Recently I have seen a number of questions on the reef bulletin boards about Christmas Tree Worms, members of the genus Spirobranchus, and decided to write something about their biology for this month.  The spectacularly multicolored plumes of these worms, especially when jutting up from a live colony of Porites coral, always makes an eye-catching display.  Despite the fact that they are a beautiful and frequently available in the hobby, they generally do not survive well in reef tanks, and in this article I will try to convince you that they should be avoided by all but experienced hobbyists.

As usual, I’d like to start with a little background biology before I get into the details of why these worms do poorly in captivity, and how to care for them should you decide to try anyway.  Like other tube-dwelling and ‘feather duster’ worms, Christmas Tree Worms are polychaetes.  I use the term feather duster loosely, because this is a common name that means different things to different people.  For example, some pet shops use the term to refer to any worms that have a tube and a feeding crown, while others use it to specifically refer to only one or a couple of families of polychaetes (usually either the sabellid and/or serpulid polychaetes).

I guess I should back up a step here, and introduce everyone to these groups so we’re all on the same page before I get any further in the discussion.  Polychaetes are one of three traditional Classes of worms in the Phylum Annelida (the ring worms).  The other two traditional Classes of Annelids, the Class Oligochaeta (the earthworms) and the Class Hirudinida (the leeches) are the subject of some debate, but many worm biologists now consider both these groups to be sub-classes of the Class Clitellata (Rouse and Pleijel 2001).  As with most groups of marine organisms, the taxonomy of annelid worms is a subject of on-going research, and the exact relationships among the groups is yet to be resolved satisfactorily.  Regardless of the exact relationships among the classes, the polychaetes appear to be a good group, and that is the group that we are talking about right now.

Polychaetes are often referred to collectively as “bristleworms.” I personally dislike that term, because there are so many negative connotations associated with it among reef aquarists.  I also dislike it because it is used in so many ways by different people that it is virtually impossible to have a useful conversation using the term.  For example, some people use “bristleworm” synonymously with polychaete to refer to the entire Class as a whole, other people use “bristleworm” only to denote those families with particularly long bristles (such as the Families Nereidae and Amphinomidae), and yet others use it to refer only to the group specifically known as “fireworms” (the Amphinomidae) in the hobby.  Obviously, with such drastically different meanings, unless you know exactly in which way the term “bristleworm” is meant, it could refer to the nearly 10,000 currently described species of polychaetes, it could refer to a couple of specific Families of this class (just over a thousand species), or it could refer to a handful of potential pest species of worms that give the entire group a bad reputation, respectively.  Like the term ‘bristleworm’ and ‘feather duster’ can have widely varying meanings, it is hard to have a specific conversation using such general and poorly defined terms that are often used in different ways by different people.

The calcareous tube of Spirobranchus worms, with its obvious spike, is sealed by an operculum when the worm withdraws (top & bottom). The tube of these worms lies almost entirely beneath the living tissue of its coral associate, such that the brightly-colored radioles appear to emerge from the surface of the coral itself when the worm is feeding (left). Photo – James Wiseman

So having tried to make that clear, I’m now going to talk a little about tube- dwelling worms in general, because despite the variety of families (including sabellids, serpulids, spirorbids, sabellariids and chaetopterids, just to name some of the better-known ones) which have tube-dwelling members, many of these worms have surprisingly similar feeding preferences and aquarium requirements.  In general, most small tube worms feed actively by capturing tiny suspended plankton from the water column.  Depending on the size and species of the worm in question, the particles upon which they feed could be as small as bacterial floc or as large as zooplankton.  In general, the larger the worm, the larger the particles on which they feed.  So, in the case of tiny worms, such as the spirorbid polychaetes, they are feeding primarily on particles in the range of bacterial floc and tiny suspended particles of organic detritus to the smaller end of cell sizes of phytoplankton.  In the case of large worms, such as the giant feather duster worms of the genus Sabellastarte, they feed primarily at the other end of the particle size range, and collect primarily the largest sized cells of phytoplankton and small zooplankton (such as ciliates, rotifers and invertebrate larvae), along with occasional bits of suspended organic detritus.

