The Glyceriforms: Stabby Worms and Grabby Worms

Historically, the annelid worms have been considered a difficult group to classify. Whereas most of the recognised families have been fairly well established, higher taxa uniting these families have tended to be a bit on the vague side. Nevertheless, there are some supra-familial groups that can be considered well established, one such group being the Glyceriformia.

Specimen of Goniadidae (head to the right), from NOAA Fisheries.

The glyceriforms are two families of marine worms, the Glyceridae and Goniadidae. More than a hundred species are known in this clade (over forty glycerids and over sixty goniadids), found in habitats ranging from the intertidal to the abyssal. They range in size from about a centimetre in length to well over half a metre. The front end of the body tapers to a narrow, elongate conical point in front of the mouth, bearing two terminal pairs of small, slender appendages that may correspond to the antennae and palps of other worms. Eyes may be present or absent. The pharynx forms a remarkably elongate, eversible proboscis. In Glyceridae, the proboscis ends in a ring of four hook-shaped jaws, all similar to each other. In Goniadidae, the arrangement of jaws is more complex with the usual arrangement being small micrognaths on one side of the ring and larger macrognaths on the other. Glycerids usually have a transparent skin and an overall red or white colour reflecting the coloration of the internal fluids (red-coloured individuals are sometimes known as 'bloodworms', as are many other similarly coloured worm-like invertebrates). Goniadids have a more opaque cuticle and often have an iridescent sheen (Rouse & Pleijel 2001).

Glycera dibranchiata with everted proboscis, from the Yale Peabody Museum.

Glyceriforms most commonly live as burrowers in muddy or sandy substrates though some live on the surface of rocks. Most are carnivores of active invertebrates such as crustaceans or other worms; some may be detritivores. They may be vagile or they may construct permanent galleries of burrows with multiple entrance and exit openings in which they wait to lunge at anything foolish enough to pass nearby. In glycerids, the stabby jaws are associated with venom glands leading to ducts opening through pores on the jaw's underside. In some species, this venom is strong enough to cause a painful reaction in humans (though I haven't come across any references to long-term consequences). Goniadids lack venom glands and seem to rely on the physical use of their jaws to capture prey. As with many other marine worms, reproduction happens via pelagic epitokes. As a suitable time approaches (Prentiss, 2020, records goniadid epitokes emerging only during a full moon), the glyceriform worm undergoes a metamorphosis involving the break-down of the digestive system and enlargement of the parapodia. The transformed epitokes swim towards the surface where they release gametes through ruptures of the body wall, ending their life in a suicidal orgasm.

Close-up on proboscis of Glycera alba, copyright Hans Hillewaert.

Because of their hardened jaws, which are mostly constructed of protein but partially mineralised, glyceriforms have quite a good fossil record compared to many other worms (Böggemann 2006). Fossilised glyceriform jaws have been found as far back as the Triassic and are little different from those of modern glyceriforms. Body fossils are, unsurprisingly, much rarer but a worm from the Carboniferous Mazon Creek fauna, Pieckonia helenae, has been identified as a stem-group goniadid. The glyceriform body plan seems to have been a very successful one, remaining essentially unchanged over hundreds of millions of years.

REFERENCES

Böggemann, M. 2006. Worms that might be 300 million years old. Marine Biology Research 2: 130–135.

Prentiss, N. K. 2020. Nocturnally swarming Caribbean polychaetes of St. John, U.S. Virgin Islands, USA. Zoosymposia 19: 91–102.

Rouse, G. W., & F. Pleijel. 2001. Polychaetes. Oxford University Press.

How the Worm Turns (Into a Worm)

Those of you who have suffered through some of my posts on turrids may recall me discussing the subject of how differences in the mode of development of marine organisms relate to their classification. Features that were once considered of high significance are affected by whether the animal develops as a free-swimming larva or is nourished by a yolk supply provided in the egg, and may change more readily than previously thought. And indeed, it turns out that there are some cases where both developmental modes can be found in a single species.

Boccardia polybranchia, from here.

Boccardia is a genus of twenty-odd species of marine worm belonging to the family Spionidae. These are sedentary worms, living in tubes that they construct for themselves out of sediment bound together by mucus, or that they bore into substrates such as mollusc shells or coral. Boccardia and other spionids have a pair of long palps extending from the head that they use for feeding, sweeping them around to gather up detritus and such. Boccardia differs from other genera in the Spionidae in having branchiae (vascularised appendages that function as gills) starting on the second segment of the body, and two differentiated spine rows on the fifth segment with falcate spines in the upper row and bristle-tipped spines in the lower row (Williams 2001).

One of the best-studied Boccardia species is B. proboscidea, a species about one or two centimetres in length found around various parts of the Pacific, including along the western coast of North America. Boccardia proboscidea is very catholic in its habitat preferences: it can be found in the intertidal or shallow subtidal zones, and anywhere from mudflats to rubble to reefs to burrowed into the shells used by hermit crabs (Gibson et al. 1999). It also shows the aforementioned variation in larval development: some individuals hatch as small larvae and live and feed as plankton, others feed on the yolks from nurse eggs and don't hatch until they reach a more advanced stage of development. Whichever way the individual develops, the resulting adult seems to be more or less the same.

Nevertheless, it would be fair to wonder if this variation is as it appears. Combine the variation in development with the variation in habits, and you might wonder whether two or more morphologically similar species are being confused. However, not only are the adults of each larval type completely interfertile, but differently developing individuals may even come from a single egg case. Gibson et al. (1999) compared individuals of this species from two widely separated populations both morphologically and genetically, and found that while there were some differences between the populations, there was little or no difference between developmentally distinct individuals within each population. How and why this developmental variation is maintained seems to be an open question but there is some evidence that other spionids may show the same plasticity. After all, it doesn't matter how you get there, so long as you get there.

REFERENCES

Gibson, G., I. G. Paterson, H. Taylor & B. Woolridge. 1999. Molecular and morphological evidence of a single species, Boccardia proboscidea (Polychaeta: Spionidae), with multiple development modes. Marine Biology 134: 743–751.

Williams, J. D. 2001. Polydora and related genera associated with hermit crabs from the Indo-West Pacific (Polychaeta: Spionidae), with descriptions of two new species and a second polydorid egg predator of hermit crabs. Pacific Science 55 (4): 429-465.

Pontodrilus: Earthworms by Sea

Earthworms are primarily a terrestrial and freshwater group, sensitive to changes in the quality of their habitat. But there are some earthworm species that are tolerant of more saline environments. One such species is Pontodrilus litoralis, a widespread earthworm found in warm coastal habitats around the world, being recorded from such far-flung places as the Caribbean, the Mediterranean, Australia and Japan. The species is found in sandy or muddy soils in coastal habitats, including beaches, estuaries and around the roots of mangroves, and is able to tolerate salinities from 5 to 25 parts per thousand—that is, from fresh water to close to the standard salinity of sea water (Blakemore 2007).

Pontodrilus litoralis in its natural habitat, from here.

