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Annelids are the familiar worms, like earthworms and leeches. They are segmented burrowing animals (in fact, the segments are an adaptation for their burrowing lifestyle) that originated during the Cambrian Radiation (or perhaps in the Ediacaran) and nowadays have a worldwide distribution in all sorts of ecosystems, both on land and in the sea, from hydrothermal vents to your garden to the Antarctic. They are usually between 2 mm and 10 cm, with the largest being ~6 m big (Eunice).
They are quite diverse (see probably outdated, crudely-edited picture above; latest species count I found, 2010: ~16500 spp.) and their abundance, especially in marine habitats, has made them ideal indicators of environment and ecosystem health. Farmers know that earthworm burrows are signs of a healthy soil (well-oxygenated). Assessment of coastal health (when endangered by human activities, for example discharge of agricultural or sewage waters, fisheries, oil spills, tourism, etc.) is often monitored using polychaete worm diversity.
Earthworms, the common one being Lumbricus terrestris, have a book published about them by Charles Darwin. They dig tunnels up to 3 meters deep, eating up dead plant matter and depositing its feces at the surface (hence why farmers love it: the feces is nutritious, the tunnels aerate the soil and allow plant-symbiotic bacteria to grow) – in Central Europe, they’ve been estimated to go through 40 tons of soil per year. Their eggs are deposited in small coccoons out of which the offspring come out. Annelids are an important food source for predators, including humans – in East Asia, wormburgers are apparently popular (although this may just be an urban legend).
The next post will look at annelid systematics in more detail. To summarise it, the primarily marine Polychaeta (where they also fulfill essential roles in sediment aeration and stabilisation) are viewed as the basal, and most likely paraphyletic, annelid lineage, with the terrestrial and limnic Clitellata being decisively monophyletic and the sister group to the Polychaeta; a grouping of Oligochaeta is also named. This is also paraphyletic, and I use it as synonymous with Clitellata. The Polychaeta are much more diverse, due to the plasticity of their body plan: they can modify their head and trunk appendages to suit any kind of lifestyle, while the Oligochaeta lack these appendages and thus are more restricted.
The annelids also include the leeches, the Hirudinea, within the Clitellata. The medicinal leech, Hirudo medicinalis, was very popular in 19th century medicine, especially in France. They could suck up as much as five times their body mass in blood. Up to 100 of them were placed on the body – one can imagine the death rate resulting from this ‘treatment’ (which, by the way, is still recommended by quackorific naturopaths). They were supposed to treat obesity and whatever you call it when you have thick veins. It is nowadays still used in medicine, but in a much different way. It has chemicals with medicinal properties: hirudine helps with thromboses; caline slows down wound closure (useful in surgery); hyaluronidases are antibacterial; eglines have anti-inflammatory effects.
Their fossil record is surprisingly present – and not just in the form of trace fossils. The most ancient are, as usual, found in Konservat Lagerstätten (Burgess Shale, Sirius Passett), where annelid-like fossils have been found. These belong to the annelidan stem group: they have an overall segmented, annelidan appearance, some even with parapodia and setae, but have no sclerotised jaws. The crown-group of the annelids is known from jaws in Early Ordovician rocks. The picture above shows Kenostrychus clementsi from the Herefordshire locality, England (fossils from here are serially cut into thin sections and reconstructed digitally – the original fossil lives on only as a 3D reconstruction).
There have also been several memorable misinterpretations of these early fossils. Hallucigenia, now widely accepted as a stem-group panarthropod (possible onychophore), was originally said to be a polychaete. Wiwaxia also began its storied history the same way, going on to become a member of a mollusc-allied extinct phylum, then back to a crown-group polychaete, then reduced to a stem-group annelid, then simply a bilaterian, finally ending up as a stem-group mollusc. Similarly, some Ediacaran fossils have been placed within the annelids, but without any convincing arguments to back the interpretations up.
Anatomically, the feature that is most well-known in annelids is their segmentation. Their body is simply a series of repeated identical units (segments or metameres). Each of these units includes the coelom, parapodia (‘legs’), ganglia (nodes in the nervous system), muscles, blood vessels, nephridia (‘kidneys’) and septa (walls between the segments; also called dissepiments). In the animal kingdom, segmentation processes are varied. The segments are separated from each other by septa, which have valves allowing fluid flow between them. Annelids have a posterior growth zone where special cells are herded and aligned (by molecular signals from the mesoderm) and divide to produce the new segment – this happens continually throughout the annelid’s life.
