Tie A Yellow Ribbon (Worm) Around The Old Reef Rock...

Over the past couple of years, I have devoted several columns to the various kinds of segmented worms found in reef aquaria. The bodies of these worms are composed of repeated body units which are generally manifested on the outside of the worm as a series of rings or annuli. The name that scientists give this great group of worms is the Phylum Annelida, recognizing that the "annuli" or segments are the worm's major visible characteristic. Most annelids found in reef tanks are polychaetes, known to most aquarists as "bristle worms." These worms have a couple of other notable visible characteristics such as the presence of appendages off each side of the segments and tentacles from the head or other regions of the body. These annelids are often large and evident, and numerous species of them thrive in aquaria. After looking into their tanks when the "clean up crew" of bristle worms is active and visible, reef aquarists might be forgiven for thinking all worms likely to be found in their systems are annelids. However, upon reflection most aquarists would also count flatworms among the wormy denizens of their systems. These two types of worms are commonly the basis for much discussion amongst aquarists, as they are generally foreign to the average hobbyist. Nonetheless, they are common inhabitants of marine aquaria, as eventually most hobbyists come to realize.

Recently, however, a third variety of worm has occasionally been found in reef aquaria. These worms are moderately large, up to several inches in length. Unlike the annelids, they don't have segments, and they have no visible appendages such as tentacles or the small paddle-like parapodia off the sides. While these worms appear in some cases to look a lot like flatworms, they aren't flat. They are decidedly "meaty" and have some real depth to their length and width. And, unlike most free-living flatworms, they may be quite large; in nature some of them reach lengths well over 100 feet long. These are the ribbon worms. Unlike a lot of the other worms as well, many of them are strikingly beautifully colored, and well worth keeping if we get the chance.

Ribbon worms are placed by taxonomists in a group that goes by several names. The group is most commonly referred to as the Phylum Nemertea, but it may also be called the Phylum Nermertinea, the Phylum Nemertini or, alternatively, the Phylum Rhynchocoela. All of these names refer to exactly the same group of animals, and simply represent the names given to that group by different researchers at different times or in different countries. It is probably worth using this example to illustrate the arbitrary nature of taxonomy and the study of animals. Within any large scientific discipline, there are differences of opinion, and methodology. For example, the scientific discipline that most American reef aquarists would recognize as "marine ecology" really doesn't exist within the same framework in Russia. While the science of marine ecology is present in Russia, the way in which it is studied and concepts emphasized as important differ significantly from what is studied, or even conceived of, in the United States. Likewise, taxonomy differs from place to place. In the middle part of the twentieth century, the American invertebrate zoologists and taxonomists who studied ribbon worms considered the worms' characteristic extensible prey-capturing proboscis, called a rhyncocoele, as the most important defining structural feature of the group. In use, the ribbon worm's proboscis projects in front of the worm rather like an elephant's trunk or proboscis. To emphasize that this notable feature had a contained space or cavity within it, some American invertebrate zoologists coined the term, "Rhynchocoela;" rhynchocoela literally means "cavity in the nose, or beak." These biologists then began to refer to the ribbon worms by that name. However, most other invertebrate zoologists kept referring to the group by its earlier name of Nemertea; a name derived from the name of the ancient Greek Sea Nymph or Nereid, known as Nemertes, "the unerring one." This was also an appropriate name for these worms in that the proboscis is unerring and always spears or grabs the prey. The name "Rhynchocoela" was used extensively in the United States and Canada until the 1970s when it began to fall out of fashion, nonetheless, it is still occasionally used. Presently, the older name of Nemertea is far more commonly used. In any event, should the reader become interested in this group, information about them will be found under all of the names listed above.

Ribbon worms don't have any manifestation of segmentation. Unlike the annelids, the body is smooth. They also lack appendages or any other permanent projections from the body. The body is often brightly colored, and there are often small dark eyespots found near the front end. On careful examination, a pair of grooves is sometimes found just behind the head, and the animal will be seen to have either one or two openings at the front end, and one opening at the rear end. They are typically long and thin, about the length and width of some ribbons, hence giving the group their common name. However, they are not flat like either ribbons or flat worms. The bodies are typically circular or elliptical in cross section. They really have only one claim to zoological fame. Some species of nemerteans may well be the longest of all animals. Nemerteans longer than 30 feet long are surprisingly common, and some have been measured at well over 100 feet in length. There is a nemertean story, probably apocryphal, about the eminent late nineteenth and early twentieth century British zoologist, E.Ray Lankester. Lankester was pretty much the dean of British scientists at the end of the Victorian period, and as one of his many perks, enjoyed golfing privileges at St. Andrews golf course in Scotland. During one round of golf, the eminent doctor whacked a ball into the rough, which as the golf course runs along the sea shore, was the intertidal zone. He is reputed to have gone in search of the ball, only to be distracted by finding a nemertean coming out of one hole and going into a second hole over 100 feet away. Neither end of the worm was seen, so the total length remains unknown, except that it was in excess of 100 feet long. Lankester also collected a sipunculan, or peanut, worm on one his forays into this golfing intertidal zone. It was new to science, and he immortalized his passion by naming the worm genus, Golfingia, but that is another story. Other nemertean worms have subsequently been collected with lengths similar to what Lankester found, validating his observations. Alas, the largest nemerteans that I have personally collected were only about 60 feet long.