Unlike the suspension-feeding corals I discussed in the March issue (Toonen 2002), these worms generate their own flow to capture food particles in addition to relying on the flow of currents to bring food particles to them.  These worms extend their feeding pinnules (the colorful “crown” of the feather duster) and actively pump water through the ciliated tentacles to capture organic particles as they pass through the feeding pinnules (cilia are tiny hair-like extensions on the surface of cells that are under active control and used to generate currents to move water or mucus around).  The worms then sort the captured particles in a number of ways before swallowing the ones that are of the correct size and taste.  I can’t go into detail on how tube-dwelling feather dusters feed in the space of this article, but Ron Shimek (1998) has an article that covers ciliary suspension feeding for those interested in more detail.

One thing I do want to make clear, however, is that worms feed from the bottom up.  I always find it somewhat amusing when I see a well-meaning hobbyist try to target feed their worm by squirting some sort of particulate food into the center of the crown. Target feeding is difficult enough because the worms typically withdraw into their tubes as soon as they sense the current generated by spraying food towards them.  However, most people are rather shocked to discover that the current is generated from the outside of the tentacles as water is drawn upwards into the crown from underneath and expelled towards the center of the ring on the upper side.  Thus, by directing target feeding streams towards the center of the crown, even those worms that don’t retract immediately get little to no food from that well-intentioned effort because the food will be blown away from the animal by the feeding current it generates (the center of the crown is where their waste water gets pumped away — by target feeding the center of the crown, you’re effectively trying to feed their butts).  Therefore, if you are trying to feed a feather duster worm, you should be directing the food to the side and below the crown, where it will be drawn through the feeding tentacles and feed the worm.  By creating water flow through the feeding tentacles, the worms actually use the eddies generated by having a branch of their crown in the flow (similar to a rock in a stream causes a swirling eddy which pulls objects in behind the rock) to cause food particles to swirl around that branch and get captured on the upper surface of the tentacle.

Depending on the species of worm and how big it is, the ‘mesh size’ through the feeding pinnules can be very tiny or quite large, and the efficiency of capturing particles of various sizes depends on how big that “mesh” of feeding tentacles is.  Tube worms are very efficient at capturing particles of the correct size, and an undisturbed worm feeding at it’s maximum rate can actually clear 100% of the particles of correct size (whether that is phytoplankton or zooplankton depends on the size of the worm) suspended in the water pumped through the pinnules.  Again this is important, because that filtering efficiency is much higher than that of corals, clams and other animals that can also feed on suspended plankton, so, in general, tube worms should be the last to show signs of starvation — if you have other filter- feeders, the chances are that they are suffering at least as much as your worm…

As I said above, most small tube worms feed on phytoplankton, but the very large species, such as Sabellestarte spp., tend to switch to consuming largely zooplankton as they grow – small animals feed primarily on small phytoplankton, but as the animal grows, so does the size of the mesh, and therefore the size of the phytoplankton preferred, and by the time the animal is an adult, these worms feed primarily on tiny zooplankton (rotifers, invertebrate larvae, copepods, etc.) but probably still capture large phytoplankton as well.  The worms usually get enough suspended detritus and bacterial aggregates to grow when they are small, but as the animals mature and require larger plankton, the supply in most aquaria is quite limited, and specific feeding becomes ever more important. This is why many people observe that a worm initially does well in their tank, but as it grows it seems to languish and eventually suffer in the aquarium after long periods of apparently thriving.  Feeding a variety of phytoplankton to small worms will obviously benefit them, but as they grow, the larger organic particles they will want in their diet.  The Christmas Tree Worms, Spirobranchus are an intermediate sized worm, and in the lab they appear to feed primarily on detrital floc, phytoplankton and ciliates.  However, feeding preferences and strategies likely vary among species, and there are very few studies examining the natural diet of these worms.  In the absence of such studies, we have only distributional studies suggesting that certain particle sizes or abundances are appropriate for certain species of Christmas Tree Worms.  For example, some species, such as S. tetracerosain  thrive only in highly turbid water with high organic particle counts of intermediate size; whereas others, such as S. giganteus, are never found in such habitats and only thrive in areas characterized by clear water with relatively few tiny organic particles (Frank and Ten 1992).