Pontodrilus litoralis is one of five species currently recognised in the genus Pontodrilus, though many more have been recognised in the past (Blakemore, 2007, listed eighteen species and subspecies now regarded as synonyms of P. litoralis). Characteristic features of the genus include an absence of nephridia in the anterior segments, and tubular prostrate organs opening to male pores on the eighteenth segment. The other Pontodrilus species have more restricted, non-coastal ranges; one, P. lacustris, is found free-swimming in Lake Wakatipu in New Zealand, whereas the other three are found in terrestrial habitats in Sri Lanka, China and Tasmania.

How P. litoralis achieved its wide distribution is currently unknown. If it arose prior to the separation of the land-masses on which it is now found then it would have had to have survived almost unchanged for hundreds of millions of years, which seems on the face of it unlikely. It seems more credible that it has dispersed more recently from its original point of origin, but while its green, spindle-shaped cocoons are often found attached to floating vegetation we do not know how long they can stand immersion in full-strength salt water. Nor do we know just where P. litoralis originated. It was first described in 1855 from the French Riviera so many authors have assumed the species is Mediterranean in origin. However, the distribution of related species seems to make an Indo-Pacific origin more likely. It may well be that P. litoralis was spread from its original home by humans, carried with rocks and sand used for ballast.

REFERENCE

Blakemore, R. J. 2007. Origin and means of dispersal of cosmopolitans Pontodrilus litoralis (Oligochaeta: Megascolecidae). European Journal of Soil Biology 43: S3—S8.

A Place for Worms

When we think of endangered species, we tend to focus on the charismatic vertebrates, such as pandas, parrots, tigers or turtles. But endangered species may come from all walks, crawls or wriggles of life. Have you ever considered, for instance, the plight of endangered earthworms?

An unidentified species of Glossodrilus, copyright Thibaud Decaens.

Glossodrilus is a genus of earthworms found in tropical and subtropical regions of Central and South America. They are mostly fairly small as earthworms go, averaging only a few centimetres long and one or two millimetres in diameter. The largest, G. oliveirai from Brazil's Roraima State and Guyana, is about 25 centimetres long; the smallest, G. tico from Roraima and Venezuela, is less than two centimetres in length. Most species lack pigmentation, meaning that they appear greyish from the colour of their gut contents. A single species, G. freitasi from Amapá State in Brazil, is a bright violet in colour. Other diagnostic features of the genus include: eight setae per segment, arranged in regular series; a pair of (or sometimes one) calciferous glands sitting above the oesophagus in segments XI to XII; two or three pairs of lateral hearts in segments VII to IX, and two pairs of intestinal hearts in X and XI; and a pair of testes in segment XI. Glossodrilus is distinguished from a closely related earthworm genus, Glossoscolex, by the absent of a pair of muscular copulatory chambers associated with the male ducts in the latter genus (Righi 1996).

Over sixty species have been assigned to Glossodrilus; as is usual with earthworms, they are mostly distinguished by internal characters such as features of the reproductive systems. They are most diverse in upland regions, with many species inhabiting high rain forest. A few species in the northernmost or southernmost parts of the genus' range inhabit secondary grasslands. Glossodrilus species are conspicuous by their absence in the Brazilian central plateau, and only infrequently present in lowland Amazonia (Righi 1996).

And this is where the question of conservation comes in. You see, the greater number of Glossodrilus species are known only from a very restricted area (Lavelle & Lapied 2003). Part of this may be an artefact of sampling: in more recent decades, our understanding of South American earthworm diversity has been heavily shaped by one researcher, Gilberto Righi of the Universidade de São Paulo (I referred to him briefly in an earlier post on Amazonian earthworms), and we know little of areas where Righi did not collect specimens himself or from where he did not receive specimens supplied by ecological surveys. Nevertheless, sampling has probably been extensive enough to expect that the low number of shared species between different regions will hold firm at the broad scale at least. Most Glossodrilus species (and other native South American earthworms) are dependent on old-growth habitats; as land is cleared for farming, forestry and the like, exotic and invasive earthworm species take over. It would be all to easily for the little Glossodrilus to find themselves homeless, and slip into extinction without any to mark their passing.

REFERENCES

Lavelle, P., & E. Lapied. 2003. Endangered earthworms of Amazonia: an homage to Gilberto Righi. Pedobiologia 47: 419–427.

Righi, G. 1996. Colombian earthworms. Studies on Tropical Andean Ecosystems 4: 485–607.

Serpularia: A Rightly Forgotten Problematicum

I think it may be time to rock out something that hasn't been seen on this site for a while. Horns at the ready...

(Credit, again, to Neil from Microecos). And I'm afraid that may just be the most excitement that we get in this post. While some fossils are problematic because they're so strange that they can't be easily compared to living animals, others are problematic simply because they're rubbish.

In 1840, the palaeontologist Georg Graf zu Münster ('Graf' being a German title that generally gets translated as 'Count') published his Beiträge zur Petrefakten-Kunde, in which he described a number of fossils held in his collection. This book included a section on fossils from the Ordovician Orthoceratite Limestone of the Fichtel Mountains in Bavaria. Which, close to the end, included this little tidbit:

Unter mehreren Bruchstücken einiger mir noch unbekannten Versteinerungen kommen auch einige röhrenformige Korper vor, welche ich anfänglich für den von Murchison aus der 27sten Tafel abgebildeten Myrianites hielt, allein genaue Untersuchung zeigte, dass diese Korper formliche Schalen hatten und daher vielleicht zu den Serpuliten gehört hatten, daher ich sie vorläufig Serpularia genannt habe. Aus der Taf. IX. Fig. 14 und 15 sind zwei Arten von dergleichen Bruchstücken abgebildet; Fig. II. Serpularia crenata; glatt gebogene Röhre, aus dem Rücken crenulirt. Fig. 15. Serpularia bicrenata; glatte etwas zusammengedrückte ganz grade Röhrchen, die an beiden Seiten crenulirt sind.

Translated with the help of Google Translate, I think this means: "Among several fragments of fossils unknown to me occured a tube-like body, which I initially took for Myrianites as figured by Murchison in the 27th plate, until close examination showed that this body had distinct signs of segmentation and was therefore perhaps one of the Serpulidae. Therefore, I have provisionally called it Serpularia. On Plate IX Figs 14 and 15 are shown two types of the like fragments; Fig. 14, Serpularia crenata: smooth curved tube crenulated from the back. Fig. 15, Serpularia bicrenata: smooth, slightly compressed, quite straight tubes that are crenulated on both sides".

Münster's (1840) original figures of the two Serpularia.

As perfunctory as it was, that seems to be all there was to say on the matter. The good Graf's Serpularia has pretty much never been mentioned again*, beyond being cited to cause a name change in a later homonymous gastropod genus, and a brief listing in Howell's (1962) coverage of worm fossils for the Treatise on Invertebrate Paleontology that adds nothing to the original description.

*Though if it were to be mentioned again, it would probably have to be under a different name. The name 'Serpularia' had earlier been used by Fries in 1829 for a genus of slime moulds. At the time, slime moulds were treated as fungi, and hence fell under the purview of botanical rather than zoological names, but with the recognition that they are amoebozoans an increasing number of authors would move them into the field of the Zoological Code.

