The diversity of eyes in nature is truly astonishing. Perhaps no other animal demonstrates the evolutionary peculiarities of eyes quite so well as the fanworm. They have been described by the scientists who study them as ‘eye-factories’, with almost every species favouring a slightly different type of eye. From no eyes to complex compound eyes the fanworm family has them all.
A ‘beautiful worm’ might seem like a contradiction in terms, but fanworms have an intricate beauty all of their own. Their name comes from the colourful fan-like fronds they have on their heads. These fans are not only beautiful, but crucial for the lifestyle and survival of this strange animal.
Fanworms spend the majority of their life inside a tube of hard material anchored to rock or coral. They’re found across the globe, typically in shallow waters. Their bodies (which are stereotypically worm-like) remain in their tube-homes at all times, with only their fan-like fronds extending out into the water. These colourful fans are made up of hundreds of tentacles which fan worms use both for breathing and for collecting food. The tentacles filter out pieces of organic matter from the water column, which are ferried down to the fanworm’s mouth back in the tube.
However, their idyllic life of filter-feeding in sun-filled shallow waters is rudely interrupted by attacks from predatory fish who also have food on their minds. Evidently tentacles provide a fish with a nourishing meal. The fanworm’s only line of defence is to rapidly withdraw their whole body, fans and all, deep into their tubes. Fortunately, most fish are only looking to nip off a tentacle or two, rather than eating the whole of the worm, so this defence works rather well. Or it does as long as the fanworm has sufficient warning that a fish is approaching, which is where vision comes in handy.
Given they’ve been nick-named ‘eye-factories’, it won’t come as a surprise to learn that fanworms do have eyes - just not as we might know them. They do not have camera-type eyes, instead their vision is provided by ocelli. Each single ocellus is made up of a single photoreceptor and three supporting cells which form a pigment cup and a lens. Unusually for an invertebrate, they have ciliary photoreceptors, much like our rods and cones. This discovery was a complete surprise as historically it was thought that all invertebrates had rhabdomeric photoreceptors and all vertebrates ciliary photoreceptors with no cross-over exceptions. Thanks to the fanworms and other subsequent discoveries, we now know that this is not the case, which leads to some interesting questions about how and when vision first evolved. Ciliary photoreceptors aside, these ocellar units are effectively vision at its most basic, but how they’re deployed by the fanworms across their bodies is where things start to get interesting.
Image: The increasing scale of complexity of eyes in fanworms, from no eyes to single ocelli to ocellar clusters to compound eyes. (Image: Michael Bok)
Most fanworm species have ocelli on the tentacles of their fan, which makes sense as this is the part of the animal that is actually out in the world while the rest of it remains in the dark safety of its tube. But how and where these ocelli are distributed varies greatly between species. Some species just have single ocelli dotted all across their fan. Others have groups of ocelli clustered together at regular points. Some have even evolved complex compound eyes that look remarkably similar to those of crabs. For instance the ocelli in Acromegalomma interruptum, a species found off the coast of Australia, have formed two consolidated compound eyes that are on the ends of long tentacles, which reach above and beyond the crown of the fan, giving the fanworm almost 360° vision.
The obvious question that comes to mind looking at the fanworm family’s sliding scale of eye complexity is whether they represent evolutionary progression. Are the species with the more complex eyes more highly evolved than those with the simple distributed ocelli? Sadly, it’s not that neat. There’s no evidence of a simple evolutionary progression as suggested by the increasing complexity in eyes. Instead, it seems as though the same eye types have evolved repeatedly and independently in the fanworm family, which is quite remarkable. The similarities in eye type between only distantly related species may be a physiological constraint of the sensory cells and neural pathways that are available.
