muscle allows the body cavity to be pulled tightly closed, providing protection and, for intertidal species, holding water inside the body to protect against desiccation.

*Actinia equina, offhand, was given its species name by Carl Linnaeus who described it under the name Priapus equinus. 'Equinus' means 'of a horse' whereas 'priapus' means... exactly what you think it means. Yes, the name of this species literally means 'hung like a donkey'.

Pompom anemone Liponema brevicornis, copyright Ocean Networks Australia.

Other common features of actinioids include well-developed muscles around the base of the column and an adhesive basal disc for clinging to rocks. However, both the upper sphincter muscle and the basal muscles have been lost in various subgroups of the actinioids, often at the same time. Anemones lacking these muscles, such as the ghost anemones Haloclava, are generally deeper water forms that do not cling to rocks but instead live burrowed into sand with their tentacles extended above the surface. One such anemone, the twelve-tentacled parasitic anemone Peachia qinquecapitata, develops as a larva as a parasite on the hydrozoan medusa Clytia gregaria. The larvae gain entry to their host by being eaten as food particles but proceed to themselves feed on the contents of the host's gastric cavity and eventually on the host itself. Another group of deep-sea actinioids, including such species as the deeplet anemone Bolocera tuediae and the pompom anemone Liponema brevicornis, are able to shed their tentacles as a defence thanks to small sphincter muscles at the base of each tentacle. Bolocera tuediae, found in the North Sea, is a particularly large anemone reaching up to a foot in diameter.

Aggregating anemones Anthopleura elegantissima fighting over space, copyright Brocken Inaglory. The white 'tentacles' the anemones are extending towards each other are inflated acrorhagi (see below).

Many actinioids form symbiotic associations with microscopic algae such as zooxanthellae, containing them within their body and supplementing their own nutrition through the algae's photosynthesis. A number of species reproduce by brooding larvae within the body cavity, only releasing them when they are more developed and better equipped to survive the outside world. Finally, many species of actinioid have the column ornamented by various protuberances such as vesicles or verrucae. These structures may serve environmental protective functions, such as increasing desiccation resistance or functioning in camouflage. Members of Anthopleura and related genera often have specialised bulbous protuberances called acrorhagi around the distal part of the column (Daly et al. 2017). These acrorhagi are packed with stinging cells and are used not so much to protect against predators as against other sea anemones. The acrorhagi-equipped anemone flails its column about, pressing the acrorhagi against any competitor that gets too close and stinging it until it is forced to back off. Its a tough world out there and any anemone worth its salt has got to be willing to defend its position.

REFERENCES

Daly, M., L. M. Crowley, P. Larson, E. Rodríguez, E. H. Saucier & D. G. Fautin. 2017. Anthopleura and the phylogeny of Actinioidea (Cnidaria: Anthozoa: Actiniaria). Organisms, Diversity & Evolution 17: 545–564.

Rodríguez, E., M. S. Barbeitos, M. R. Brugler, L. M. Crowley, A. Grajales, L. Gusmão, V. Häussermann, A. Reft & M. Daly. 2014. Hidden among sea anemones: the first comprehensive phylogenetic reconstruction of the order Actiniaria (Cnidaria, Anthozoa, Hexacorallia) reveals a novel group of hexacorals. PLoS One 9 (5): e96998.

Antipatharia: The Black Corals

The black coral Antipathes, copyright Jez Tryner.

One piece of trivia I've learnt while looking stuff up for this post: the genus name Antipathes, from which the whole group of the Antipatharia derives its name, was coined to refer to the supposed ability of black coral to cure illnesses and protect against evil. It almost goes without saying that I found no indications that this evaluation was warranted.

The black corals of the Antipatharia are a group of colonial, sessile cnidarians that are found in marine waters around the world. They are predominantly deep-water animals, found mostly below the level of light penetrance. Those individuals that are found in shallower waters still keep to secluded habitats out of the light. Some of the shallowest communities are found in New Zealand at depths of only 4 m in the fiords of the South Island, where a rich concentration of tannins in the top layer of the water prevents light from reaching even that far down (Wagner et al. 2012). Black corals have been harvested in many parts of the world for jewellery (and also for their supposed curative properties referred to above), but they are very slow-growing animals. At least one colony subjected to radiocarbon dating was estimated to be over 4000 years old (Roark et al. 2009).

Wire coral Cirrhipathes, copyright Frédéric Ducarme.