Münster believed that his fossils belonged to the Serpulidae, a family of annelid worms. Annelids, being mostly soft and squishy things that do not stand up well to decay, have a pretty deplorable fossil record, but serpulids are a bit of an exception. These are sessile worms that secrete a calcareous tube in which they live their lives (modern serpulids appeared on this site in this post). Unfortunately, while these tubes are eminently fossilisable, they are also a bit nondescript, and have little to mark them as uniquely serpulid.

Because of the dominance of annelids among modern worms, there has been a definite tendency in the past to assume that any given worm-like fossil represents an annelid. Howell's (1962) aforementioned list of annelids includes the Ediacaran Spriggina (identity still under debate, but probably not an annelid) and the Cambrian Pikaia (now generally regarded as an early chordate). Similarly, any worm-like tube has been assumed a serpulid. But even among annelids, serpulids are not the only tube-bearing worms. At least two other families, the Sabellidae and the Cirratulidae, include species producing calcareous tubes. There are also other groups of non-annelid worms that, though relatively uncommon or unprepossessing today, may have been more prominent in the past. After all, we are talking here about a period of hundreds of millions of years. We know that vertebrates have gone through a great deal of evolutionary change over that period; why should we assume that worms have not?

So while fossils have been assigned to the serpulids going back as far as the Cambrian (if not beyond), there is little reason to take those assignations at face value. When so-called Palaeozoic serpulids have been examined critically in recent years, they have so far proven to lack features that would definitely confirm their identification (Vinn & Mutvei 2009). Weedon (1994) found that Palaeozoic fossils that had been assigned not only to the Serpulidae, but to the modern genus Spirorbis, had a shell microstructure that suggested a relationship to bryozoans or brachiozoans rather than to annelids. Without a similar close analysis, we could not assume a priori that Münster's Serpularia were not serpulids, but odds would currently be against it.

REFERENCES

Howell, B. F. 1962. Worms. In: Moore, R. C. (ed.) Treatise on Invertebrate Paleontology pt W. Miscellanea: Conodonts, Conoidal Shells of Uncertain Affinities, Worms, Trace Fossils and Problematica pp. W144–W177. Geological Society of America and University of Kansas Press.

Münster, G. 1840. Beiträge zur Petrefacten-Kunde von Herm. v. Meyer und Georg Graf zu Münster vol. 3. In Commission der Buchner'schen Buchhandlung: Bayreuth.

Vinn, O., & H. Mutvei. 2009. Calcareous tubeworms of the Phanerozoic. Estonian Journal of Earth Sciences 58 (4): 286–296.

Weedon, M. J. 1994. Tube microstructure of Recent and Jurassic serpulid polychaets and the question of the Palaeozoic 'spirorbids'. Acta Palaeontologica Polonica 39 (1): 1–15.

Exogone sexoculata, a Worm of the Interstitial

Drawings of head and representative chaetae of Exogone sexoculata, from San Martín (2005).
The sort-of-randomly chosen subject of today's post is the marine annelid worm Exogone (Parexogone) sexoculata, a member of the interstitial fauna around the coast of Australia. A previous record of this species from Italy has since been re-identified as the related species E. gambiae (Lanera et al. 1994). Exogone sexoculata is found among sand, mud, algae and dead coral, and in depths of up to 24 m (San Martín 2005). Despite the species name, it actually has four eyes, plus two eyespots that lack the lenses of the true eyes. As this is a fairly standard arrangement for Exogone species, E. sexoculata can't really claim to have one of the most distinguishing of species names.

Unidentified species of Exogone (in its epitokous form, perhaps?) from the Biodiversity Institute of Ontario.
Exogone sexoculata is a member of the family Syllidae, whose sometimes dramatic reproductive habits were discussed in an earlier post. Like other syllids, most Exogone species go through the process known as epitoky, where reproductively mature individuals metamorphose into a more mobile form, with enlarged eyes and parapodia. In the subfamily including Exogone, Exogoninae, the entire animal transforms into an epitoke (rather than epitokes budding off as may happen in other syllids). After releasing its gametes in the water column, the epitoke returns to the substrate and transforms back into the interstitial form. Females of Exogoninae brood their fertilised eggs attached to their body, and juvenile worms hatch out without going through a planktonic larval stage. In Exogone, the brooded eggs are attached on the underside of the female's body, whereas in other genera brooding may be dorsal. Exogone is also distinguished from other exogonine genera by the absence of a covering of papillae, the presence of only a single pair of tentacular cirri, and palps that are fused along all or almost all of their length. Exogone sexoculata is distinguished from other species in the genus by the absence of dorsal cirri on the second chaeta-bearing segment, its long median antenna, and by features of the chaetae (San Martín 2005).

REFERENCES

Lanera, P., P. Sordino & G. San Martín. 1994. Exogone (Parexogone) gambiae, a new species of Exogoninae (Polychaeta, Syllidae) from the Mediterranean Sea. Bolletino di Zoologia 61 (3): 235-240.

San Martín, G. 2005. Exogoninae (Polychaeta: Syllidae) from Australia with the description of a new genus and twenty-two new species. Records of the Australian Museum 57: 39-152.

Earthworms of the Amazon (Taxon of the Week: Urobenus buritis)

This week's Taxon of the Week post has been delayed a little: getting hold of some of the reference for it required me to enter a real library and locate an actual journal physically printed on paper. Always an experience.

Urobenus buritis (no pictures of this one, I'm afraid) is an earthworm only recorded from the region of Manaus in the state of Amazonas in northern Brazil. This may or may not be significant. Perhaps not surprisingly, collections of earthworms around the Amazon have been somewhat scattered; most of our knowledge of the area (including U. buritis itself in Righi et al., 1976) can be credited to the work of one researcher, Gliberto Righi. Nevertheless, what we do know suggests that many species in the area have very localised ranges (James & Brown, 2006). Earthworms are poor dispersers and many of them are very particular in their habitat preferences, making them highly vulnerable to disturbance.

The genus Urobenus possesses three pairs of calciferous glands in segments VII-IX (many other glossoscolecid genera possess only two*) and can be distinguished from the similar genus Rhinodrilus by the shape of the glands. In Rhinodrilus, all three pairs of glands are tubular; in Urobenus, the first two pairs are tubular and the third pair (in segment IX) is sac-shaped (Righi, 1985). Urobenus buritis has three pairs of spermathecae, delicate anterior septa and the male pores opening at segments 20-21 (U. brasiliensis, which U. buritis was originally described as a subspecies of, has them at segments 19-20).

*Offhand, this is something to consider when thinking about how vertebrate diversity compares to invertebrate diversity. Two externally quite similar taxa, that the vast majority of people would regard as both being 'just worms' and pretty much identical, may actually differ in something as seemingly basic as how many organs they have.

I haven't seen the original description of Urobenus buritis, so I can't say whether there is any information on its lifestyle, but the closely related U. brasiliensis is an epigeic (living above the ground) species inhabiting leaf litter (James & Brown, 2006). Many of the earthworms around the Amazon have cyclical life histories to deal with the contrast between wet and dry seasons. Tuiba dianae migrates towards drier forest as flood waters rise, maintaining a distance of at least five metres from the water's edge. Other species, such as Andiorrhinus tarumanis, climb up the nearest tree during the wet season and take up residence in patches of leaf litter trapped in the forest canopy while the ground is flooded. Whether Urobenus buritis indulges in such behaviour is currently unknown.

