Aquarium Invertebrates: Sea Apples

by | Mar 15, 2003 | 1 comment

Death in a Colorful Package” is a title that has been used several times (e.g., Friese 1973, Wilkens 1998) to describe a marine invertebrate with aposematic coloration. Aposematic coloration is defined as a specific set of conspicuous colors and/or patterns of marking on an animal to make it easily recognizable in order to warn potential predators that the animal is poisonous, foul-tasting or otherwise potentially dangerous. Monarch butterflies ( Danaus plexippus ) and Poison arrow frogs ( Dendrobates spp.) are two of the best known examples of such coloration patterns. Among marine invertebrates, perhaps the best known example are the spectacularly-colored dorid sea slugs (better known as simply nudibranchs in the hobby) which sequester toxic compounds or stinging cells from their prey. In each case, the brilliant and easily recognizable color patterns of these species make it very easy for a potential predator to remember that taking a bite of these animals is a highly unpleasant experience. Such chemical defenses are wide-spread among marine taxa, and many invertebrate and algal species defend themselves by producing foul- tasting chemicals that are avoided by most predatory species (e.g., Bryan et al. 1997, Chanas & Pawlik 1995, Lindquist & Hay 1996, Pawlik et al. 1995, Stachowicz & Hay 1999). However, not all colorful species are toxic or distasteful, and not all toxic or distasteful species are colorful. For example, some species of very colorful marine sponges appear to be completely undefended whereas some blandly-colored and cryptic species are highly defended with nasty or toxic chemicals (reviewed by Pawlik et al. 1995). One example of a species that lacks obvious bright coloration is the marine alga, Desmarestia, which concentrates sulfuric acid in species vacuoles throughout their cells. In fact, this alga can contain up to 16% of its body weight as concentrated sulfuric acid baggies (Pelletreau & Muller-Parker 2002). This concentrated sulfuric acid drops the pH of macerated algal tissue to < 2.0, and acts to both make the alga highly distasteful and to actually dissolve the carbonate teeth of potential grazers such as urchins. Field and laboratory studies with these algae and artificially acidified foods have shown that containing concentrated sulfuric acid is a great way to discourage potential predators from feeding on these algae (Pelletreau & Muller-Parker 2002).

In the aquarium industry, however, “death in a colorful package” is most often applied to the strikingly-colored group of sea cucumbers known as Sea Apples. Let me first explain what a sea apple actually is. These commonly imported suspension feeding sea cucumbers (see my previous sea cucumber columns for more information Toonen 2002, 2003) belong to the genus Pseudocolochirus. The most common species found in pet shops is the Indonesian Sea Apple, P. axiologus although the more colorful Australian Sea Apple ( P. violaceus ) has become a much more common import recently as well. Both species are obligate filter-feeders and have obvious rows of tube feet which they use to attach themselves to some substrate in an area of high flow. The high flow allows them to expose their feeding tentacles to the greatest amount of passing water in order to collect suspended organic particles on which to feed. These attractive animals remain relatively small, and a full grown animal would probably average about 10cm (4″) in length. However, they are also capable of greatly inflating their bodies with water under certain conditions. When disturbed, unhappy or otherwise stressed by local conditions, a sea apple can react in one of two ways: 1) they can shut down and collapse their body to the minimum possible size, or 2) they can inflate themselves to more than double their normal size (some can reach the size of a volleyball) and either ride the current, or “gallop” around the aquarium (at least it seems like galloping for a sea cucumber). Quite often when people see a fully engorged sea apple at the local petshop, they assume that the animal is healthy, but more often than not, this is an indication of stress for the animal.