Colonies of antipatharians may be highly branched, or they may form an unbranched whip (the latter forms are sometimes referred to as wire corals or whip corals). They may be only a few centimetres tall, or they may reach a length of several metres in the case of some wire corals (Wagner et al. 2012). The core of the colony is a stalk composed of chitin that varies in colour from jet black in the main stem to golden yellow at branch tips. The stalk is lined with spines that may be simple cones, or may be covered with denticles, or may even be branched and antler-like. In life, the stalk is encased in living tissue, so black corals are not actually black. Unlike other skeletonised cnidarians in which the polyps are recessed within the skeleton, those of antipatharians are entirely external to it. As a result, black corals are rarely found in locations where there is a lot of moving sediment in the water, as they lack the ability to entirely retract the polyps to protect them from abrasion. The individual polyps are usually only a few milimetres wide and up to a few centimetres tall when extended. All antipatharian polyps have six tentacles and six primary mesenteries; depending on the species, there may also be four or six secondary mesenteries, though members of the family Cladopathidae lack secondary mesenteries altogether.

The most recent classification of the Antipatharia divides it between seven families, some of which have been recognised only very recently. Because their deep-water habitat makes the study of live colonies difficult, and many features of the minute polyps become obscured in preserved material, earlier classifications focused heavily on features such as the branching arrangement of the colony, or the morphology of the spines on the skeletal axis. However, these features may be influenced by environmental factors, and their significance may have been overestimated. For instance, a molecular phylogenetic analysis by Brugler et al. (2013) found that the unbranched wire coral genus Cirrhipathes was polyphyletic and not separated from the branched genus Antipathes. Nevertheless, Brugler et al. did find that the higher-level relationships within the Antipatharia were mostly concordant with morphology, including the distinction of the seven families. These relationships included a divergent position for Leiopathes, the only genus with six secondary mesenteries; a clade including the bathyal families Schizopathidae and Cladopathidae, in which the polyps are transversely elongated; a close relationship between the families Myriopathidae and Stylopathidae, with polyps that are not elongated and have relatively short, subequal tentacles; and an association of the families Antipathidae and Aphanipathidae, in which the sagittal tentacles tend to be quite elongate relative to the lateral tentacles. There was still, of course, room for investigation: one notable anomaly is that the type species of Antipathes, A. dichotoma, was identified as a member of 'Aphanipathidae' rather than 'Antipathidae'. If correct, this would mean that aphanipathids should be called antipathids, while antipathids would be... something else.

REFERENCES

Brugler, M. R., D. M. Opresko & S. C. France. 2013. The evolutionary history of the order Antipatharia (Cnidaria: Anthozoa: Hexacorallia) as inferred from mitochondrial and nuclear DNA: implications for black coral taxonomy and systematics. Zoological Journal of the Linnean Society 169: 312-361.

Roark, E. B., T. P. Guilderson, R. B. Dunbar, S. J. Fallon & D. A. Mucciarone. 2009. Extreme longevity in proteinaceous deep-sea corals. Proceedings of the National Academy of Sciences of the USA 106 (13): 5204-5208.

Wagner, D., D. J. Luck & R. J. Toonen. 2012. The biology and ecology of black corals (Cnidaria: Anthozoa: Hexacorallia: Antipatharia). Advances in Marine Biology 63: 67-132.

A Brain Explosion

Elliptical star coral Favia speciosa, photographed by Utsunomiya.
For today's random taxon, I drew the Faviinae. This is a subfamily within the Faviidae, commonly known as 'brain corals' and recognised as an important family among the tropical reef-builders. Families of corals have generally been distinguished by the arrangement and morphology of skeletal structures within the coral cup: Faviidae were characterised by having trabeculae (the calcareous fibres forming the basis of the skeletal septa) arranged in one or two fans, with more or less regular marginal teeth at the top of the septum. The Faviidae were divided into two subfamilies, the Faviinae and Montastreinae, based on whether the budding of polyps takes place inside (Faviinae) or outside (Montastreinae) the individual cups in a colony. Several genera recognised within the Faviinae were mostly distinguished by their colony form and how the individual polyps are arranged (Budd & Stolarski 2011).

Leptoria phrygia, photographed by Neville Coleman.
And if any of you were wondering about the use of the past tense in the last paragraph, that is because more recent studies have been pretty unanimous in indicating that the system just described is in need of a significant shake-up. As noted here in an earlier post, molecular studies have indicated that coral taxa distinguished by septal characters are widely problematic. A broad phylogenetic study of corals by Fukami et al. (2008) found that, of sixteen recognised families tested, eleven were polyphyletic. Faviidae, in particular, were scattered between no less than seven of the twelve supported clades identified by Fukami et al. within the broader 'robust clade'. Some of the larger genera, such as the type genus Favia, were also polyphyletic and dispersed between multiple clades. The level of discordance between morphological classification and molecular phylogeny is reflected by the fact that Fukami et al.'s large clade XVII, containing members of the families Faviidae, Merulinidae and Pectiniidae, has since been informally dubbed the 'Bigmessidae' (Huang et al. 2011). The 'Bigmessidae' also includes the genus Trachyphyllia, a morphologically very variable coral that is generally found free-living, either solitary or colonial, among the sand at the very base of coral reefs (Best & Hoeksema 1987). Trachyphyllia has been treated by some authors as its own family, or regarded by others as an unusual member of the Faviinae.