Which brings me to my next point: what is the exact nature of the association between Porites coral and these worms?  I’m not sure where the idea that Spirobranchus feeds on the mucus from Porites first originated, but I often see this claim repeated.  Sometimes this idea is quite general, simply suggesting that the worms likely benefit from the presence of the coral mucus because the worms are an obligate associate of live corals.  However, I have also seen highly specific claims, and I have heard that the mechanism by which worms benefit from the association ranges from the coral mucus trapping phytoplankton which the worms then eat, or even that there are nutrients in the coral mucus without which the worms simply cannot survive.  However, as far as I can tell this is all aquarium urban legend, because there is absolutely no scientific research to support any such claims.  It is true that the worms are obligate associates of live corals (i.e., they are rarely ever found in corals that are not live), but they are found in a variety of species, and Porites is actually one of the species in which they do the worst in the wild (I’ll explain this more below).

It’s actually sort of a complicated system, and no one has really figured out exactly what is going on yet with either the species identity or the biology of Christmas Tree Worms, but I will try to synthesize the information that is available so far.  In terms of the animals, the worms that we’ve always called Spirobranchus giganteus turn out not to be a valid species.  Instead, there is an entire species complex of cryptic species (researchers use this phrase to describe morphologically similar species that have previously been considered a single entity), and several of the well-known ‘morphs’ of this misunderstood species have turned out to be completely infertile (i.e., they are incapable of fertilizing one another’s eggs) when crossed in the laboratory (e.g., Marsden 1992).

Researchers have recently discovered that the worms are found on specific corals as a result of their larvae showing a strong settlement preference for corals such as Porites or Millepora while completely ignoring corals such as Siderastrea, Dendrogyra and Agaricia (e.g., Hunte et al. 1990a; Marsden 1991; Marsden et al. 1990; Marsden and Meeuwig 1990).  Perhaps I need to back up a step here.  In case you don’t already know this, these worms (together with about 80% of all marine animals) produce tiny larvae that develop on their own until they metamorphose into the adult body form (like a caterpillar metamorphoses into the adult body form of a butterfly as a more familiar example).  Obviously, the choice of a suitable habitat is of critical importance to the survival of an animal that is permanently affixed to their choice once they metamorphose (such as a Christmas Tree Worm), and the chemical and physical cues associated with mature larvae selecting an appropriate habitat and metamorphosing into the adult body form are the focus of a great deal of research (see McEdward 1995 for a detailed review).  Unfortunately, larval settlement preferences are a difficult problem to study, and the exact mechanisms and cues to which larvae respond remain a mystery for all but a couple of species.  However, despite the difficulty in identifying the exact cues responsible, researchers have become quite good at locating the source of settlement cues in the wild.  Once the source of the cue has been isolated, researchers can determine the conditions under which most mature larvae will settle into a given habitat and metamorphose from the microscopic larva into a tiny version of the adult.