REFERENCES

James, S. W., & G. G. Brown. 2006. Earthworm ecology and diversity in Brazil. In Soil Biodiversity in Amazonian and other Brazilian Ecosystems (F. M. S. Moreira, J. O. Siqueira & L. Brussaard, eds) pp. 56-116. CABI Publishing.

Righi, G. 1985. Sobre Rhinodrilus e Urobenus (Oligochaeta, Glossoscolecidae). Boletim de Zoologia 9: 231-257.

Righi, G., I. Ayres & E. C. R. Bittencourt. 1976. Glossoscolecidae (Oligochaeta) do Instituto Nacional des Pesquisas da Amazônia. Acta Amazônica 6 (3): 335-367.

Of Interstitial Annelids (Taxon of the Week: Pisionidae)

Head end of Pisione. Photo by Greg Rouse.

The Pisionidae are tiny (about a centimetre or less in length), transparent, mostly marine annelid worms (a single species has been described from fresh water - San Martín et al., 1998). They are usually counted as members of the meiofauna, the community of minute animals (and other heterotrophic eukaryotes) that live in the spaces between sand grains, though Rouse and Pleijel (2001) quibbled with this assignation on the grounds that pisionids are too large relative to average sand grain size. Nevertheless, they are probably predators of meiofaunal organisms that they capture with their venomous jaws. About forty species of Pisionidae are currently recognised; however, in light of their ease of being overlooked, it would not be surprising if many species remain undescribed. Most pisionids are found in shallower and intertidal waters but some have been recorded at depths of up to 1000 m. The life histories of few pisionids have been studied but fertilisation is direct with males possessing paired ventral "penes" on varying numbers of segments that transfer the aflagellate sperm to the females' seminal receptacles. Larvae of the species Pisione remota are planktic feeders, capturing food by means of a mucus net.

Phylogenetic studies of Pisione remota have provided strong support for a position of pisionids among the scale worms, a clade of annelids normally characterised by the possession of paired chitinous elytra (Wiklund et al., 2005). This is supported both by molecular analysis and by similarities in the venom glands. The study of Wiklund et al. (2005) went so far as to find P. remota nested among species of the elytra-bearing family Sigalionidae and suggested that 'pisionids' may in fact be derived sigalionids (however, only a single pisionid and three sigalionids were included in the analysis so further more extensive studies are required to confirm the families' relative positions). The implied loss of the elytra in pisionids is usually suggested to be an adaptation to their infaunal habitat and small size. However, other infaunal scale worms have not lost their elytra so this may not be the entire story.

REFERENCES

Rouse, G. W., & F. Pleijel. 2001. Polychaetes. Oxford University Press.

San Martín, G., E. López & A. I. Camacho. 1998. First record of a freshwater Pisionidae (Polychaeta): description of a new species from Panama with a key to the species of Pisione. Journal of Natural History 32 (8): 1115-1127.

Wiklund, H., A. Nygren, F. Pleijel & P. Sundberg. 2005. Phylogeny of Aphroditiformia (Polychaeta) based on molecular and morphological data. Molecular Phylogenetics and Evolution 37 (2): 494-502.

Building a Home of Your Own (Taxon of the Week: Hydroides)

Close-up of the front end of the tubeworm Hydroides elegans, showing the double-level operculum. Photo by John Lewis.

This week's highlight taxon is the worm genus Hydroides. Hydroides unites about eighty species of the family Serpulidae, the tubeworms, an easily-found component of many a beach all over the world. Serpulids (previously commented on here) are a distinctive group of annelid worms that secrete themselves a tubular shell of calcium carbonate in which they live permanently attached to a rock or some other substrate (not uncommonly, that "other substrate" will be another tubeworm, leading to the production of tangled masses of worm tubes). Many authors have divided serpulids between two families, Serpulidae proper and Spirorbidae, but phylogenetic studies place spirorbids as a derived subgroup of Serpulidae rather than their sister group (Kupriyanova et al., 2006; Lehrke et al., 2006). Hydroides is not a spirorbid, so it remains in Serpulidae whatever the preferred arrangement.

With more than eighty species, Hydroides is a reasonably large assemblage, and it is distributed worldwide. Among the more distinctive features of the genus is the division of the spinose operculum into two tiers, a lower (rather daisy-like, in my opinion) ring called the funnel and an upper ring of spines called the verticil. The features and arrangement of the verticil spines are often the main distinguishing characters between species, but this can be complicated somewhat by changes in spine morphology over the course of growth and regeneration (ten Hove & Ben-Eliahu, 2005). It is also notable that at least one Caribbean species, Hydroides spongicola, has been recorded as showing a tendency towards reduction of the operculum; this species lives in close association with the highly toxic touch-me-not sponge (Neofibularia nolitangere) and presumably the host sponge's irritating spicules offer all the protection the tubeworm needs (Lehrke et al., 2006).



The first species of Hydroides to be described was H. norvegica (now Hydroides norvegicus to match the gender of the genus) in 1768 by Johan Ernst Gunnerus, Bishop of Trondhjem*. An English translation of Gunnerus' original description was published by Moen (2006); as shown in the reproduction above from Moen (2006) of the first few lines, the original is not among the easiest of reads. Interestingly enough, Gunnerus bestowed a different name on the animal ("Hydroides norvegica") from the tube that it lived in ("Serpula norvegica") - I suspect that this may represent a different philosophy from the present about how to deal with animals versus their products, as opposed to any doubt about whether the one had produced the other. In a letter to Linnaeus (or von Linné as he'd become by then), Gunnerus also described his doubt about just what type of animal it was he'd described - a hydrozoan, or possibly a sea cucumber? It seems that its sessile lifestyle had quite put him off the idea of it being a worm**.

*Among other animals described by Gunnerus are the basking shark and Lineus longissimus, the world's longest ribbon worm and possibly the longest of all living animals.

**Remember, Gunnerus and Linnaeus were both working in a largely non-evolutionary paradigm. As such, their classifications were not intended to reflect an organism's "affinities" in the sense that we'd understand them, but rather to reflect how their overall features compared to other animals.


Congregation of Hydroides ezoensis on the side of a ship. Image from Science in Salamanca.

These days, Hydroides species are among the most intensely studied of all marine annelids. The motives for this interest are primarily economical - not surprisingly, Hydroides have often earned the ire of humans through their penchant for attaching themselves to the humans' nice clean boats and jetties. A number of Hydroides species have been transported and established outside their native ranges by human agency - probably in ballast water for the most part, though H. ezoensis was transported from Japan to France on the shells of oysters imported to stock oyster farms (Thorp et al., 1987). With this economic focus, it is not surprising that the majority of studies appear to have been on factors affecting larval development and settlement. One interesting point is that Hydroides larvae are far more likely to settle somewhere already inhabited by tubeworms than on a completely fresh surface (Scheltema et al., 1981), a common pattern among sessile organisms that do not reproduce by budding. After all, there's safety in numbers.