Maze brain coral Goniastrea australensis, photographed by David Witherall.
As yet, no formal reclassification of the corals has been proposed, but when it eventually is, it is likely that there will be no Faviidae at all. The type species of the family, Favia fragum, is closely related to the type species of another family, Mussidae, and the latter name is the one with priority. Interestingly, both these taxa are found in the Atlantic Ocean, and the molecular phylogenies do support a separation of the Atlantic faviids from the Pacific species. Also, it is still possible that morphological characters will play their part in the coming coral reclassification: even though the broader scale features of the septa and colony form have proven vulnerable to convergence, smaller scale features of the skeletal microstructure promise to be less discordant with molecular phylogenies (Budd & Stolarski 2011).

REFERENCES

Best, M. B., & B. W. Hoeksema. 1987. New observations on scleractinian corals from Indonesia: 1. Free-living species belonging to the Faviina. Zoologische Mededelingen 61 (27): 387-403.

Budd, A. F., & J. Stolarski. 2011. Corallite wall and septal microstructure in scleractinian reef corals: comparison of molecular clades within the family Faviidae. Journal of Morphology 272: 66-88.

Fukami, H., C. A. Chen, A. F. Budd, A. Collins, C. Wallace, Y.-Y. Chuang, C. Chen, C.-F. Dai, K. Iwao, C. Sheppard & N. Knowlton. 2008. Mitochondrial and nuclear genes suggest that stony corals are monophyletic but most families of stony corals are not (order Scleractinia, class Anthozoa, phylum Cnidaria). PLoS ONE 3 (9): e3222.

Huang, D., W. Y. Licuanan, A. H. Baird & H. Fukami. 2011. Cleaning up the ‘Bigmessidae’: molecular phylogeny of scleractinian corals from Faviidae, Merulinidae, Pectiniidae and Trachyphylliidae. BMC Evolutionary Biology 11: 37.

From Three to Two

(I've been waiting three and a half years to use Neil's icon.)

The mysterious anabaritids of the Lower Cambrian have been referred to on this site before. In the earlier, somewhat brief post, I referred to their triradial structure and uncertain, though probably coelenterate-grade, relationships. In the time since that post appeared, the anabaritids have been the subject of a review by Kouchinsky et al. (2009) that brought together a lot of the previously scattered information on these animals.

The image of an anabaritid in the previous post showed the best known species, Anabarites trisulcatus. However, this was not the only species in the group. The image just above, from Kouchinsky et al. (2009), shows another species, Anabarites biplicatus, recorded from the Siberian Platform. This species differs from A. trisulcatus in that it started out life triradial (albeit with the internal dividing ridges between the lobes only weak), but as it grew it lost its triradiality and became more bilateral (cross-section below from Kouchinsky et al.):

Some of my readers may remember that Cambrian problematica were something of a cause célèbre during the mid-90s when a lot of journals and magazines ran features on them (probably inspired to a certain degree by Stephen Jay Gould's somewhat dreadful book Wonderful Life). In the more academic corners of this pageant, the triradiality of anabaritids (as well as some other early animals such as Tribrachidium) garnered them a certain degree of attention. It was suggested by some that they might represent a unique animal lineage that was eventually superseded by our own bilateral dynasty. However, the changing symmetry of Anabarites biplicatus serves as a reminder that we should not be too hasty to assign great significance to such features. Indeed, in the modern fauna, nematodes are partially triradial (they have a triradial head structure, with one upper and two lower lips around the mouth). Though the affinities of anabaritids are somewhat debatable, the most popular scenario is that they are related to cnidarians: their tubes bear a certain resemblance to the polyps of some medusozoans. Cnidarians also exhibit a wide variety of symmetries, such as the tetraradial organisation of scyphozoans and the hexaradial organisation of hexacorals. Without preserved soft tissue to inform us what the organisation of the inhabitant animal may have been, it is difficult to say just how much weight the triradiality of the anabaritid tube should be given.

REFERENCE

Kouchinsky, A., S. Bengtson, W. Feng, R. Kutygin & A. Val'kov. 2009. The Lower Cambrian fossil anabaritids: affinities, occurrences and systematics. Journal of Systematic Palaeontology 7 (3): 241-298.