The twin spiral radioles and stunningly bright colors of Spirobrachus give it the common name of Christmas Tree Worm. Although the taxonomy of the group is yet to be worked out, most worms in this genus appear to be obligate associates of live corals. Photo – James Wiseman

OK, with that background, lets move on to the larval settlement preferences of Spirobranchus.  Researchers have examined the settlement preferences of mature larvae of several species of Christmas Tree Worms, and found that the larvae prefer to settle and metamorphose into adults on only certain species of live corals (e.g., Dai and Yang 1995; Marsden 1987; Marsden et al. 1990; Marsden and Meeuwig 1990).  Because it has only recently been discovered that Spirobranchus giganteus is a complex composed of many species, the initial results of worm abundances and larval preferences were very confusing.  For example, one study found that worms in Taiwan showed a distinct preference for Porites lutea, P. lobata, P. lichen, and Montipora informis (Dai and Yang 1995), whereas in Barbados, researchers found that Porites was not colonized as frequently as a number of other corals including  Diploria strigosa and Millepora complanata (Hunte et al. 1990a).  Now that we understand that there are many species of these worms, these initially conflicting results make more sense: different species of Christmas Tree Worms are doing different things.

Taken together, the few studies of Spirobranchus habitat preferences suggest that worms of a given species still inhabit a wide range of corals within a given region.  Larval settlement appears to occur on dead portions of a colony adjacent to living coral tissue, even if the dead patch has been previously colonized by turf or filamentous algae (Nishi and Kikuchi 1996).  Worm larvae show specific preferences for certain species of corals, and this larval preference seems to explain their abundance on different coral colonies as adults – larvae settle with much higher frequency in response to corals on which adults are common than on those on which adults are rare in the field (Marsden 1987; Marsden et al. 1990; Marsden and Meeuwig 1990).  However, it gets more complicated, because worms are almost always clumped on coral colonies, and researchers have shown that larvae are also attracted to one another, and tend to settle in groups on certain corals (e.g., Marsden 1991).  Thus, the presence of a worm on a coral increases the probability that future larval recruitment will occur nearby, even if there are uncolonized corals of the same species nearby.  In the Caribbean, researchers found that larval settlement preference did not correlate with the total surface area of coral available to larvae (i.e., they did not choose the most abundant corals), mean coral colony size (i.e., they did not choose the largest coral colonies), nor with the rank of the coral in an aggression hierarchy (i.e., they did not choose the colonies most aggressive colonies that avoid overgrowth by others).  Worms were found most frequently, and in the greatest abundance in colonies of Diploria strigosa, Porites astreoides and Millepora complanata.  Montastrea annularis, Madracis spp. and Agaricia spp. also had a moderate number of live worms, whereas Porites porites, Diploria labyrinthiformes, Montastrea cavernosa and Siderastrea siderea were all sparsely colonized by Christmas Tree Worms (Hunte et al. 1990a; Hunte et al. 1990b; Marsden et al. 1990).

These researchers found that the larval settlement preferences of worms matched the adult surveys, and suggested that the distribution of Christmas Tree Worms is largely controlled by larval settlement preference (Hunte et al. 1990a; Hunte et al. 1990b; Marsden et al. 1990).  However, if worms are not choosing the most abundant, biggest or most aggressive corals, why are the larvae attracted to certain species?  Well, it turns out that the larvae prefer to settle in coral colonies in which they tended to do the best.  When researchers went a step further, and examined the average size, age, growth and survival rates of worms on different coral species, they found that worms that settled on Diploria strigosa did the best, followed by those living in Montastrea annularis and M. cavernosa, and with Porites porites being solidly in last place for every measure of growth or survival measured for the worms (Hunte et al. 1990b)!

I am only presenting a single example here for a reason, however, because as I mentioned above different researchers often find different results in different regions (including everything from which corals are preferred by mature larvae, and in which corals juvenile worms do best).  The differences found among researchers suggests that either there is a lot of variation among the worms in different portions of their range, or that there are still more similar but unidentified species that are mistakenly being tested as the same animal.  Until we know what causes the observed variation in these results, it is difficult to make accurate generalizations about the habits and care of any particular worm brought into the aquarium hobby.  However, regardless of the study which we consider, of the more than 30 species of coral with which worms in the genus Spirobranchus are associated, the rate of growth and survival is typically lower in Porites than a large number of other coral species.

