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.

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.

Belemnitellidae: Reaching the End of an Era

Fossil cephalopods have featured on this site numerous times in the past. I've talked about nautiloids, I've talked about ammonoids. But one group of cephalopods that I haven't given that much time to to date is the group including the majority of living species: the coleoids. In coleoids, the ancestral cephalopod shell has become reduced and internalised (one group, the octopods, has lost the shell entirely) so it should not come as much of a surprise that their fossil record is more limited than that of other cephalopod groups. Nevertheless, the coleoid lineage does include at least one group known from an abundant fossil record: the Mesozoic belemnites.

Fossil guard of Belemnitella americana, from here, in ventral view with the ventral opening of the alveolus visible as a longitudinal fissure.

Belemnites were a significant part of the marine fauna during the Jurassic and Cretaceous. Externally, they were similar in overall appearance to modern squid, as demonstrated by rare finds of specimens with preserved soft body parts. However, whereas squid have the internal shell reduced to the thin, non-calcified pen, belemnites possessed a well-developed internal shell. The posterior end of the shell was a solid, bullet-shaped rostrum or guard, in front of which was a chambered section known as the phragmocone. Being completely calcified, the rostrum of a belemnite was readily preserved and isolated rostra make up the greater part of the belemnite fossil record (the more delicate phragmocone was less likely to survive the fossilisation process). Different belemnite taxa may be recognised by variations in rostral shape and structure and several families are recognised from various parts of the Mesozoic. The latest surviving belemnite family was the Belemnitellidae.

Reconstruction of a typical belemnite showing the life position of the shell (not actually visible externally), copyright Charlotte Miller.

Belemnitellids are characterised by rostra with an alveolus or pseudoalveolus (an anterior conical depression into which the phragmocone would have originally fit) that opens through a ventral fissure, and longitudinal dorsolateral impressions (Christensen 1997, 2002). The earliest belemnitellids appeared during the early part of the Cenomanian epoch of the Cretaceous period, about 98 million years ago (Christensen 1997). They reached their peak of diversity during the lower Santonian, about 86 million years ago, but they persisted in one form or another right up to the end of the Cretaceous, eventually disappearing in the giant colossal environmental clusterbump that brought that period to a close. Throughout their history, belemnitellids were restricted to the Northern Hemisphere, being known from what is now Europe and North America. By the late Cretaceous, of course, the modern continents were definitely approaching their modern forms and positions but were not quite there yet. For a large chunk of this period, sea levels were higher than they are now so much of modern Europe and the central part of North America were covered by shallow seas. The North Atlantic was still a developing prospect; it looks like there still would have been something of a continental shelf connection between what is now its two sides during the Santonian. This continental shelf and shallow seas was the habitat of the belemnitellids; it appears that they never made the shift to deeper waters. Hence their geographical restriction as the deeper Tethys Ocean still separated Eurasia from Africa and India. When the belemnitellids first appeared, these deeper Tethys waters were home to another belemnite family, the Belemnopseidae (the belemnitellids would make some inroads to the northern coast of the Tethys after the belemnopseids became extinct during the Cenomanian but never anything extensive). A third family, the Dimitobelidae, occupied the position of the belemnitellids in the Southern Hemisphere.

The earliest belemnitellids are known from northern Europe where they presumably evolved from belemnopseid ancestors (Christensen 1997). There do appear to be some questions about whether the belemnitellids as currently recognised represent a monophyletic group or whether the belemnopseid invasion happened more than once. However it be, northern Europe would remain the centre of diversity for the group. They reached North America during the Turonian, about ninety million years ago, but for whatever reason never quite diversified there as much as they did in their homeland. During the Campanian, from about 83 million years ago, there is a period of close to ten million years where belemnitellids disappeared from the North American fossil record entirely. Presumably this represents a local extinction followed by a later recolonisation from Europe.