Conical Problematica

Scattered throughout the fossil record are little mysteries, organisms whose remains have been preserved but which are not obviously relatable to any more familiar group. Either their remains are too simple to preserve much evidence of their affinities (as with the 'tubular problematica' I've discussed before), or they are too distinct from other organisms for their affinities to be clear, or both, or some other reason. Unless they are particularly common or otherwise significant, most of these problematica are probably doomed to remain so. Case in point:



The figures above show Asymmetroconus splendidus, described by Korde in 1975 from the Albian (early Cretaceous) of the Crimea. The photos are of thin sections of the fossils; the complete skeleton would have probably been shaped rather like a wine goblet. The largest specimens of Asymmetroconus were just under 8 mm in height. In the same paper, Korde described a number of similar fossils aged from the Albian to the Danian (earliest Palaeocene), assigning them all to the new order Asymmetroconida. Korde attributed the asymmetroconidans to the Hydroconozoa, a group of similar fossils he had himself described previously from the early Cambrian. Hydroconozoa have generally been assigned to the Cnidaria, though their exact position therein remains obscure. Asymmetroconida resembled hydroconozoans in being small and goblet-shaped, with a conical interior to the cup and a basal globular hollow below the point of the cone. However, they differed from Cambrian hydroconozoans in their skeletal microstructure and in the asymmetry of the cup, with one side much thicker than the other. Rozanov & Zhuravlev (1992) later dismissed the idea of Mesozoic hydroconozoans, stating simply that structures described as such had 'little in common with this group'. No alternative identification of the Asymmetroconida has ever been proposed, and they do not appear to have been properly studied since Korde's original description.


Reconstruction of the hydroconozoan Hydroconus mirabilis, from Rozanov & Zhuravlev (1992). Whether actually related or not, the Asymmetroconida would have probably looked superficially similar.

REFERENCES

Korde, K. B. 1975. [Hydroconozoa from Cretaceous and Palaeocene deposits of the Crimea]. In: Shimansky, V. N., & A. N. Soloviev (eds) Razvitie i smena organičeskogo mira na rubeže Mezozoâ i Kajnozoâ. Novye dankye o razvitii fauny pp. 32-38. Nauka: Moscow. [in Russian]

Rozanov, A. Yu., & A. Yu. Zhuravlev. 1992. The lower Cambrian fossil record of the Soviet Union. In: Lipps, J. H., & P. W. Signor (eds) Origin and Early Evolution of the Metazoa pp. 205-282. Plenum Press: New York.

Thought-Crime: I Have Slandered the Gelatinous

The video at the end of this post comes via Miriam Goldstein. The beasty (or, technically speaking, colony of beasties) that it shows is a siphonophore not unlike the Physophora hydrostatica illustrated by Haeckel near the beginning of the 1900s:



Siphonophores were covered here back in August, and that post will (hopefully) help you understand just what you're looking at here. Nevertheless, the video above still stunned me. I had assumed that Haeckel had been employing a certain amount of (not entirely uncharacteristic) artistic licence in drawing those curly palpons (the fat tentacle-like structures) - the still photos of siphonophores I had seem looked as if they would be fairly stiff in real life. How wrong I was! Watch the video - those things are sinuous.



Need I remind you that siphonophores can be up to 30 m in length, and severely toxic? Pleasant dreams, kiddies.

Coral Love

The solitary coral Javania erhardti, a member of the 'caryophylliine' family Flabellidae, from here.

Cnidarian classification can be a terrible thing. Like many other groups of soft-bodied animals, useful characters for distinguishing taxa can be few and far between, and those few characters that are available may be difficult to identify and readily subject to evolutionary change. Corals are no exception. The current generally-used classification of living corals divides them between seven suborders, distinguished from each other primarily by the structure of their septa, the ribs of skeletal material within each polyp. The Caryophylliina, for instance, have simple septa, with little in the way of internal ornamentation. Members of this suborder have been found from as long ago as the early Jurassic, not too long after the modern Scleractinia corals originated in the mid-Triassic. Caryophylliines remain a successful group - nearly five hundred species have been described, and they include both shallow-water and deep-sea forms. The majority of caryophylliines do not contain zooxanthellae (symbiotic dinoflagellates) and while there are some colonial forms, the majority are solitary.

Which sounds all very fine and dandy, but is not anywhere near as informative as one might think. It doesn't take much reading between the lines to note that the 'Caryophylliina' with their 'simple septa' are essentially united by the absence of the features characterising other suborders. As such, it is hardly surprising that they should be nearly as old as the Scleractinia as a whole, because they are quite possibly phylogenetically equivalent to the Scleractinia as a whole. A caryophylliine is simply a coral that doesn't put on airs. This possibility is bourne out by molecular analysis (Le Goff-Vitry et al., 2004), which divides scleractinians between two major clades that have been dubbed the 'robust' and 'complex' clades (or 'Robusta' and 'Complexa' by Kerr, 2005)*. Though not corresponding to earlier morphological divisions, the two clades are not without morphological support. 'Robust' corals have solid, heavily calcified skeletons, while 'complex' corals have lighter, more porous skeletons. Caryophylliines, it turns out, are distributed between both clades, and multiple subclades within those clades. Even the type family of the 'suborder', the Caryophylliidae, is not monophyletic, with a suggested division between no less than five clades scattered among the Robusta and Complexa (Kerr, 2005).