As far as I can tell from the research done on these worms to date, however, the reason that they are found almost entirely in association with live corals has little to do with nutrition.  I cannot find a single study in which nutrition derived from the living coral was considered a factor in the survival or growth of these worms. In fact, as far as I can tell from the research conducted to date, the association of worms with live coral seems to result more from a need for protection rather than nutrition. When researchers examined the boring invertebrate communities in corals that are live, and compared them to those communities in which 50%, or 100% of the colony was dead, they found big differences (Nishi 1996).  In living corals, only 3 species of invertebrate were commonly found (a bivalve mollusc, a vermetid tube snail and the Xmas Tree Worms).  The number of species boring through the colony and the amount of the coral’s carbonate skeleton lost to tunneling activity increases quickly with the proportion of the coral colony that is dead.  Completely dead colonies were rapidly colonized by 17-18 species of boring invertebrates (the most significant and destructive of which are the sipunculans, or peanut worms) which remove an average of 14.2 kg of carbonate skeleton per cubic meter of reef per year (Peyrot-Clausade et al. 1992).  In addition, parrotfishes and grazing echinoderms (including urchins, brittle & serpent stars) removed an additional 5.25 kg per m3 and together these boring activities are pretty likely to ensure that the worms don’t survive for long once the coral dies (Peyrot-Clausade et al. 1992). These boring invertebrates are responsible for the breakdown of dead coral skeletons into coral sand and play an important role in natural reef communities.  However, they make life very difficult for the Christmas Tree Worms, because it is unlikely that the boring invertebrates would differentiate between the calcareous tube of Spirobranchus and that of the dead coral.  Removal of portions of the worm tube exposes the body of the worm to attack from predators, pathogens and other additional stresses not experienced when the worms inhabit a healthy live coral.  It is therefore not surprising that the worms aren’t found in many dead coral skeletons, but it doesn’t mean that the worms are somehow eating coral mucus.

Unlike most worms that only live for relatively short times (a few years on average), Spirobranchus are a relatively slow growing worm that lives for a very long time in the wild. Researchers used X-rays to determine the age of the worm by counting the annual growth rings of the corals in which they were embedded, and found that the majority of worms were more than 10 years old and some were over 40 years of age (Nishi and Nishihira 1996)!  On average, a healthy worm grows about 0.2mm in the diameter of the tube opening each year, but under ideal conditions the maximum growth rates are up to 1.0 mm increase in orifice diameter per year (Nishi and Nishihira 1996).  In any case, these worms appear to average roughly 15-20 years old in some natural populations (Nishi and Nishihira 1999), which means that they should easily live for more than 10 years on average in the aquarium, if provided with proper care.

In closing there is no indication that these worms feed on anything different than the majority of other tube-dwelling serpulid polychaetes do: a mixture of primarily phytoplankton with some small zooplankters thrown in as the worm grows to maturity.  However, having said that, I cannot find a single study of prey preference or gut content analyses of Spirobranchus in the wild (so anything is possible, and a new study may warrant a new article).   The fact that Spirobranchus are generally imported with pieces of Porites does not mean that they are obligate associates of this coral, nor does it mean that they are feeding off the mucus of the coral.  In fact, depending on the source you check, the best coral associate for Spirobranchus is likely to be something other than Porites, and even within the genus Porites, P. lutea, P. lobata, and P.lichen appear to be much better ‘hosts’ than does P. porites. Furthermore, in the hands of experienced aquarists, success with these worms appears to be the same whether the coral is alive or dead (obviously aquarists who are unable to maintain Porites and have a healthy colony rapidly die in their tanks tend to have lower success with the worms in that colony as well).  However, our dismal success rate with these animals for more than a year or so in the aquarium suggests that we are failing to provide them with anything approaching ‘proper’ care!  That means we cannot delude ourselves into thinking that the animals died of old age if they fade in our aquariums within a year or two (no matter how comforting we may find that excuse), and that is why I suggest they be avoided by any but experienced aquarists who want to experiment with maintaining these beautiful animals.