Ok, having explained what a sea apple actually is, let’s get down to the discussion of why they have such a dangerous reputation among reef aquarists. As I explained above, many marine plants and animals defend themselves from being eaten by having some sort of chemical defense that makes them toxic or highly distasteful to potential predators. These brightly colored sea cucumbers are popular because they are so beautiful, but in this case, sea apples are one of those species that appear to advertise the fact that they are toxic by having bright and easily recognizable color patterns on their bodies. The potent chemical defenses of these colorful sea cucumbers can be extremely toxic to fish and other coral reef inhabitants in an enclosed aquarium. The dangerous reputation of this attractive sea cucumber is certainly based in reality, however, as I explained in my previous articles (Toonen 1998b, 2002, 2003), sea cucumbers have a variety of defenses that are generally tried before they resort to a general release of their toxic chemicals for defense. In general, it is only when a sea apple is extremely stressed that they will actually release the toxic chemicals that are capable of wiping out an aquarium, and many people have had one of these animals die in their tanks without any evidence of toxic release. Furthermore, there are many animals that we commonly keep in our tanks (in particular some sponges and zooanthids) that have much more potent chemical defenses than do sea apples. So, basically the main reason that sea apples are potentially dangerous to a reef aquarium has less to do with their chemical defenses than with the fact that they move around and are more likely to meet an unpleasant end in our reef tanks than an equally toxic sponge or soft coral.

In addition to the other signs of stress that I mention in my previous articles, the most drastic response a stressed cucumber can make is to expel its Cuvierian tubules. The tubules of Cuvier are a series of long, spaghetti-like tubes leading off the hindgut – the cucumber equivalent of a colon – at the base of the respiratory tree – the sea cucumber equivalent of gills. The Cuvierian tubules are expelled by rupturing the hindgut, and this dramatic defensive ploy is almost always accompanied by the release of a soup of defensive chemicals that are likely to seriously impact, and potentially wipe out an enclosed tank. Although the effect of these defensive chemicals are rarely lethal in the wild, more than 96% of predators exposed to a cucumber after having previously experienced the defensive chemicals remained far away from the cucumbers (Hamel & Mercier 2000). I have discussed cucumber responses to stress at detail in the previous articles listed above, so I won’t go into detail on the subject again here. However, I do want to say something about the dire warnings that often appear on the web about ever adding a sea cucumber to an aquarium. While I will repeat that it certainly is possible for a sea apple to kill tankmates if sufficiently stressed, I have often included a sea apple in my own tanks without any problems. If proper precautions are taken to ensure that the sea apple is not damaged by a pump intake or overflow, chances are very slim that you’ll ever see any evidence of the toxicity of these animals. In my experience, reports of “cuke nukes” most often occur when the tank is small, runs an undersized (or no) skimmer, does not use or regularly replace carbon, or when the tank is not checked on a daily basis (such as when someone goes away for vacation and has a friend look after their tank). Sadly, I have had a number of sea cucumbers (including sea apples) meet an unpleasant end in my aquariums over the years, and have never suffered a wipe out from any of these unfortunate events. I attribute my “luck” with sea cucumbers to catching the problem early, doing extensive water changes and increasing skimming and carbon use to remove the toxins as quickly as possible. If any large animal, such as a sea cucumber, dies in an aquarium and is not immediately dealt with, it will cause problems with water quality. I suspect that because cucumbers do not move around very much, and few people know exactly what to expect in terms of their behavior, many people may miss a dead animal simply because they do not know what to look for. Obviously a chemical defense would not be particularly useful if it also kills the animal that it is supposed to be defending – therefore we should not hear reports of “cuke nukes” in which the cucumber was also killed. It seems to be common that web reports of tanks affected by sea cucumbers also include the sea cucumber itself among the casualties, and therefore, at least some of these “cuke nukes” reported on the web are likely to be the result of insufficient attention to a decaying animal in the aquarium.

Now, if you were reading carefully there, you should have caught the fact that I mentioned the Cuvierian tubules are “leading off the hindgut at the base of the respiratory tree” – but if the respiratory tree is associated with the hindgut, that must mean that the breathing structures (respiratory tree) is close to the butt end of the animal, and how can that be? Well, one of the most interesting features of sea cucumbers for most people is that fact that they do, indeed, breathe through their butts! Often when people first see a sea apple, the animal is closed up in the tank of the local petshop waiting to detect phytoplankton so it can begin feeding (I’ll discuss this further below). If you watch the animal closely for a while, you’ll see a small hole opening and closing as the animal first “inhales” water into the respiratory tree and then “exhales” it again. This breathing behavior (or more correctly, respiration) is very familiar to us, and people typically assume that the end
which is doing that breathing is the front, but in this case, the respiratory tree is attached to the cloaca (a common opening for waste from both the urinary tract and the gut found in most animals other than mammals, which have a separate opening for each excretory function) and it is actually the anus which is opening and closing as the animal inhales and exhales. The rate of water exchange is dependent on temperature, but is generally quite slow in these animals. On average it takes 5-10 “breaths” (a cycle of dilation and contraction of the cloaca) to completely fill the respiratory tree, and depending on the temperature and the size of the animal in question, each “breath” could take as much as one minute. Once the tree is completely filled, the entire volume of water is typically expelled in a single large contraction. It is during such contractions that wastes (including both urine and feces) are generally also expelled in a jet away from the animal. Observing an animal
defecate is a very good sign, because if you never see your sea apple poop, there is a good chance that it is not getting enough food.