Indeed, evolution seems to have taken some strange turns in the fanworms, especially when it comes to the eyes of the Christmas tree worm. This highly colorful species of fanworm hides its body in a burrow it makes in hard coral. They have complex compound eyes, but with an unusual banana-like shape, quite unlike any other eye we’ve ever seen. It means that most of the eye is actually looking at itself. As an additional peculiarity, these eyes are on short tentacles tucked underneath the animal’s fan, which must block most of its vision. It seems as though Christmas tree worms can only really see a small part of their world directly in front of the eye along the surface of their coral home. Quite why they’ve evolved such an inconvenient set of eyes is unclear.
Image right: Two Christmas tree worms in a coral head. The bright orange banana shapes are their eyes, tucked under their fans. (Image: Michael Bok)
From the simple to the complex, all these eyes have the same function; to detect the approach of predatory fish and enable the fanworm to retreat fully into the safety of its burrow. It would be natural to assume that the species which have more complex eyes would have better, or at least more comprehensive vision, than the species which only have single ocelli dotted around their fan. Broadly speaking there are four types of vision: changes in light level, detection of dark or light regions, motion detection and object detection for recognition. Only the latter two are considered to be vision in the true sense of the word. So, do fanworms have vision?
Experimentally, all of the fanworm species tested, regardless of eye complexity, have responded to the exact same set of visual stimuli. They react very strongly to the appearance of a dark object against a brighter background and that’s it. They don’t respond to the appearance of an object that’s brighter than the background, or to an object which has a different shape and pattern from the background but the same overall brightness. It appears as though they’re looking for one thing and one thing only; an approaching fish which would appear as a dark object against a bright background. Strictly speaking, fanworms do not possess vision. That having been said, there is some anecdotal evidence that some fanworms can detect motion. Not only that, but that they only respond to the motion profile of the specific fish species that are their major predators, but this has yet to be proven scientifically.
So why the diversity and complexity of eyes if they all give the same view? It’s hard to be sure, but it’s likely to be about balancing the “costs”. Despite their fast retraction reflex, it's not uncommon for fanworms to lose tentacles to hungry fish. If they build complex eyes, which give better vision (as in true vision) than single or grouped ocelli, they run the risk of losing them. Complex eyes are energetically costly to grow. While fanworms can regenerate their bodies and their eyes, this too is energetically costly and it’s unclear whether the neural pathways that connect the eyes to the brain also reform. Perhaps by keeping their eyes hidden beneath their fans Christmas tree worms are simply protecting their compound eyes, but the inevitable trade-off is having a really limited view of the world around them. By distributing their ocellar “resources” across multiple tentacles in their fan, fanworms minimise the cost of losing a tentacle. They also ensure a full field of view of the world, so they can see danger from any direction. But why not build multiple complex eyes to offset the cost of losing one? Aside from the obvious energy burden this would place on the animal, it would also require a great deal of neural processing, which may be beyond the capability of their simple brains.
The tentacles are not the only places that fanworms have eyes; they’re also found deep in the brain and on the segments that make up their body and their tail. This is a little surprising, given that the fanworm’s body is almost always buried deep in the dark of its tube, hidden from the world. It’s not quite clear what these eyes are for or if indeed they have any function at all. It’s possible that the cerebral eyes (the ones deep in the brain) are used to measure the overall environmental light level to detect if it is day or night in order to regulate the fanworm’s biological rhythms. The eyes on the body may be useful in indicating whether the fanworm has over extended its body from the tube or they, along with the eyes on the tail, may be useful for the rare occasions when the fanworm is not in its tube. Sometimes they’re forced to leave the sanctuary of their tubes either due to having outgrown it or if it’s been damaged beyond repair. Without a tube, a fanworm is incredibly vulnerable and must find shelter immediately. The eyes on the tail may be useful for detecting dark patches on the sea floor that would indicate the sanctuary of a nook or cranny in the rock; an ideal place to construct a new tube.
In conclusion, fanworms are a most fascinating and unexpected animal. They rightly deserve their reputation for being ‘eye-factories’, with a stunning range of eye types and evolutionary strategies which are proving a rich study ground for scientists.