Skeleton of the 'caryophylliine' coral Deltocyathus rotulus, showing the fairly plain septa. Photo by Stephen Cairns.

The necessary changes to scleractinian classification could yet be even more radical. Medina et al. (2006) found that the Complexa were more closely related to the soft-bodied, skeletonless Corallimorpharia than they were to the Robusta. It remains an open question whether the calcified skeleton evolved independently in the two clades, or whether the corallimorpharians represent a secondary loss of the skeleton, but my one suspicions lean towards the latter, especially since it has been demonstrated that the loss of the ability to secrete a skeleton does not constitute a death sentence for a coral (Fine & Chernov, 2007)*. Skeletal construction may yet play a role in coral taxonomy, as researchers identify more reliable ultrastructural characters (Stolarski & Roniewicz, 2001), but I think we can safely say that the 'Caryophylliina' as we have hitherto known it is, well, dead in the water.

REFERENCES

Fine, M., & D. Tchernov. 2007. Scleractinian coral species survive and recover from decalcification. Science 315 (5820): 1811.

Kerr, A. M. 2005. Molecular and morphological supertree of stony corals (Anthozoa: Scleractinia) using matrix representation parsimony. Biological Reviews 80: 543-558.

Le Goff-Vitry, M. L., A. D. Rogers & D. Baglow. 2004. A deep-sea slant on the molecular phylogeny of the Scleractinia. Molecular Phylogenetics and Evolution 30: 167-177.

Medina, M., A. G. Collins, T. L. Takaoka, J. V. Kuehl & J. L. Boone. 2006. Naked corals: skeleton loss in Scleractinia. Proceedings of the National Academy of Sciences of the USA 103 (24): 9096-9100.

Stolarski, J., & E. Roniewicz. 2001. Towards a new synthesis of evolutionary relationships and classification of Scleractinia. Journal of Paleontology 75 (6): 1090-1108.

E Pluribus Unum

For many people, the name "Ernst Haeckel" is most associated with slightly dodgy illustrations of vertebrate embryos that have doomed his memmory to be quote-mined by people with an agenda to push for all eternity. For others, though, the epitome of Haeckel's work lies in the many spectacular illustrations of invertebrates and protozoa he produced in such works as his reports on the biological material collected by the HMS Challenger expedition, and his 1899-1904 Kunstformen der Natur ("Artforms in Nature"). With their awe-inspiring detail and spectacular presentation, the plates he produced are more than just technical illustrations, they are true works of art. Perhaps among the greatest of his productions were the plates of siphonophores, an example of which is shown above. Baroque tentacled horrors, they loom out of the page threatening to engulf Dunwich. I wouldn't be able to tell you whether Lovecraft had ever seen one of Haeckel's illustrations to inspire him in his descriptions of the twisted hybrid offspring of Yog-Sothoth, but the resemblance is uncanny.

Siphonophores are planktonic cnidarians (the group that includes corals and jellyfish), distantly related to hydras (a good online reference on siphonophores has been put together by Casey Dunn). The most familiar member of the group is Physalia, the Portuguese man of war (so-called because of a supposed resemblance to that form of ship), but on the whole Physalia is not very typical of the order. All siphonophores are colonial, in their way - incomplete budding leads to the production of a colony of generally large numbers of metabolically interconnected zooids that are developmentally homologous to the more independent polyps of other cnidarians. However, the individual zooids of siphonophores are each highly specialised for separate divided functions such as feeding, reproduction or motility, meaning that siphonophore zooids are incapable of living independently of the colony. Perhaps more than any other group of organisms, the siphonophores challenge the question of what defines an individual or a colony, which has led to their description as "superorganisms".