I will come back to a discussion of whether or not your animal is getting enough food below, but I first wanted to make a brief aside while on the subject of anal respiration. I probably should have discussed this in one of the more general sea cucumber articles in the past couple of columns, but because I did not, I’ll mention it here. There are actually a variety of fishes that are specialized to take advantage of this constant flow of water through the respiratory tree of sea cucumbers while simultaneously gaining the protection of living within the sea cucumber itself. I have occasionally responded to questions from reef keepers who suddenly discover a thin silvery fish, closely resembling a small freshwater knife-fish (e.g., Notopterus or Xenomystus spp.) that was never added intentionally to the aquarium suddenly cruising the tank at night. This is most likely a slender pearlfish (e.g., Carapus or Encheliophis spp.) which make their daytime home wedged into one of the branches of respiratory trees of several common species of sea cucumbers. At night many of these fish emerge from the anus of the sea cucumber in search of food. The food preference varies among different pearlfish species, with some (such as Carapus acus, Encheliophis boraborensis, and E. homei ) being primarily predatory animals in search of small fish and crustacean prey (such as mysid shrimp and amphipods), while others (such as Encheliophis gracilis ) is a specialist on the tissue of the sea cucumber host in which they live (Parmentier et al. 1998). These fish typically return to the protective shelter of the well-ventilated respiratory tree of their host sea cucumber during the daylight hours and emerge to hunt again during the dead of night. In addition to these fish, there are a number of polychaete worms (e.g., Britaev & Zamyshlyak 1994) and tiny crab species (e.g., Hamel et al. 1999, Takeda et al. 1997) that take similar advantage of the safe haven provided inside the body cavity of sea cucumbers.

Ok, coming back to the issue of feeding, after water quality, one of the most important determinants of how well an animal is likely to do in a given aquarium is its nutritional condition. Not surprisingly, if an animal is not getting enough food, chances are slim that it will survive for long regardless of how good the water quality is kept in the tank. Whether or not a sea apple is getting enough food in the aquarium is typically a function of three primary factors: 1) is the correct food available and in sufficient quantity for them; 2) flow rates – like most suspension feeding sea cucumbers, these animals are able to feed most efficiently under a relatively narrow range of specific water flow speeds; and 3) the stocking density of the animals in the aquarium – is it sufficiently low that all the animals are able to get sufficient food? I will discuss each of these in further detail below, but first I want to emphasize that sea cucumbers, like most marine invertebrates, require
relatively little energy to sustain themselves, and are quite tolerant of starvation by our standards; a healthy, well-fed sea cucumber imported into an aquarium will likely take something on the order of 6-18 months to starve to death (depending on its size, energy reserves, and whether or not it can occasionally pick up a little food in the aquarium). I often see people on various bulletin boards exclaiming something to the effect of: “sea apples are easy to keep, I’ve had mine for 6 months and it’s doing great.” Unfortunately, many marine invertebrates show few or no obvious signs of starvation, and they deal with periods of low food by digesting their internal organs while waiting for food to become abundant again. The first sign of difficulty for many sea apples is that people notice that it seems to be a little smaller than when they first bought it, but some don’t even notice this. It is only once the animal shrinks significantly that most people decide that something is wrong with the way the animal is being kept, and more often than not, it is really too late to save the animal by that time. As I mentioned above, a good rule of thumb is that if you don’t see an animal pooping, it’s most likely not eating enough! Although I am focussing primarily on sea apples in this column, the recommendations regarding their care and feeding in the aquarium could be equally well applied to most of the suspension feeding sea cucumbers in the hobby (such as Colochirus or Pentacta species).