Having said that, ‘segmentation’ is, surprisingly enough, not a well-defined feature, and this has led to quite a lot of controversy (a glimpse of which will be offered in a future post in the series, examining the position of the annelids within the metazoans). By the definition above, the only segmented animal groups are the annelids, arthropods and chordates. And it is really so that there has been a phylogenetic relationship proposed, whereby those three clades are allied together as the Polymera, and segmentaton is thus monophyletic. This is, of course, completely false – somitogenesis (segment-formation in chordates) is radically different from anything seen in arthropods and annelids. However, as we will see in the next post, the arthropods and annelids have classically been grouped together as the Articulata due to their shared segmentation. But as I said, we will look at this in more detail in the coming post.
Their coelom is highly-developed to form the annelid’s hydrostatic skeleton, which gives it considerable robustness and is also an adaptation for burrowing, as well as generally for surface locomotion.
The formermost (prostomium) and posteriormost (pygidium) body parts are not segments: they have no coelom.
The cuticle of annelids is made of collagen fibres secreted by the epidermis; note that the collagen here is very different from mammalian collagen: it has up to 18% carbohydrates, whereas mammalian collagen has less than 1%, so the structural properties are different. Annelids have characteristic (read: autapomorphic) ß-chitin chaetae (setae, bristles) on their bodies, formed by special cells called chaetoblasts and anchored in epidermal sacs of cells (like a plant in a pot). Each bristle is hollow. They’re used for locomotion and protection; the Hirudinea have lost them completely.
The nervous system is a typical ladder-like nervous system (as in the arthropods). The brain (cerebral ganglion) lies in the prostomium, with paired ventral ganglia in each segment. Numerically, the total numer of neurons in the brain of annelids is in the 10³ to 10⁴ region. In the medicinal leech, each segmental ganglion has ~400 neurons, and those in the two sex segments have 700. The ventral nerve cord is split into two paired cords, which wind around the cerebral ganglion and extend all the way down to the pygidium, connecting the ganglia. Lateral connections are called commissures; ganglial connections are called connectives. There is also a peripheral nervous system, connected to each of the ganglia by three or four nerves. Unlike the majority of invertebrates, annelid axons are myelinated (to make up for the lack of that, most invertebrates simply have axons with large diameters, which achieves a similar effect of increaing the signal’s speed, for example squid with their 1 mm thick axons).
Notably, annelids have mushroom bodies – or structures that look a lot like mushroom bodies. Keep this in mind when reading the phylogenetics post: only arthropods are also known to have mushroom bodies ;) Before someone accuses me of “leading the witness” or “begging the question”, I will state this in my defence: no other animal phyla with similar brain sophistication (cf. cephalopods, vertebrates) have converged on mushroom bodies – why should these two converge on it? Of course, it could also be that mushroom bodies are ancestral to all the Bilateria and then reduced in over 30 animal phyla. While genetic developmental studies hint at this, they are not as conclusive as may seem – simply sharing a developmental pathway is not proof of sharing a last common ancestor. I do not want to dwell on this point here (or in the next post) – the simple truth is that in this modern age of biology, comparative studies on organisms other than model taxa are severly lacking due to lack of funding; until we can get those studies done, we don’t have enough data to suppor either the Articulata or the Ecdysozoa based on brain architecture (cf. the phylogenetics post later!).
In terms of senses, annelids can have eyes anywhere on their body, not just the head. The photoreceptor is usually just an ocellus or a small eyespot; most of the time, it can only be seen in fresh specimens, as it simply disappears in preservative. Some groups do have ‘compound eyes’, as in several hundred bunched-together ocelli. Chemoreception is well-developed in annelids. Polychaetes use pheromones to coordinate mating and reproduction. For example, some species reproduce in swarms. Males swim in circles around the female, who releases a pheromone that attracts them and makes them swim closer. When close enough, the males release their sperm along with a fluid containing an egg release pheromone. This casues the female to discharge her eggs, as well as a sperm release pheromone, which makes the males ejaculate more. The closest human equivalent for this is some kind of orgy where the woman just can’t get enough and keeps on asking for more. Kind of. Whatever, let’s move on.