Figure 1. The head of a large nemertean worm I photographed in
about six feet of water near Seward, Alaska. The body of the worm
was well over 40 feet (12 m) long.

The 550, or so, species of ribbon worms, are mostly marine, and most are found in the polar seas where they are often both diverse and abundant. However, they are by no means rare or uncommon in temperate or tropical habitats. While most marine forms are bottom dwellers, there are few species that are wholly pelagic, swimming in mid-water. There are a few species found living on the bottom in freshwater habitats. One species, called either Prostoma rubrum or Prostoma graecense, is widely reported from streams throughout North and Central America. There are also numerous terrestrial species, found mostly in the tropics, but at least one species of Geonemertes has been accidentally introduced to the west coast of North America and is now found from Vancouver, British Columbia, to San Francisco. It lives in and under leaf litter and is thought to prey upon small slugs.

Nemerteans have a misleading simplicity of structure. Superficially, they look rather like "unflat" flatworms. It is easy to look at small ones, particularly, and see a relationship to flatworms. After all, both flatworms and nemerteans are flattened (more-or-less) unsegmented worms, with no clear definition of a head or other body regions. They both move with the gliding type of movement characteristic of ciliary locomotion when small and by a combination of gliding and muscular movement when larger. Neither of these types of worms has a hard shell or cuticle, and both have similar simple eyespots. Internally, neither of these worm types has a body cavity surrounding the gut. All of these things have indicated to several generations of zoologists that nemerteans and flatworms are closely related.

Figure 2. A small individual of Tubulanus polymorphus, about six inches (15 cm) in length.
This species may eat small crustaceans, and reaches lengths of about three feet.

Such a close relationship made for a pretty story and allowed a lot interesting theory and discussion about how nemerteans were somehow "advanced" animals at the flatworm structural grade. Unfortunately, such stories and discussions were well within the realm of science fiction. Close examination of internal structures, as well as studies of the genetic material of both groups, indicates no relationship at all. Nemerteans are descended from a totally different group of animals than those that gave rise to flatworms. Although ribbon worms may look like flatworms, the most recent ancestor they likely shared was alive over a billion years ago.

Ribbon worms are typically elongate worms with a circular or elliptical cross section. They have a ciliated epidermis which is the major means of locomotion for most of them. Cilia on the bottom surface move the animals in a gliding locomotion, in many ways similar to the gliding locomotion seen in many snails. These snails, such as individuals of the common aquarium snail, Nassarius vibex, also move by ciliary means. These worms are, however, also highly muscular, and the larger forms also use muscular means to move themselves along. They may pass muscular waves of contraction down their bodies using these to provide propulsive power. Some forms are very active swimmers as well. Most, however, use a combination of ciliary gliding and peristaltic muscular means for locomotion.

The internal anatomy of these animals is complex, but not as complicated as the average annelid worm. The gut is a complete gut with sequential digestion occurring from front to back in the gut. Unlike the gut found in flatworms, which has only one opening, the gut in ribbon worms has an anterior mouth and a posterior anus. The mouth may be found either at the front of the body, or on the bottom of the body a short distance behind the front end. The anus is generally terminal at the back end, although a few forms have a small "pigtail-like" cirrus projecting behind it. The gut has quite a few internal divisions, but they don't correspond closely to what is seen in many other animals. Behind the mouth is a short esophagus, often with a large pouch or caecum extending from it. Located just after the esophagus is the relatively small stomach, and then a long intestine extends almost all the way to the end of the worm. The intestine has many side pouches, referred to, collectively, as intestinal caecae. It appears that much of the digestion occurs within the cells lining the various pouches rather than in the gut cavity. A short hindgut terminates in the anus. The gut is embedded in the body musculature, and no body cavity is found surrounding the gut as it is in annelid worms, fish, or crustaceans.