Siphonophores have been divided into three main groups, the Cystonectae, Physonectae and Calycophorae, but the phylogenetic analysis of Dunn et al. (2005) found calycophores to be nested within physonects, the two together forming a clade they named the Codonophora. Cystonects (which include Physalia) form the sister-group to the codonophores, and share a colony morphology characterised by a division between a terminal pneumatophore (float) and the siphosome, the region of the colony containing feeding and reproductive zooids coming off a central stalk (in Physalia the central stalk is relatively short, but other siphonophores will have exceedingly long colonies). In the "physonects", the pneumatophore and siphosome are separated by the nectosome, a region of generally bell-shaped zooids called nectophores specialised for motility. In the calycophores, the pneumatophore has been lost and the colony is composed of the nectosome and siphosome. The illustration at the top of the post represents the physonect Physophora hydrostatica - the pneumatophore is the bulb-shaped structure at the top, with the zooids of the nectosome between the pneumatophore and the tentacle-like structures representing the top of the siphosome. These latter structures are not actually tentacles (the tentacles are the filaments radiating from the siphosome) but palpons, zooids whose function remains unknown but has been suggested to be related to excretion or defense. Underneath the palpons are the gonophores, the reproductive zooids, with separate male and female forms (males and females may both be present in a single colony, or there may be colonies of separate sexes). The large funnels like the horn of an old gramophone are gastrozooids, the feeding individuals. The clubbed side-branches on the trailing tentacles are tentilla, and contain concentrations of nematocysts for capturing prey. Most codonophores (but not cystonects) also have shield-like gelatinous bracts protecting the siphosome. Cystonects also have structures called gonodendra, which are concentrations of gonophores, palpons and also specialised nectophores that can propel a detached gonodendron through the water. Many codonophores are bioluminescent - the bracts may contain luminescent cells, and at least one member of the genus Erenna has flashing red tentilla that probably function as lures. The Physonecta illustrated above has only one iteration of the siphosome, but in other forms (such as the one illustrated below in another Haeckel plate) the clusters of palpons, gastrozooids and gonophores may form iterative elements that repeat continuously down the growing stem.



Despite what can only be described as their inherent coolness, siphonophores as a group are poorly known. Like other planktonic cnidarians, their gelatinous structure makes them quite frail and difficult to collect. The entire colony may be only loosely connected by the slender stem, such as in the example just above. Some siphonophores reach spectacularly large sizes - species of Apolemia may be more than 30 m in length, yet only a few centimetres in diameter. Attempts to net such specimens using conventional means would be lucky to retrieve anything more than disassociated mush.

REFERENCES

Dunn, C. W., P. R. Pugh & S. H. D. Haddock. 2005. Molecular phylogenetics of the Siphonophora (Cnidaria), with implications for the evolution of functional specialization. Systematic Biology 54: 916-935.

Haeckel, E. 1899-1904. Kunstformen der Natur. Bibliographisches Institut: Leipzig & Wien.

Buddenbrockia: The Gift that Keeps on Giving

A few days ago, I commented on the recent publication by Jiménez-Guri et al. (2007) on the basal myxozoan and parasitic worm Buddenbrockia (I'd recommend reading that post before this one - see Pharyngula for another good post on the same paper). I really should have held my tongue just a little longer, because just today I received notice of yet another paper on Buddenbrockia (Morris & Adams, 2007), and it makes the creature even cooler than I realised. Which is a big thing, because I already thought Buddenbrockia was a very cool little animal.

Firstly, I'll briefly cover the 'relationships of the Myxozoa' section, because there's not too much to say there. Morris and Adams support the idea of Buddenbrockia and Myxozoa as basal bilaterians, in a similar grade (though not necessarily clade) with Acoela and Mesozoa. However, they defer to past analyses in this, and their points against a cnidarian position for Buddenbrockia (primarily possession of muscle blocks and Hox genes) were both dealt with by Jiménez-Guri et al., with the former present in some cnidarians and the latter shown to be contamination (ironically, Morris and Adams note the similarity of one 'myxozoan' Hox gene to vertebrates and suggest the possibility of lateral transfer). That said, Jiménez-Guri et al. did not include any Acoela, which lie outside the Protostomia + Deuterostomia clade, in their analysis, and I feel that the possibility cannot be ruled out that their inclusion may have affected the result. As always in science, there is the prospect of further testing.

The really interesting part of Morris and Adams, however, lies in their detailed description of Buddenbrockia's development, which is bizarre and incredible and makes me all the more sympathetic to earlier researchers who did not even recognise myxozoans as animals. Buddenbrockia reproduces by means of spores (produced asexually, as far as I can tell - I haven't come across any reference to cross-fertilisation methods) that accumulate in the central cavity of the worm until it bursts open, releasing the spores into the host's coelom from whence they are ejected by the host into the surrounding water. It is not clear how exactly the spores infect a new host, but when we see them next they have hatched into unicellular amoeboids (the pre-saccular phase) within the basal lamina of the host. Note that I said unicellular - on PZ Myers' post linked to above, David Marjanović corrected him on the point that myxosporeans aren't really ever unicellular in the strict sense but syncytial (large multinucleate mass without individual cells, also called plasmodial). Nevertheless, Buddenbrockia unicells do have only a single nucleus. Because of the laminal connection between individual zooids in Bryozoa, it is possible that Buddenbrockia infection can spread through a colony at this stage.