REFERENCES

Hove, H. A. ten, & M. N. Ben-Eliahu. 2005. On the identity of Hydroides priscus Pillai 1971 – taxonomic confusion due to ontogeny in some serpulid genera (Annelida: Polychaeta: Serpulidae). Senckenbergiana Biologica 85 (2): 127-145.

Kupriyanova, E. K., T. A. Macdonald & G. W. Rouse. 2006. Phylogenetic relationships within Serpulidae (Sabellida, Annelida) inferred from molecular and morphological data. Zoologica Scripta 35: 421-439.

Lehrke, J., H. A. ten Hove, T. A. Macdonald, T. Bartolomaeus & C. Bleidorn. 2006. Phylogenetic relationships of Serpulidae (Annelida: Polychaeta) based on 18S rDNA sequence data, and implications for opercular evolution. Organisms Diversity & Evolution 7 (3): 195-206.

Moen, T. L. 2006. A translation of Bishop Gunnerus’ description of the species Hydroides norvegicus with comments on his Serpula triqvetra. Scientia Marina 70S3: 112-123.

Scheltema, R. S., I. P. Williams, M. A. Shaw & C. Loudon. 1981. Gregarious settlement by the larvae of Hydroides dianthus (Polychaeta: Serpulidae). Marine Ecology Progress Series 5: 69-74.

Thorp, C. H., S. Pyne & S. A. West. 1987. Hydroides ezoensis Okuda, a fouling serpulid new to British coastal waters. Journal of Natural History 21 (4): 863-877.

My Genitals Just Grew Eyes and Swam Away: The Life of a Syllid Worm

The syllid worm Myrianida pachycera with a chain of developing epitokes. Photo by Leslie Harris.

It is currently Sex Week at Deep-Sea News, and this post is written in honour of that event. Sex, after all, is a big part of biology (hur, hur, hurr).

Marine worms of the family Syllidae are small polychaetes, usually less than two centimetres in length and about a millimetre in width. Many syllids are interstitial (living buried in sand), others live in association with corals or sponges (on which they may feed). The main feature of syllids that has captured people's attention, however, is their extremely multifarious sex lives (Franke, 1999).

Syllids are one of a number of polychaete families exhibiting what is called epitoky, a significant metamorphosis between the juvenile or atokous and sexually mature or epitokous stages. The originally benthic worm grows long, extended parapodia, and the eyes and other sensory organs become greatly enlarged. More significantly, the reproductive tissue expands to fill almost the entire body, and other organs such as the digestive system degenerate, so the final epitokous worm is basically a highly sensitive pelagic gonad. In other worms such as members of the family Nereididae, the mature worm will swim up into the water column to meet up with other pelagic gonads, after which the entire mass will explode in a cloud of gametes.

Syllids, however, do things a little differently. Seemingly not as keen on ending life with a bang, they have evolved a number of ways to continue on with their life after maturity. The original syllid mode of reproduction involved metamorphosis to an epitoke as in other related polychaete families, but without the degeneration of the digestive system. And nereidids release their gametes by fatally rupturing the body wall, syllid epitokes release theirs through modified nephridia. Afterwards, the syllid epitoke is able to return to the ocean floor and partially revert back to its original atokous form, ready to reproduce another year. This mode of reproduction, called epigamy, remains the one used in two of the four syllid subfamilies, Eusyllinae and Exogoninae, as well as part of the subfamily Autolytinae.


Some epigamous syllids brood their eggs after fertilisation, and may even retain the offspring after hatching. This is an illustration of one such syllid, Exogone rubescens, from here.

Two other syllid lineages, the remainder of Autolytinae and the subfamily Syllinae, developed a mode of reproduction called schizogamy - the joy of budding. In schizogamous syllids, instead of the whole worm developing into an epitoke, a separate epitoke buds off the original atoke. In the most basic form of schizogamy, it is the posterior part of the worm that metamorphoses into the epitoke, in most cases growing its own separate, fully-developed head before breaking away from the anterior "parent" part (some Syllinae have headless epitokes). In some syllids, another epitoke may begin developing in front of the original epitoke before it breaks away, and possibly even more, so that the animal turns into a chain of developing worms. Others produce a number of epitokes growing in a bunch. After the epitoke(s) break off, the remaining atoke will regenerate any losses. Indeed, the atoke may begin regenerating even before the epitoke breaks off - the left and right sides of the new posterior part grow on either side of the epitoke, and once the epitoke is gone they fuse together down the middle.



Very few syllids have developed true asexual reproduction, where they fragment to give rise to new atokes instead of epitokes. But no survey of syllid budding would be complete without mention of the most bizarre of all syllids, the deep-sea sponge-dwelling Syllis ramosa. In this species (shown above in a drawing from here), buds develop laterally but don't detach from the parent worm. As these lateral buds grow, they start growing their own lateral buds, so that over time the worm develops into a branched network, spreading through the channels of its hexactinellid host.

REFERENCES

Franke, H.-D. 1999. Reproduction of the Syllidae (Annelida: Polychaeta). Hydrobiologia 402: 39-55.

More Crunchy Scleritome Goodness

Yep, it's time for another installment on my favourite assemblage of polyphyletic problematica. Two significant new additions have been made to the repertoire of articulated scleritomes:


An assortment of articulated Lepidocoleus (each about an inch long). Take especial note of figure d! From Högström et al. (in press).

Firstly, does anyone remember machaeridians? The animals for which I labelled the discovery of a specimen preserving soft tissue as "the greatest announcement of 2008"? (And now that 2008 has been and gone, I wholeheartedly support that designation.) Well, there's more. Högström et al. (in press) have described a collection of articulated machaeridians from the Devonian Hunsrück Slate in Germany, and among them is a second specimen with soft-tissue remains!

There are a few reasons why this is a very satisfying discovery. Firstly, the specimen supports the annelid affinities proposed for machaeridians by Vinther et al. (2008) when the first soft-tissue specimen was described from the Ordovician Fezouata Formation of Morocco. Secondly, the Hunsrück specimens represent a different family (Lepidocoleidae) from the Fezouata specimen (Plumulitidae), which confirms that the machaeridians do represent a monophyletic grouping, and are not unrelated taxa that have convergently developed similar sclerite morphologies (always a possibility with animals only known from disarticulated sclerites). [I should point out that articulated lepidocoleid scleritomes have been found before, but not preserving any soft tissue.] Whereas plumulitids appear to have had rather loosely articulated sclerites, giving them an ornamental spined appearance, lepidocoleids had a much more tightly-woven, armour-plated scleritome (see the earlier post for a comparative picture).

And thirdly, just as a kind of cherry on the top, one of the other Hunsrück specimens, while it may not have soft-tissue remains, has something else to commend it that some palaeontologists would probably find even more exciting. It's sitting neatly positioned at the end of a well-preserved trail. Trace fossils are often the best evidence you can get for working out the behaviour of extinct animals, but it can be a frustrating exercise because often the best conditions for preserving traces are not very good for preserving the animals that made them, and vice versa. When I was on a palaeontology field trip as an undergrad, I was told that one of the lecturers had a standing offer of a crate of beer for anyone who found a body fossil in association with a trace fossil. Finding a machaeridian in association with a trace fossil, I feel, would have warranted at least two.