So, what exactly is the correct food for these animals? Well, if you search around the internet you’ll find a variety of recommendations for what to feed a sea apple. Some of the most common are commercially prepared invertebrate foods and newly hatched baby brine shrimp. Sadly this information is utterly incorrect, and I suspect that the failure of most hobbyists to successfully maintain these animals in captivity is due in large part to the continual offering of this sort of misinformation. The simple fact is that sea apples are suspension feeding cucumbers that specialize on phytoplankton, and even foods that appears small to us (like the baby brine shrimp that are so commonly recommended), are much (I emphasize MUCH) too large for these animals to capture and ingest. Studies in which researchers sifted the gut contents of a variety of suspension-feeding sea cucumbers found that all but one species ate only particles of less than 53 μm in diameter (for comparison, newly hatched brine shrimp are approximately 400 µm, and my survey of commercially prepared invertebrate foods found such products contained a mean particle size of 365 ± 696 µm, see Toonen et al. 2002). Researchers have found that the majority of the diet of suspension feeding sea cucumbers such as sea apples consist of phytoplankton cells (primarily larger species of phytoplankton such as Coscinodiscus, Chaetoceros, Skeletonema, and Thalassiosira ), with occasional ingestion of tiny invertebrate eggs and larvae (Hamel & Mercier 1998). In fact, even full- grown rotifers (which average between 75 and 300 μm, depending on the strain) are too large for most suspension feeding cucumbers to eat, and regardless of the advice offered on the web and by many petshops about what to feed your sea apple, if you are not supplementing your tank with phytoplankton on a daily basis, your sea apple is almost sure to slowly starve to death. In fact, it would be better if you were feeding your tank with phytoplankton at least a couple of times a day to keep these animals healthy. Researchers found that sea cucumbers fill and empty their guts 2-3 times per day in the wild (e.g., Hammond 1982, Sewell & Bergquist 1990), and in order to meet their metabolic demands, these animals need to be fed daily at the very least in the aquarium. Because suspension feeders are generally adapted to continuous feeding, most will generally be healthier if fed small amounts more often than high doses of planktonic food less often. This is a very good reason to dose your tank with half the recommended amount of phytoplankton twice per day rather than adding a heavy dose every few days as many aquarists tend to do…

Until recently the ability to regularly feed phytoplankton to a reef tank was quite a feat, and involved complicated and time-consuming culture techniques to raise greenwater at home. Recently several suppliers have started to market phytoplankton for home aquaria and you can now buy live, frozen or spray-dried phytoplankton cultures to feed your reef in much the same way as you add other prepared foods. There are a number of good articles available online for how to culture phytoplankton at home (e.g., Marini 2002, Toonen 1998a), but it is now so simple to buy phytoplankton to feed to a reef tank rather than growing your own that unless you’ve got a very large tank and are using a lot of phytoplankton, most people opt to simply buy it. If you’re a real do-it-yourselfer, then it is certainly possible and cheap to culture algae at home, but you have to do it correctly or the phytoplankton can not only be non-nutritious, under some improper culture conditions, it can be downright toxic (see, Toonen 1998a). If you want to culture phytoplankton, then take the time to read some of the articles above and do it properly. Otherwise, I’d suggest purchasing your phytoplankton and let someone else do the work of culturing the stuff for you.

Sea apples, like most suspension feeding sea cucumbers tend not to waste energy trying to feed if there is nothing around for them to eat. The animals are very sensitive to both flow conditions and the presence of phytoplankton in the water. In my tank, the sea apple will close for days if no phytoplankton is added to the tank, but will start to feed actively within literally seconds of adding phytoplankton to the aquarium. I have actually done this demonstration with a sea apple from one of the local petshops which had not opened since it arrived, and despite the stress of being pulled from the tank and stuck into a bag, by simply adding a squirt of phytoplankton to the bag, I got the animal to open up and immediately start feeding in the bag. In nature, suspension feeding sea cucumbers such as sea apples tend to feed on a regular daily basis. In experiments using large flow-through aquaria fed by unfiltered natural seawater, the regular daily feeding schedule was shown to
coincide with the maximum amount of phytoplankton coming through the system each day (Rabindra et al. 1998). However, when researchers began to filter the seawater, the regular timing of feeding in these cucumbers quickly broke down. The researchers subsequently found that hungry animals in flowing seawater could be induced to feed at any time by simply adding cultured phytoplankton to the tank water (Rabindra et al. 1998).