North American belemnitellids also failed to quite make it to the end of the Cretaceous, dropping out about one or two million years earlier. In Europe, however, three species are known from the period's closing hours. Though not at their earlier levels of success, belemnitellids were diversifying right to the end: the distinctive Fusiteuthis polonica appears well within the last couple of million years. Nevertheless, there was precious little from that part of the world at that time in history that did not have the word DOOM stamped firmly on its forehead and belemnitellids were no exception. Their passing marked the final end of the belemnite hegemony and the stage was now completely clear for the more modern coleoids to rise.

REFERENCES

Christensen, W. K. 1997. The Late Cretaceous belemnite family Belemnitellidae: taxonomy and evolutionary history. Bulletin of the Geological Society of Denmark 44: 59–88.

Christensen, W. K. 2002. Fusiteuthis polonica, a rare and unusual belemnite from the Maastrichtian. Acta Palaeontologica Polonica 47 (4): 679-683.

A Neogene Moon

Back when I was a young lad, some time not so long after the end-Cretaceous extinction, we often spent part of the Christmas holidays camped at the estuary beach-front below my great-grandparents' house. Among the things I recall doing there was going out at low tide with my great-grandmother to dig up cockles for lunch. The New Zealand cockle Austrovenus stutchburyi is not an immediate relative of the bivalves of the family Cardiidae known as cockles in Europe but a member of a different bivalve family, the Veneridae. Venerids are shallowly burrowing bivalves that generally live buried below the sand or mud just shallowly enough to extend their short siphons to the surface for filter-feeding.

Dorsal (left) and lateral views of Marama hurupiensis, from Beu & Maxwell (1990).

Because they live pre-buried in this manner in fairly low-energy habitats, venerids have an excellent fossil record. Marama is a fossil genus of a dozen species of venerids known only from New Zealand and Tasmania (Beu & Maxwell 1990; Beu 2012). The genus was first recognised by Marwick (1927) who divided it between two subgenera, Marama sensu stricto and Hina. Both names derive from Maori names for the moon, presumably in reference to the clams' appearance. Marama species are similar in overall appearance to the modern New Zealand cockle, the primary defining characters of the genus reflecting features of the shell hinge. These include the presence of a moderate anterior lateral tooth or tubercle in the left valve. The size of the species varies from the small M. tumida, a bit less than two centimetres in length, to the relatively large M. hurupiensis which reaches six centimetres in length. The shells are sculpted with concentric lamellae, varying from fine and very dense in M. tumida to strong and widely spaced in M. pristina to weak and sparse in M. ovata.

Marama species are known from the Kaiatan to the Nukumaruan stages in the New Zealand stratigraphic system, corresponding to the ealy Late Eocene to the late Pliocene/earliest Pleistocene in the international stratigraphic divisions. Many regions of the world have their own local stratigraphic divisions that may be used in preference to the glocal system for various reasons. In some cases, this may be because of difficulties in correlating the local geological record to global events. There may not be suitable resources preserved for calculating a deposit's absolute age, or a geographically isolated region may lack fossils of cosmopolitan index species. As a result, it may be possible to recognise temporally successive biotas in a region's palaeontological record without being able to tell for sure whether a given biota is (for instance) Eocene or Oligocene. Alternatively, because stratigraphic divisions are commonly based on biotic turnovers such as mass extinctions, the major local biotic events may not exactly line up with the global average (for instance, the characteristic biota of a given geological period may have persisted longer in one region than it did in another). In the case of the New Zealand palaeontological record, Marama was one of a number of molluscan genera that became extinct towards the end of the Nukumaruan in relation to cooling temperatures representing the onset of the Pleistocene ice ages.

REFERENCES

Beu, A. G. 2012. Marine Mollusca of the last 2 million years in New Zealand. Part 5. Summary. Journal of the Royal Society of New Zealand 42 (1): 1–47.

Beu, A. G., & P. A. Maxwell. 1990. Cenozoic Mollusca of New Zealand. New Zealand Geological Survey Paleontological Bulletin 58: 1–518.