The ribbon worms possess a closed circulatory system similar in concept to that found in annelids, fishes or, for that matter, humans. The blood always is found with vessels, unlike the situation in mollusks or crustaceans, where the blood flows freely over and through the tissues. There is a blood vessel loop around the brain region and lateral blood vessels which extend down the length of the body on either side, meeting at the posterior end of the body. Often, but not always, a dorsal vessel is found running from the anterior blood vessel ring to the juncture of the two lateral vessels. There is no heart, nor are there valves within the system. Blood simply sloshes around within the vessels and is moved by muscle contractions throughout the body. The blood may or may not contain hemoglobin, but if it does, the hemoglobin is not found in cells.

As befitting long and narrow animals with a permeable body surface, there are no specialized organs for respiration. Dissolved gases simply diffuse in and out over the body surface. Instead of using a high a high pressure filter system as a kidney, such as found in octopuses, these worms rely on a fine system of tubules with fluid motion dependent upon a few small clusters of beating cilia. Such systems are simple kidneys that are more adapted to control water balance than to excrete nitrogenous wastes. Nonetheless, they do secrete ammonium ion as a waste product. These kidneys empty through pores near the front end of the animal.

Although they seem like simple worms with not much going for them, they have a surprisingly complicated nervous system. They have a large bilobed brain with a major nerve running around the front of the gut, in the region of the throat. Instead of a single spinal cord, they have paired major nerves running the length of the body on either side. Additionally, large nerves run from the brain to the proboscis. They typically have eyespots, sometimes as many as several dozen. These eyespots cannot form images, but in the most sophisticated receptors can detect changes in light intensity and the angle of light impingement. Additionally, they have several well-enervated organs in the head region that are thought to be mostly chemosensory.

Their reproductive systems are simple to the point of being rudimentary. The sexes are separate, and the gonads are found as masses of egg or sperm producing tissue between the intestinal pouches. When the animals are gravid, and "the time is right," temporary openings form to the outside and spawning occurs. In a few nemerteans, such as Cerebratulus species, a specialized hat-shaped larvae, called a "pilidium" occurs. This larva develops and then undergoes a metamorphosis into a juvenile worm. In most nemerteans, the embryo develops directly into a small worm, and has no larval form. They also develop asexually by fragmentation.

Figure 4. A pilidium larva collected from the plankton. The juvenile worm starts
development at different discrete points within the larvae. These all grow together
as the larva ages to eventually form a worm which will emerge from the larvae at
metamorphosis. This larva was about 0.004 inches (100 µm) long.

The single structure that sets these worms apart from all other worms is their proboscis, the rhyncocoele. Basically, the term "proboscis" simply means a large, evident and sometimes mobile nose, such as an elephant's trunk. However, that really isn't the case with these worms. Here the proboscis is a rapid-strike prey capture organ. The nemertean proboscis is normally retracted into an internal sheath or pouch found above the worm's gut. The proboscis proper is a thin walled closed tube, shaped like a rather long, flexible, soda straw with a closed end. The open end is continuous with the body surface at a pore on the front of the animal. The closed end is held inside the sheath, pulled into the sheath by the contraction of a long muscle called the proboscis retractor muscle. The inside of the straw is continuous with the outside of the animal, and is collapsed on itself when the proboscis is retracted. The proboscis sheath is a closed impermeable tube and is filled with fluid. When the animal senses a prey organism nearby, a circular muscle layer around the proboscis sheath rapidly and vigorously contracts. This contraction forces the fluid from the proboscis sheath into the proboscis and, in the process, literally turns it inside out, blowing it out of the proboscis sheath. The proboscis will rapidly (within a second or so) wrap itself around the prey, which is then drawn to the mouth and eaten.

There are two basic types of nemerteans, and the difference between them is based on the structure of the proboscis. In the ones considered to be primitive, in what taxonomists call the class Anopla, the mouth is located ventrally, and the proboscis exits at the front of the worm. These animals have a poisonous or sticky proboscis secretion that acts to immobilize the prey, which is subsequently eaten. Some common genera of Anoplans are Cerebratulus, and Lineus. Ray Lankester's long nemertean found by the golf course was probably a species of Lineus. Some worms in the Anoplan genus Cerebratulus are notable for their swimming ability. They are flattened top to bottom and very muscular. They swim by undulating their bodies much in the manner of a sea snake or leech. I have had several of these worms, about two or three feet long swim by me, always on night dives in murky dirty water. It is enough to make one swear off alcoholic beverages…almost.