The unicells then push their way through the host muscle tissue and aggregate together under the peritoneum. And when I say aggregate, I mean they are packed. Morris and Adams use the term 'pseudosyncytium' to describes how the cells are pressed so close together that it becomes nigh on impossible to distinguish individual cells, if indeed they remain individual cells (Morris & Adams were unable to satisfactorily resolve this question). The host cells surrounding the pseudosyncytium react strongly, encapsulating the pseudosyncytium within cytoplasmic extensions and necrotic cells. It is from this 'pseudocapsule' as the authors call it that the mature worm develops.

Now comes one really cool point - this does not happen the same way in every host species. In most host species, the mature parasite develops muscle blocks and forms the worm-like form we've been discussing so far. In Cristatella, the muscle blocks never develop, and the mature Buddenbrockia forms an ovoid sac, the Tetracapsula form (believed once upon a time to be a separate taxon). Morris & Adams' observations are of the worm form, and that's what we'll continue to explore.

Within the pseudocapsule, the individual unicells form junctions with each other, and start growing out into the host coelom as the 'worm'. Fibres are extruded from the pseudosyncytium that anchor it to the surrounding host cells. Within the worm, the pseudosyncytial cells differentiate into an outer layer of ectoderm and two inner layers of mesendoderm. The worm hollows out as it grows and a fibrous lamina develops between the mesoderm and endoderm. The endoderm develops into spore-producing cells, while the mesoderm forms the muscle blocks.

The muscle blocks develop from the base of the worm at the pseudosyncytium. One of the more unusual suggestions about Buddenbrockia muscle develop is that it may involve the co-option of host myofibres. If correct, this suggestion may explain why Buddenbrockia doesn't develop muscle tissue in all host species, as maturation of Buddenbrockia in Cristatella (as well as development of the closely-related Tetracapsuloides, which also doesn't develop muscles) takes place entirely in the coelom rather than in the cell wall. It also correlates with Buddenbrockia's unusual develop of muscle blocks within already-differentiated mesoderm. However, Morris & Adams didn't find any direct evidence for host co-option.

Eventually, the mature worm is released from the coelom wall to become the free worm we all know and love. Whether the worm is released from the pseudosyncytium which remains behind to generate other worms, or whether the pseudosyncytium comes free with the worm and is resorbed is currently unknown, though Morris & Adams cite past observations of worms with scalloped ends as suggesting the latter option.

As I already noted, the malacosporean (Buddenbrockia + Tetracapsuloides) lifecycle with multiple individuals coming together to form a single mature form is completely unlike any other class of animal. In many ways, it is more reminiscent of the slime moulds, a point noted by Morris & Adams, particularly the so-called 'cellular slime moulds'. Cellular slime moulds are now regarded as forming two separate groups - the dictyostelids in Amoebozoa and the acrasids in Heterolobosea. Neither of these groups is related to myxozoans (or, for that matter, to each other), so this form of life cycle has evolved independently in all three. It would be fascinating to see if the separate unicells aggregating together all derive from a single infective spore multiplying at the unicellular stage, or whether the products of multiple infections with different genetic identities can form a single pseudosyncytium. Aggregation of different genetic 'individuals' can happen in slime moulds - such chimaeras seem to be at a functional disadvantage to genetically pure aggregates, but this may be compensated for by the ability to form a larger colony (Foster et al., 2002). For Buddenbrockia, living in a soup of host-supplied nutrients with no need to move particularly far, the functional restrictions on chimaera formation might be even less.

REFERENCES

Foster, K. R., A. Fortunato, J. E. Strassmann & D. C. Queller. 2002. The costs and benefits of being a chimera. Proceedings of the Royal Society of London Series B – Biological Sciences 269: 2357-2362.

Jiménez-Guri, E., H. Philippe, B. Okamura & P. W. H. Holland. 2007. Buddenbrockia is a cnidarian worm. Science 317: 116-118.

Morris, D. J., & A. Adams. 2007. Sacculogenesis of Buddenbrockia plumatellae (Myxozoa) within the invertebrate host Plumatella repens (Bryozoa) with comments on the evolutionary relationships of the Myxozoa. International Journal for Parasitology 37 (10): 1163-1171.

The return of Buddenbrockia

In a previous post I briefly mentioned the mysterious worm Buddenbrockia plumatellae Schröder 1910, listed by Haszprunar et al. (1991) as an "extant problematicum", and alluded to how the true identity of this critter was rather unexpectedly resolved a few years back (Okamura et al., 2002). Further work on the position of Buddenbrockia appeared this past Friday in Science and adds a further small twist to the tale (Jiménez-Guri et al., 2007).