Chemoreception also plays an important role in larvae, as they choose their settlement location according to chemical cues (either environmental or from biogenic sources, such as microbial mats or conspecifics). Of course, chemoreception is also integral for feeding – and feeding-related behaviour: there is evidence that when blood of conspecifics is detected in the water, feeding will stop and the annelids will go into hiding (as an alarm response).
Chemoreceptive structures are, as with the eyes, present singularly all over the body and going through them is overkill for this post. I’ll just talk of the most important ones. In the larva, a bunch of cillia (tiny hairs) are found on the head and are presumed to be associated with chemoreception, as they are richly innervated. Larvae always have rows of hairs along the body used for chemo- and mechanoreception, especially associated with finding an appropriate substrate. The parapodia are also obviously important for detecting stimuli.
Worth noting are the nuchal organs, found on the posterior part of the prostomium of polychaetes but not the clitellates. Nuchal organs are paired and hairy sensory organs and are considered unique to the annelids – nemerteans and sipunculids have similar structures, but they are not thought to be homologous to the annelidan nuchal organs (despite having the same name).
The circulatory system is closed, its boundaries formed by the primary coelom. There are two main longitudinal branches. One lies above the digestive system and the blood is pushed forward to the prostomium when the body contracts; a ventral store lies beneath the digestive system, and is connected to many capillaries leading the blood to all the organs and extremities. Some of these capillaries – lateral hearts – can contract. The blood is either red (haemoglobin), green (chlorocruorin) or purple (haemerythrin); the molecule may be found freely in the bloodstream or packed in blood cells.
Behind the prostomium lies the mouth, the intestinal tracts go through the entire body, ending with the anus in the pygidium. The intestines may get differentiated, but this depends on the nurtition type.
Excretion takes place in metanephridia. They’re made up of nephrostomes (small, tightly-wound canals) that are open to the main body cavity, with a nephridial canal going through the dissepiment (the wall separating segments) to a pore open to the outside in the next segment. It is in these nephridial canals, which are all tightly-wound, that ultrafiltration takes place and NH3 (and other metabolites) are released (osmoregulation and all that happens in a human kidney also takes place here). The picture above shows what the nephridium looks like (perhaps atypical, not sure; I just find the diagram very nice). Labels, lifted almost verbatim from source: A is the beginning of the nephridial duct, B is the duct with microvilli, C are duct cells showing dense apical cell plasma, D is the folded duct lumen, E is the lumen with urn-shaped protrusions [cf. two paragraphs later, reproductive purpose], F is the basal labyrinth and bladder. Numbers refer to the same rough regions, but are differentiable by visual inspection; letters by ultrastructure (histology, electron microscopy, etc.).
Annelid larvae have protonephridia, the main difference being that they don’t open into the coelom as the metanephridia do. They are then replaced by the metanephridia in the adult – although some exceptions exist, e.g. the phyllodocids, where the adults retain the larval protonephridia. Obviously, the protonephridia are larger and expanded in these adults.
Importantly, nephridia have a role in the reproductive biology of some annelids. In these taxa, e.g. the spionids, not only do the nephridial canals serve as gonoducts (where the gametes travel), as far back as 1908, it was noticed that when spionids (Annelida: Polychaeta) became sexually mature, their nephridia became enlarged and modified. The most drastic of these modifications is the development of microvilli all over the cell bodies, and them becoming urn-shaped. These microvilli produce spermatophores. As the sperm is swimming in the nephrostome, the mature ones are sorted and go into the nephridial canal, where they are then driven to go into the nephridia, where the microvilli pack them together into a compact spermatophore (hence the urn shape). The spermatophore can then be excreted: this is a perfect example of cooption of a pre-existing structure to a new function. In these annelids, the nephridia are referred to as nephromixia.
The gonads are found on every segment. Gametes are released into the body cavity and are released to the outside either through special gonoducts or through the nephridial canals; in some polychaetes, the body wall itself gets ruptured for release. Clitellates are characterised by the restriction of their gonads to only four segments – the name-giving clitellum. Polychaetes are mostly sexual, clitellates are protandric hermaphrodites.