Figure 5. A diagram of the basic structure of the front end of an Anoplan (stingless) nemertean showing
the retracted proboscis.

The other basic type of nemertean is placed in the taxonomic class Enopla. Here the gut and the mouth open through a common pore at the front of the animal. Additionally, they possess a piercing calcareous stylet which punctures the prey, introducing venom into it. The stylets bear a resemblance to a sharpened golf tee. They are glued to a pad or thickened area inside the proboscis. They typically are released or break off upon striking the prey. When the proboscis is withdrawn, it is reloaded with another stylet. The animal secretes extra stylets and may have as many as a half dozen in reserve at any one time. Some common genera of Enoplans are Paranemertes, Amphiporus, Emplectonema, and Micrura.

Figure 6. A diagram of the basic structure of the front end of an Enoplan (stinging) nemertean
illustrating the retracted proboscis. Note that there is only one open to the outside, and that the
proboscis, when everted, will exit through the mouth.

Figure 7. A diagram of the basic structure of the front end of an Enoplan (stinging) nemertean illustrating
the everted proboscis. Note that the proboscis can be much larger than shown here, it may in fact be as
long as the animal's body.

Figure 8. An unidentified enoplan nemertean, about 0.04 inch (1mm) long.
This animal has four eyespots. The proboscis is clearly visible above the gut.
The intestinal pouches, or caecae, are the site of much of the animal's digestion.

Figure 9. This is the same nemertean as shown in the previous figure.
The piercing stylet is visible in the introverted proboscis, as is the gut
underlying the proboscis.

Most nemerteans are predatory, but a few are parasites. The diets of relatively few of them have been documented in detail. The prey appear to be primarily polychaete annelids, crustaceans such as barnacles and amphipods, or fish. Cerebratulus lacteus from Nova Scotia is odd in that it eats Mya arenaria, a rather large clam. Several species of some specialized nemerteans, such as species of Malacobdella, are commonly found inside the mantle cavities of large clams. Although it is widely thought that the clam-dwelling nemerteans are parasites, in fact, they eat small crustaceans and worms found in the mantle cavities. They are probably best considered to be beneficial symbionts that clean the mantle cavities of pests.

Some of the truly parasitic forms live on crabs and are egg parasites. On the west coast of North America, Carcinonemertes species are found infesting several species of crabs. These are tiny nemerteans that live on the outside of the crab's carapace. They eat the eggs of the crabs; each worm can eat an egg or so a day. An infestation of several dozen worms can effectively eat the entire yearly spawn of the crab. These particular nemerteans can be of immense economic importance, and have been credited with single handedly destroying the economic viability of several Dungeness crab fisheries along the coast.

Several different nemerteans have been reported over the last couple of years in my forum on Reef Central. They are all moderately sized animals, a few inches long, and they probably hitchhiked into aquaria on live rock. Nemerteans are mostly predatory, and although a few, notably some large Antarctic forms, have been seen to be scavengers. It is a pretty safe bet that any turning up in aquaria will be predatory. Some of them seem to be fairly specialized in their diets, Paranemertes peregrina in the Northeastern Pacific has been well studied and appears to eat mostly one species of polychaete annelid, Platynereis bicanaliculata. Others may be less picky in their foods.

I don't think I would consider any of these animals, a priori, as a decided risk factor for any aquarium inhabitants. Neither, however, would I consider them as benign. I like nemerteans and consider them very neat creatures, but I would not risk them in my reef aquarium. I would put them in a small dedicated tank. In such a tank, they will do very well if fed properly. I maintained a large (45 feet long) worm in a chilled demonstration aquarium in one of my teaching labs for over six months and it did very well, indeed. At the end of the class year, I released it back into nature where it presumably may still reside.

Nemerteans need good water quality! They produce a lot of mucus and good filtration is a must. The benthic species also need an appropriate substrate. Those animals that enter aquaria as hitchhikers on rocks will benefit from some rockwork in their home. They will generally hide in the rocks when not hunting. Standard reef temperatures and salinity are also necessary. Should you find yourself caring for a nemertean, you are probably on pioneering ground. While a few species have been studied, the biological interactions and natural history of most of them are unknown. The small species may not live lives of very long duration, but the larger ones might well live several years to decades. Many of these are exceptionally colorful and attractive animals so if you find one in your aquarium, don't be in a hurry to dispose of it. It might be well worth the time and expenditure of setting up a small species tank.