Buddenbrockia is a parasite of freshwater bryozoans, small, sessile, colonial animals that are sometimes referred to as 'moss animals' for little apparent reason ('moss animals' happens to be the English translation of 'Bryozoa'). After Schröder first described it in 1910, he suggested two years later that it was related to nematodes due to its mesodermal muscle blocks. A relationship to trematodes (flukes) was suggested around the same time by Braem (Okamura et al., 2002).

Okamura et al. (2002) examined the ultrastructure of Buddenbrockia, and found that it possessed an inner and outer layer of cells separated by the aforementioned muscle blocks, of which there are four arranged around the body. There is no through gut. Most significantly, the outer cell layers (the mural cells) contained polar capsules. Polar capsules are rounded organelles containing a tightly coiled filament that can be ejected at great speed. The polar capsules of Buddenbrockia were very similar to those of Tetracapsula, a basal member of the Myxozoa (and also a bryozoan parasite).

In my earlier post, I referred to Myxozoa as the least animal-like of animals, and I unreservedly stand by that statement. Myxozoa are parasites and fall into two classes. The class Malacosporea contains the aforementioned Tetracapsula (and now Buddenbrockia) and are parasites of bryozoans and fish. The class Myxosporea is considerably larger and are parasites of fish and annelid worms. As an interesting aside, the Myxosporea was previously divided between two classes of superficially very distinct appearance, the fish-parasitic Myxosporea and the annelid-parasitic Actinosporea. This distinction was removed in the mid-1980s when it was shown that spores of the myxosporean Myxobolus fed to tubificid annelids developed into the actinosporean Triactinomyxon (Wolf & Markiw, 1984). The two 'classes', therefore, represent different stages in the myxosporean life cycle.

So derived are myxosporeans relative to other animals that until fairly recently they were not even recognised as animals at all, being instead classified with the parasitic protozoa (Sporozoa and Microsporidia). Myxosporeans contain very few cells, and are contained completely within the cells of the host for part of the life cycle. A connection with animals was first suggested on the basis of the presence in myxosporeans of collagen, and on the near-identical ultrastructure of the myxosporean polar capsule with the cnidarian nematocyst (stinging cell) (see here for more details).

Even after myxozoans were recognised as animals, however, their position within the animal kingdom proved very hard to establish. Obviously, the ultrastructural similarities supported a connection with the cnidarians (the parasitic cnidarian Polypodium [not to be confused with the fern genus Polypodium] was particularly suggested as a close relation). However, some molecular studies supported a connection with bilaterians, most notably the reported presence in myxozoans of bilaterian-like Hox genes.

When Okamura et al. (2002) published their ultrastructural study of Buddenbrockia, they felt that its worm-like structure supported a bilaterian relationship for myxozoans, and highlighted previous molecular studies connecting myxozoans to nematodes. Jiménez-Guri et al.'s (2007) publication, however, turns this on its head, and returns Myxozoa to a position with the Cnidaria. This was done through a Bayesian phylogenetic analysis of some 129 proteins in 47 animals (plus 13 opisthokont outgroups) in a range of higher taxa. Buddenbrockia proved to have a significant branch length (easily the longest on the tree). interestingly, parsimony analysis (which is very vulnerable to long-branch attraction) of the data set resulted in Buddenbockia associating with a clade of nematodes + platyhelminthes, the other long-branch taxa analysed. It is likely that long-branch attraction has also been the culprit for such associations in the past.

And those bilaterian-like Hox genes? Well, the authors of the current study managed to isolate the supposed myxozoan Hox genes from host species that were not even infected with myxozoans. They were unable to isolate them from myxozoan samples that had been scrupulously cleared of any host tissue. Therefore, the supposed myxozoan Hox sequences represent contamination from the hosts, and are not myxozoan at all.

REFERENCES

Haszprunar, G., R. M. Rieger & P. Schuchert. 1991. Extant "problematica" within or near the Metazoa. In The Early Evolution of Metazoa and the Significance of Problematic Taxa (A. M. Simonetta & S. Conway Morris, eds.) pp. 99-105. Cambridge University Press.

Jiménez-Guri, E., H. Philippe, B. Okamura & P. W. H. Holland. 2007. Buddenbrockia is a cnidarian worm. Science 317: 116-118.

Okamura, B., A. Curry, T. S. Wood & E. U. Canning. 2002. Ultrastructure of Buddenbrockia identifies it as a myxozoan and verifies the bilaterian origin of the Myxozoa. Parasitology 124: 215-223.

Wolf, K., & M. E. Markiw. 1984. Biology contravenes taxonomy in the Myxozoa: new discoveries show alternation of invertebrate and vertebrate hosts. Science 225: 1449-1452.