References

1. Dai, C.-F., and H.-P. Yang. 1995. Distribution of Spirobranchus giganteus corniculatus (Hove) on the coral reefs of southern Taiwan. Zoological Studies 34:117-125.
2. Frank, U., and H. H. A. Ten. 1992. In vitro exposure of Spirobranchus giganteus and Spirobranchus tetraceros (Polychaeta, Serpulidae) to various turbidities: Branchial morphologies: An expression of filtering strategies? Oebalia 18:45-52.
3. Hunte, W., B. E. Conlin, and J. R. Marsden. 1990a. Habitat selection in the tropical polychaete Spirobranchus giganteus: I. Distribution on corals. Marine Biology (Berlin) 104:87-92.
4. Hunte, W., J. R. Marsden, and B. E. Conlin. 1990b. Habitat selection in the tropical polychaete Spirobranchus giganteus: III. Effects of coral species on body size and body proportions. Marine Biology (Berlin) 104:101-108.
5. Marsden, J. R. 1987. Coral preference behavior by planktotrophic larvae of Spirobranchus giganteus corniculatus (Serpulidae:Polychaeta). Coral Reefs 6:71-74.
6. Marsden, J. R. 1991. Responses of planktonic larvae of the serpulid polychaete Spirobranchus polycerus var. augeneri to an alga, adult tubes and conspecific larvae. Marine Ecology Progress Series 71:245-251.
7. Marsden, J. R. 1992. Reproductive isolation in two forms of the serpulid polychaete Spirobranchus polycerus (Schmarda) in Barbados. Bulletin of Marine Science 51:14-18.
8. Marsden, J. R., B. E. Conlin, and W. Hunte. 1990. Habitat selection in the tropical polychaete Spirobranchus giganteus: II. Larval preferences for corals. Marine Biology (Berlin) 104:93-100.
9. Marsden, J. R., and J. Meeuwig. 1990. Preferences of planktotrophic larvae of the tropical serpulid Spirobranchus giganteus (Pallas) for exudates of corals from a Barbados (West Indies) reef. Journal of Experimental Marine Biology and Ecology 137:95-104.
10. McEdward, L. 1995. Ecology of Marine Invertebrate Larvae. CRC Press, Inc., Boac Raton, FL.
11. Nishi, E. 1996. Serpulid polychaetes associated with living and dead corals at Okinawa Island, Southwest Japan. Publications of Seto Marine Biological Laboratory 37:305-318.
12. Nishi, E., and T. Kikuchi. 1996. Preliminary observation of the tropical serpulid Spirobranchus giganteus corniculatus (Pallas). Publications from the Amakusa Marine Biological Laboratory Kyushu University 12:45-54.
13. Nishi, E., and M. Nishihira. 1996. Age-estimation of the Christmas tree worm Spirobranchus giganteus (Polychaeta, Serpulidae) living buried in the coral skeleton from the coral-growth band of the host coral. Fisheries Science (Tokyo) 62:400-403.
14. Nishi, E., and M. Nishihira. 1999. Use of annual density banding to estimate longevity of infauna of massive corals. Fisheries Science (Tokyo) 65:48-56.
15. Peyrot-Clausade, M., P. Hutchings, and G. Richard. 1992. Temporal variations of macroborers in massive Porites lobata on Moorea, French Polynesia. Coral Reefs 11:161-166.
16. Rouse, G. W., and F. Pleijel. 2001. Polychaetes. Oxford University Press, Oxford, UK.
17. Shimek, R. 1998. Consequences of suspension-feeding. Aquarium.Net Summer. (http://www.aquarium.net/0498/0498_3.shtml).
18. Toonen, R. J. 2002. Invertebrate Non-Column: The care of non-photosynthetic gorgonians. Advanced Aquarists Online Magazine 1(3).  (http://www.advancedaquarist.com/issues/2002/3/inverts)