Marwick, J. 1927. The Veneridae of New Zealand. Transactions and Proceedings of the New Zealand Institute 57: 567-636.

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.

Brittle Stars, Brittle Taxa

Amphiura arcystata brittle stars extending their arms above the sediment, copyright James Watanabe.

The brittle stars are something of the poor cousin among echinoderm classes. Their tendency to relatively small size and cryptic habitats means that they do not attract the level of attention given to starfish, sea urchins or sea cucumbers. Despite this, they are perhaps the most diverse of the living echinoderm classes, with more recognised species around today than any other.

It should therefore come as no surprise that the internal classification of brittle stars remains decidedly up in the air. The basic framework of the surrent system was established over a hundred years ago by Matsumoto (1915) and changes to this arrangement since have been fairly cosmetic. However, a significant challenge to Matsumoto's system has been arisen following the input of molecular data to the mix: many of Matsumoto's higher groupings have not been supported by moleculat analyses. Perhaps the nail in the Matsumoto system's coffin has come from a recent publication by Thuy & Stöhr (2016) who found that a formal analysis of morphological data also failed to support the pre-existing classification. At this point in time, we know that a new classification of brittle stars is needed but we don't yet know what form it will take.

Excavated specimen of Amphiuridae, copyright Arthur Anker. The radial plates are visible as a pair of bars alongside the base of each arm; I don't think that the genital plates are visible externally.

Perhaps one of Matsumoto's groupings that will survive the transition is the Gnathophiurina. Notable features of this group include a ball-and-socket articulation between the radial shields (large plates that sit on the aboral side of the central body on either side of the insertion of each arm) and the genital plates (sitting below and alongside the radial shields), with the socket in the radial shield and the ball on the genital plate. The genital plates are also firmly fixed to the basal vertebra of each arm. I haven't been able to find what the functional significance of this arrangement is, such as whether it renders the body more flexible that in other groups where the radial-genital plate articulation is more fixed. At least one of the families of Gnathophiurina, the Amphiuridae, includes species that commonly live in burrows with the tips of their arms extended into the water column, using their tube feet to capture food particles (Stöhr et al. 2012). In contrast, some Ophiotrichidae are epizoic, living entwined around black corals and the like. The Gnathophiurina as a whole seem to be most diverse in relatively shallow waters.

Matsumoto's (1915) original concept of the Gnathophiurida included species that are now classified into four families, the Amphiuridae, Ophiotrichidae, Amphilepididae and Ophiactidae, and recent analyses have returned results not inconsistent with this association. In Thuy & Stöhr's (2016) morphological analysis, Gnathophiurina species all belong to, and make up the bulk of, their clade IIIc. In the molecular analysis presented by Hunter et al. (2016), the families belong to two separate clades but the branch separating them is very weakly supported. Further research is needed, of course, but it may turn out that Matsumoto was on to something when he focused on that ball-and-socket joint.

REFERENCES

Hunter, R. L., L. M. Brown, C. A. Hill, Z. A. Kroeger & S. E. Rose. 2016. Additional insights into phylogenetic relationships of the Class Ophiuroidea (Echinodermata) from rRNA gene sequences. Journal of Zoological Systematics and Evolutionary Research 54 (4): 269–275.

Matsumoto, H. 1915. A new classification of the Ophiuroidea: with descriptions of new genera and species. Proceedings of the Academy of Natural Sciences of Philadelphia 67 (1): 43–92.

Stöhr, S. T. D. O'Hara & B. Thuy. 2012. Global diversity of brittle stars (Echinodermata: Ophiuroidea). PLoS One 7 (3): e31940.

Thuy, B., & S. Stöhr. 2016. A new morphological phylogeny of the Ophiuroidea (Echinodermata) accords with molecular evidence and renders microfossils accessible for cladistics. PLoS One 11 (5): e0156140.