Tommotiids. On the left, the articulated Eccentrotheca. On the right, sclerites of Micrina placed to show their suggested life positions. Photo from here.

The second big announcement comes from the Cambrian Arrowie Basin of South Australia - another articulated tommotiid! Last year, I reviewed a new reconstruction of the tommotiid Micrina presented by Holmer et al. (2008). This reconstruction, with two valves on either side of an attached stalk (though do note, it was a reconstruction rather than a description of an articulated specimen, so it's not immune to revision), was intriguing in its resemblance to a basal brachiopod (to which group of Recent animals tommotiids are almost certainly related, sharing a very similar shell microstructure). However, it was in fairly stark contrast to the previously described articulated tommotiid Eccentrotheca, which has its sclerites stacked one above another to form a tubular structure (Skovsted et al., 2008). The new articulated tommotiids described by Skovsted et al. (in press) may just go some way towards bridging the divide.


Paterimicra. On the left, apical (above) and lateral (below) views of the large sclerite S1. On the right, S1 in suggested life position with an S2 sclerite within the triangular notch. Scale bars for this and the next figure = 200 μm. Figures from Skovsted et al. (in press).

Skovsted et al. (in press) have described articulated scleritomes of the tommotiid Paterimitra. Like Eccentrotheca, Paterimitra had more sclerites in its scleritome than the two suggested for Micrina. However, unlike the tubular Eccentrotheca, Paterimitra had the scleritome dominated by a single basal S1 sclerite, shaped a bit like a wonky four-sided pyramid with one side extended out further than the other. On each of these two opposing sides was a deep notch or sinus, with the notch on the steeper side much deeper and with an outwards-pointing flange at the bottom. Inside this deeper notch would sit the smaller, triangular S2 sclerite, which also had an outwards-pointing flange at its bottom end that lined up with the flange of the S1 to form a loose protective tube. There were also a number of smaller, twisted-plate-shaped L sclerites. I have to confess, I'm still trying to work those out to some extent, but as far as I can tell they stacked on one side on the top of the S1 to form some degree of protective covering for the opening of the pyramid.


Lateral view of a partially-articulated Paterimicra specimen with L sclerites fused to the top of the S1 sclerite. It is noteworthy that the available articulated Paterimicra specimens with fused sclerites (this one, which is the only one to retain the L sclerites in place, particularly) show signs of injury or pathology at some point in development. This suggests that sclerite fusion was a pathological response in these individuals, not a normal part of scleritome development, which may partially explain why articulated specimens are so rare. Figure from Skovsted et al. (in press).

Skovsted et al. (in press) suggest a sessile life position for Paterimitra with the S1+S2 pyramid standing point-downwards, attached to the substrate by an organic stalk (like the pedicle of modern sessile brachiopods) passing between the flanges of the sclerites. They suggest Paterimitra may have been derived from an Eccentrotheca-like ancestor by the enlargement of the basal sclerites. Another Eccentrotheca-type lineage may have lost the sclerites entirely to give rise to the modern worm-like phoronids (though note that a few recent authors have suggested, based on soft-body characters shared with linguloids, that phoronids may be derived from within brachiopods). Micrina (in its suggested form) could be derived from a Paterimitra-type animal essentially by the loss of the L-sclerites. After that, it's simply a matter of extending the two remaining sclerites so that the shell is able to fully close (both Micrina and Paterimitra would have been permanently open to some degree, though Holmer et al., 2008, suggested a protective guard of long setae for Micrina), and what you've got is a quite passable basal brachiopod!

REFERENCES

Högström, A. E. S., D. E. G. Briggs & C. Bartels (in press, 2009) A pyritized lepidocoleid machaeridian (Annelida) from the Lower Devonian Hunsrück Slate, Germany. Proceedings of the Royal Society of London Series B - Biological Sciences.

Holmer, L. E., C. B. Skovsted, G. A. Brock, J. L. Valentine & J. R. Paterson. 2008. The Early Cambrian tommotiid Micrina, a sessile bivalved stem group brachiopod. Biology Letters 4 (6): 724-728.

Skovsted, C. B., G. A. Brock, J. R. Paterson, L. E. Holmer & G. E. Budd. 2008. The scleritome of Eccentrotheca from the Lower Cambrian of South Australia: lophophorate affinities and implications for tommotiid phylogeny. Geology 36 (2): 171-174.

Skovsted, C. B., L. E. Holmer, C. M. Larsson, A. E. S. Högström, G. A. Brock, T. P. Topper, U. Balthasar, S. Petterson Stolk & J. R. Paterson. (in press, 2009). The scleritome of Paterimitra: an Early Cambrian stem group brachiopod from South Australia. Proceedings of the Royal Society of London Series B - Biological Sciences.

Vinther, J., P. Van Roy & D. E. G. Briggs. 2008. Machaeridians are Palaeozoic armoured annelids. Nature 451 (7175): 185-188.

Separating Segments

The marine worm Perinereis amblyodonta (image from here).

Struck, T. H., N. Schult, T. Kusen, E. Hickman, C. Bleidorn, D. McHugh & K. M. Halanych. 2007. Annelid phylogeny and the status of Sipuncula and Echiura. BMC Evolutionary Biology 7: 57.

This was published last year, but I only discovered it yesterday, and had a serious "Why didn't anybody tell me about this earlier?" moment. I would of liked to have known that a significant contribution had been made to one of the harder questions in animal phylogeny - the interrelationships of the annelids.

Annelids have long been victim to a certain chauvinism in systematics. They've been treated as kind of the poor cousin to the other major animal phyla*, coupled with an idea that they were in some way "primitive". A number of other phyla, most notably the arthropods and molluscs, have at various times been explicitly or implicitly regarded as derived from annelid ancestors. It must be stressed that in very few of these cases of proposed annelid ancestry was a direct connection made to any specific annelid subgroup. Annelid ancestry was less of a rigorous hypothesis and more of a vague assertion, in the same vein as suggestions of a "thecodont" ancestry of birds.

*Though they still had the flatworms to look down on, at least.


Christmas tree worm (Serpulidae - image stolen from here).

Things changed somewhat with the advent of recent molecular or molecular-influenced phylogenetic studies. Three phyla in particular, the annelids, onychophorans and arthropods, had been united by their metameric segmentation, the regular repetition of separated, similar body segments (this pattern of segmentation has become obscured in many arthropods by specialisation of the separate segments, but is still recognisable in groups such as centipedes and millipedes). More recent analyses have shown the onychophorans and arthropods to have evolved their segmentation separately from annelids, forming a clade with the nematodes and other smaller phyla (the Ecdysozoa) while annelids sit in a clade called the Lophotrochozoa with such phyla as molluscs and brachiopods. Within the trochozoans, metameric segmentation might have been reborn as a defining character of annelids, but the spectre of "ancestral annelids" still didn't quite go away. For instance, while molluscs are mostly unsegmented, one supposedly basal taxon, the Neopilinida, possesses serial repetition of some organs and was suggested to demonstrate the origin of molluscs from a segmented ancestor, with the implication that "segmented" equaled "annelid" generally not too far behind.