Annelids have a pear- to ball-shaped trochophore larva with a through-gut. The mouth is ventral and the anus is terminal. Trochophore refers to the pro- and metatroch, rings of small hairs encircling the body both beneath and above the mouth (respctively). There may also be a telotroch near the anus. The body cavity has a pair of protonephridia. The picture above shows how the larva of the model organism Capitella teleta develops. During metamorphosis, the top part of the body becomes the prostomium and the bottom part the pygidium (hence why they are not segments). The picture below shows the full life cycle of a polychaete, Platynereis. That said, clitellates develop directly to an adult: there is no larva and a baby worm comes out of the egg.
There are many reproductive types in the polychaetes. Some reproduce once then die (e.g. some nereids). Some produce stolons which break off, swim to the surface, release the gametes and die – the parent continuing to produce stolons until it dies a natural death (e.g. in syllids). Hermaphroditism, while autapomorphic for clitellates, is also common in polychaetes, e.g. in serpulids. Eurythoe complanata can either reproduce sexually or it can break off a piece of its body which then regenerates into a new clonal individual.
One ancestral trait for the annelids is regeneration ability: they can regenerate their tail and head. Tail regeneration is almost ubiquitous, but head regeneration has been lost several times. Regeneration is simple: first the wound heals, then a blastema (a mixture of stem cells and secondarily undifferentiated adult cells) forms and regenerates the lost parts. In those lineages that have lost regeneration, the wound will heal but no blastema forms. Regeneration is obviously a useful trait – many annelids suffer sublethal predation where some part of them gets cut off (feeding tentacles in water, head or tail on land). Loss of regeneration may simply be due to energetic constraints: sometimes, it’s simply not worth investing in regeneration, so they just lick their wounds and concentrate on reproducing.
I already mentioned here and in my deep sea post series that annelids are found in the deep sea and at hydrothermal vents. In the latter, they are often highly-specialised forms, with Riftia being the most studied. The digestive system is reduced, if not absent; for food, they host endosymbiotic γ-proteobacteria in modified gills called trophosomes. These endosymbionts can oxidise hydrogen sulphide and fix carbon, which the annelid can then take. To make sure the endosymbionts get as much raw nutrients as possible, Riftia has three types of haemoglobin adapted to binding to hydrogen sulphide.
For some totally random information, here’s a couple of tidbits on annelid mitochondrial DNA. All the coding genes are found on one strand of the mtDNA, not both as is usually the case in other animals. Also unlike other animals, there is only one start codon, ATG.
Another random, but really cool tidbit: the pictures above are electron microscope pictures of Diopatra marocensis, an onuphid. Specifically, they are of the first parapodium. In A, those white globules are actually microorganisms (Epistylis colonies) living symbiotically on the parapodium. B is a close-up of the Epistylis, showing hyphae on the Epistylis: they have fungi living symbiotically on them, while they are symbiotically living on the annelid. Cool.
Arias, A., Anadón, N. & Paxton, H. 2010. New records of Diopatra marocensis (Annelida: Onuphidae) from northern Spain. Zootaxa 2691, 67-68.
Kremer, P., Fiege, D. & Wehe, T. 2011. Morphology and Ultrastructure of the Nephridial System of Hypania invalida (Grube, 1860) (Annelida, Polychaeta, Ampharetidae). Journal of Morphology 272, 1-11.
Paxton, H. & Åkesson, B. 2010. The Ophryotrocha labronica group (Annelida: Dorvilleidae) – with description of seven new species. Zootaxa 2713, 1-24.
Pimm, S. L., Russel, G. J., Gittleman J. L. & Brooks, T. M. 1995. The Future of Biodiversity. Science 269, 347-350.
Saudemont, A., Dray, N., Hudry, B., Le Gouar, M., Vervoort, M. & Balavoine, G. 2008. Complementary striped expression patterns of NK homeobox genes during segment formation in the annelid Platynereis. Developmental Biology 317, 430-443.
Shimeld, S. M., Boyle, M. J., Brunet, T., Luke, G. & Seaver, E. C. 2010. Clustered Fox genes in lophotrochozoans and the evolution of bilaterian Fox gene cluster. Developmental Biology 340, 234-248.
Sutton, M. D., Briggs, D. E. G., Siveter, D. J. & Siveter, D. J. 2001. A three-dimensionally preserved fossil polychaete worm from the Silurian of Herefordshire, England. Proceedings of the Royal Society B 268, 2355-2363.