Within the annelids, things have not been much better. Traditionally, annelids have been divided into three classes, the Polychaeta (marine worms), Oligochaeta (earthworms) and Hirudinea (leeches), but it has long been recognised that this is not a satisfactory situation. It is well-established that the earthworms and leeches form a single clade, the Clitellata, but within the Clitellata the "oligochaetes" are united only by the absence of the derived features of leeches. Relationships between the Clitellata and Polychaeta have been even more contentious - authors have differed on whether the polychaetes form a monophyletic group that is sister to the Clitellata, or whether the Clitellata is nested within the polychaetes. The polychaetes in turn have been divided between about 80 families, but relationships between those families have been almost completely unresolved.


Giant tube worms (Riftia [Pogonophora] - image from here).

An influential study in annelid phylogenetics was that of Rouse & Fauchauld (1997) which undertook a morphological analysis of the polychaetes. Rouse & Fauchauld found a monophyletic Polychaeta with Clitellata as sister group, and division of the polychaetes into three major clades, named Aciculata, Canalipalpata and Scolecida. They also found that the worms previously regarded as the separate phylum Pogonophora were actually highly derived annelids, as had been suggested by some authors previously. Unfortunately, support for any of the clades found was relatively low, and homoplasy was rampant. The benefits of hindsight allow us to quibble with their choice of outgroups, as well - Rouse & Fauchauld rooted their tree using the small non-segmented worm clades Sipuncula and Echiura (on which see more below) and the arthropods and onychophorans, for which many of the supposedly shared characters were probably homoplasies. A recent major molecular study (Rousset et al., 2007), despite including some 217 taxa, was unable to even demonstrate annelid monophyly, finding many of the supposed 'outgroups', including molluscs, brachiopods and nemerteans, scattered around within the annelids, and recovered almost none of the major clades of Rouse & Fauchauld (1997). However, support over the entire analysis was low, and large chunks of data were missing for many of the taxa included in the analysis.


The echiuran Urechis caupo (image from here).

And so we finally get to Struck et al. (2007). While Struck et al. did not cover quite as many taxa as Rousset et al. (2007), they included more genes and more complete data for the taxa included. Outgroup taxa were drawn from a number of other lophotrochozoan phyla, and the first major result of Struck et al. was the resolution of Annelida as a coherent clade, in contrast to earlier molecular studies. Within Annelida, polychaetes were paraphyletic with regard to Clitellata, and the closest relatives of the Clitellata were the Aeolosomatidae, previously suggested as such on morphological grounds. As for the major morphological clades of Rouse & Fauchauld, while none were strictly monophyletic, the conflict between morphological and molecular results was much reduced. Rouse & Fauchauld's Aciculata was largely monophyletic except for the inclusion of one taxon that had been included with the Scolecida, while the majority of the Scolecida formed two branches of an unresolved trichotomy with the clade including the Clitellata.


(From Struck et al., 2007) ML analysis and BI of Nuc data set with 81 OTUs (-ln L = 66,627.30). 1 of 2 best trees is shown. In the other tree the trichotomy of Nephtyidae, Syllidae, and Pilargidae is resolved with Syllidae being sister of Nephtyidae. OTUs with just the genus names (e.g., Lumbricus) indicate that the sequences from different species of that genus were concatenated. Nuc consisted of 9,482 characters, from which 4,552 (28S rRNA – 2,504; 18S rRNA – 1,375; EF1α – 673) unambiguously aligned and non-saturated ones were included. BS values above 50 shown at the branches on the left; PP's on the right or alone. The branch leading to Ophryotrocha labronica is reduced by 90%. Ophryotrocha individuals have been sampled from a long time culture, which got bottlenecked several times. For 28S rRNA, Capitella forms a long branch and does not cluster with the two other Capitellidae in the analyses. ML settings: Base frequencies: A = 0.2727, C = 0.2495, G = 0.2586, T = 0.2192; Rate matrix: AC, AT, CG, GT = 1.0000, AG = 2.5097, CT = 3.7263; α = 0.4830; Proportion of invariant sites = 0.3103. Models in BI: 28S rRNA, 18S rRNA, EF1α : GTR+I+Γ. Clitellata, Echiura, Siboglinidae, Sipuncula highlighted with gray and bars indicate polychaete groups: orange = outgroup; A, blue = Aciculata; C, green = Canalipalpata; S, red = Scolecida; Ca = Capitellida; Eu = Eunicida; Ph = Phyllodocida; Sa = Sabellida; Sp = Spionida; Te = Terebelliformia; Aph = Aphroditiformia.

Three small groups of worms previously classified as separate phyla were also included among the annelids. The annelid nature of the Pogonophora (corresponding to the Siboglinidae in the tree above) was confirmed, as was its position in the order Sabellida as proposed by Rouse & Fauchauld. The Echiura had also been previously suggested to be derived annelids - while the adults are non-segmented, echiurans do possess chaetae (bristles) like those of annelids and characters related to segmentation have been demonstrated in their larvae. Struck et al. found a relationship between Echiura and the polychaete family Capitellidae, as had been found in previous molecular studies.



Something that is likely to cause more debate, though, is Struck et al.'s finding the Sipuncula (examples shown above in a photo from here) within the annelids. The relationships of the Sipuncula or peanut worms have long been debatable. Some authors have favoured a relationship with annelids, while others have placed them closer to molluscs. Unfortunately, Struck et al. included only one representative of the Sipuncula, and while it was nested well within the annelids its position therein was quite unstable, moving about a lot between analyses. It is worth noting here that the large-scale analysis of animal interrelationships by Dunn et al. available from yesterday as an advance online publication at Nature also positioned Sipuncula within the Annelida. Nevertheless, I can see a lot of further study being done on this result in the future.

A lot remains to be done before we can fully understand the evolution of the annelids, but Struck et al. have certainly made an important contribution. Hopefully, the exorcism of the spectral "ancestral annelid" will encourage the study of annelids not as some relictual halfway-house on the way to somewhere else, but as a specialised and diverse grouping in their own right.

REFERENCES

Rouse, G. W., & K. Fauchald. 1997. Cladistics and polychaetes. Zoologica Scripta 26 (2): 139-204.

Rousset, V., F. Pleijel, G. W. Rouse, C. Erséus & M. E. Siddall. 2007. A molecular phylogeny of annelids. Cladistics 23: 41-63.

Yay, Machaeridians!

I'm back from holiday, and a very good one it was too. Two weeks free from work, free from children, free from responsibilities or restrictions (unless being forced to eat Rocquefort cheese in the hotel room en suite because Jack refused to share a room with the malodorous delicacy counts as a restriction) - what more could one ask? However, the one downside of going away (apart, of course, from the e-mail backlog lurking in wait upon my return) is that I always seem to miss the announcement of some fantastic discovery, and this trip was no exception. Indeed, the publication notice that I found waiting in my in-box was something so huge, so absolutely incredible, so much something that I've been dreaming of for years that I'm worried that the greatest announcement of 2008 has already happened less than two weeks into the year, and it may only be downhill from here. 150 years after their initial discovery, we finally have soft-body remains of a machaeridian!


(from Vinther et al., 2008) a, Holotype YPM 221134, part. b, Camera lucida drawing of the part. Colours indicate the trunk (yellow), parapodia (red), chaetae (gray), attachment of shell plates (green), gut (purple) and dorsal linear structure (blue). Abbreviations: os, outer shell plate; is, inner shell plate; aos, anterior outer shell plate; ls, linear structure; cw, cuticular wrinkles; r, rami evidenced by divergent bundles of chaetae. Scale bar, 5 mm.

Machaeridians were small invertebrate animals found from the Ordovician to the Carboniferous. Like a number of other Palaeozoic shelled taxa, they possessed a body armour composed of multiple sclerites rather than a single solid shell. Despite often being implicitly dismissed as ultimately inferior or primitive with regard to the more familiar shelled animals that we see around us today, the scleritome body plan was actually very successful (the Ordovician to the Carboniferous was no small stretch of time) and survives to this day in groups such as the chitons. Vinther et al. (2008) state that machaeridian sclerites are near-ubiquitous in benthic marine assemblages of the appropriate time period. The problem is that because scleritome plates are not directly fused to each other, on death the scleritome generally becomes disarticulated and it can be exceedingly difficult if not impossible to reconstruct the appearance of the entire animal in life. As a result, scleritome animals have been swept into the too-hard basket in the past and not received the attention that they probably deserve. Even with the massive renaissance of interest in problematica that popularised the Cambrian explosion and the Ediacara fauna in the 1990s, the Machaeridia retained their internationally ignored status. Guesses as to their affinity ranged from molluscs to annelids to arthropods (specifically barnacles) to echinoderms.


(from Caron, 2008) Top, a complete machaeridian scleritome from 425-million-year-old deposits in New York state. Length, 5.4 mm. Bottom, dorsal reconstructions of presumed complete scleritomes (not to scale) showing the diversity of scleritomes within the three families of machaeridians — running upper to lower, the Lepidocoleidae, Turrilepadidae and Plumulitidae. The fossil specimen (top) is a lepidocoleid; that described by Vinther et al. is a plumulitid. All scleritomes are shown with the presumed head to the right. (Top image courtesy of A. Högström; bottom images courtesy of J. Dzik.)

Hence my excitement at the publication of Vinther et al. (2008), which gives us our most complete picture of a machaeridian to date, in the form of an articulated specimen of Plumulites bengtsoni from the Lower Ordovician of Morocco preserving soft body parts. The specimen is not perfect - the preserved soft parts are a little smeared, and the head is missing - but what we have is very informative. Most significant are what seem to be bristle groups running down each side of the body, which the authors feel are probably parapodia. Parapodia are groups of chitinous bristles (chaetae) found in polychaete annelids, and their presence in machaeridians is about as clear as indication of annelid affinities as you can get. Polychaete parapodia are divided into upper and lower clusters of chaetae, and a few of the apparent parapodia in P. bengtsoni do appear to show branching compatible with such an arrangement.

Accepting that machaeridians are closer to annelids than other living animal phyla, it still remains difficult to establish their exact position relative to that group, whether as a stem outgroup or derived ingroup. Phylogeny of living annelids remains almost totally unresolved - annelids possess relatively few phylogenetically useful morphological characters, while molecular analyses are so far unable to even recover their monophyly relative to other phyla (Rousset et al., 2007). A possible relationship to the annelid order Phyllodocida, some members of which possess dorsal plates as shown below in an image of Iphione ovata from here, in Vinther et al.'s phylogenetic analysis was dependent on coding the mineralised machaeridian sclerites as homologous with the chitinous phyllodocidan elytra. Leaving this character as uncertain caused the annelid interrelationships to collapse to a polytomy, with the possibility remaining that machaeridians sit on the annelid stem. As it has also been suggested that phyllodocidans represent a paraphyletic grade relative to other annelids, the two results are not necessarily incompatible.



Machaeridians are but one of a number of groups of Palaeozoic scleritome animals that appear to occupy basal positions on the trochozoan family tree - other examples include the sachitids, tommotiids, wiwaxiids and halkieriids*. Interestingly, there is no indication that these groups all form a clade. Halkieriids (shown at left in an image from Palaeos) may be related to brachiopods (Holmer et al., 2002), to which tommotiids are also ultrastructurally similar (Vinther et al., 2008). Wiwaxiids have been interpreted by different authors as related to molluscs and/or annelids, while molluscs of course include chitons (one extinct order of which - the Multiplacophora - possessed a more complex scleritome than modern species - Vendrasco et al., 2004). It seems not unlikely that the scleritome animals as a whole represent the ancestral group of a brachiopod-annelid-mollusc clade, with the three modern lineages arising independently from scleritome ancestors**. The scleritome would have been reduced and lost in the annelids, while brachiopods and molluscs each independently evolved towards more consolidated armation (if halkieriids are brachiopod relatives, then the two larger terminal plates were expanded in the ancestral brachiopod to the expense of the other plates; the mode of evolution in molluscs is a bit more obscure due to more uncertain phylogeny). Of course, this scenario is still pretty provisional, and there are a number of basal shell-less taxa involved such as Odontogriphus, phoronids and aplacophorans that could still potentially cause it to collapse into a quivering heap. As I've so often said in relation to matters of phylogeny, watch this space.

*Many of these groups have been included in a taxon called Coeloscleritophora that was also suggested to include the strange Cambrian organisms called chancelloriids. Individual sclerites of chancelloriids do have a similar structure to those of other "coeloscleritophorans", but articulated specimens indicate a radically different body plan for the entire animal with sclerites arranged radially over a vase-shaped form. It seems most likely that chancelloriids were sponge-grade animals unrelated to the other "coeloscleritophorans", but the question is complicated by the complete absense of a living sponge group that is even remotely similar to chancelloriids beyond superficial appearance.

**Recent genetic analyses show that these three phyla fall within a clade called Spiralia (or Lophotrochozoa, a name which is used often but for various reasons gives me grief, so I try to avoid it) that also includes a number of other taxa such as nemerteans and platyzoans. Relationships within Spiralia have not been satisfactorily sorted out. It is possible that some other spiralian taxa may fall within the annelid-brachiopod-mollusc clade, which would even further complicate my scenario.

REFERENCES

Caron, J. B. 2008. Ancient worms in armour. Nature 451 (7175): 133-134.

Holmer, L. E., C. B. Skovsted & A. Williams. 2002. A stem group brachiopod from the Lower Cambrian: Support for a Micrina (halkieriid) ancestry. Palaeontology 45 (5): 875-882.

Rousset, V., F. Pleijel, G. W. Rouse, C. Erséus & M. E. Siddall. 2007. A molecular phylogeny of annelids. Cladistics 23: 41-63.

Vendrasco, M. J., T. E. Wood & B. N. Runnegar. 2004. Articulated Palaeozoic fossil with 17 plates greatly expands disparity of early chitons. Nature 429: 288-291.

Vinther, J., P. Van Roy & D. E. G. Briggs. 2008. Machaeridians are Palaeozoic armoured annelids. Nature 451 (7175): 185-188.