This sea apple ( Pseudocholochirus ) has extended its tree-like feeding tentacles into the water column to capture tiny planktonic food. Although these animals have a reputation for being extremely dangerous to a coral reef aquarium, they only cause problems in self-defense. A sea apple can make an attractive and interesting addition to well-designed aquarium in which the animal is protected from pump intakes and receives appropriate and sufficient food. Photo by Julian Sprung

One more detail that I think is worth explaining is that like most suspension feeders, these animals use mucus to trap particulates from the water column. However, like other sea cucumbers they lack mucus secreting cells on the feeding tentacles themselves, and instead have a small sac-like structure inside the mouth where the tentacles are covered in mucus before being stuck forth into the water flow to trap more particles. Once a tentacle becomes covered with phytoplankton, that tentacle is popped into the mouth and sucked clean (just like us using our fingers to eat from a honey jar) before being covered in mucus within that sac and deployed once again. This is what leads to the stereotypic feeding behavior of all holothurians in which a single tentacle is withdrawn and sucked clean while the rest are left extended. If the tentacles are not being withdrawn to the mouth on a regular basis, the cucumber is not actually feeding, and the frequency of tentacle withdrawal can be used as a reasonable gauge for how well an animal is feeding. On average, these animals should be sucking a tentacle clean and re-deploying it about once per minute, and it will be faster if the animal is provided with high quality food, such as live phytoplankton, and slower if offered a low quality food such as a commercial invertebrate food based on pea flour and yeast. If the tentacle withdrawal rate is significantly slower than one per minute, then the animal is not getting enough or the proper quality food to feed effectively, and you can be confident that it will eventually starve in your aquarium. If your sea apple is not extending its feeding tentacles, there is a serious problem with either the flow regime or the food that it is being offered.

Despite the recent availability of phytoplankton products in the hobby, however, sea apples continue to have a relatively low rate of success in captivity. In fact, a recent poll of aquarists on the internet suggested that very few people had kept one of these animals alive for 3 years or more. Estimates of the first age of reproduction for many sea cucumbers is on the order of 4-5 years old, and many cucumbers have been found to live for 35 years or more in nature (e.g., Herrero-Perezrul et al. 1999). Given a potential lifespan of decades, our failure to keep these animals alive for any reasonable length of time in captivity is very discouraging. In addition to the misinformation regarding the feeding requirements of these animals, I believe that this low rate of success is also a function of at least a couple of other factors. The first is incorrect flow rate, and the second is physical damage in the aquarium. As I mentioned above, both the presence of food and the proper flow rates are generally necessary for animals to effectively feed. Flow rates need to be reasonably high in order for suspension-feeding sea cucumbers to be able to collect food effectively. In the lab, it appears that turnover rates of between 7-10 tank volumes per hour are required for sea cucumbers to feed in a natural manner (Rabindra et al. 1998). To some extent you can compensate if you do not have a sufficient flow rate in your aquarium by placing your sea apple closer to a pump outlet, but in general, these animals tend to be a moderate flow animal, and do not generally thrive in extremely low flow regimens.

Stocking density is a complicated issue, and it is often difficult to give good recommendations for a specific value for appropriate stocking density because every aquarium is unique, and the conditions vary from one tank to the next. However, stocking density is an important consideration, and most people have a natural tendency to overstock their aquarium rather than understock it. Stocking density has a dramatic effect on growth even in nature, but growth rates of sea cucumbers are even more strongly dependent on the stocking rate in aquariums. Using the sea cucumber Actinopyga mauritiana, researchers found that stocking rates in excess of 26 g of sea cucumber per square meter of sediment led to reduced growth rates, and growth stopped completely as cucumbers reached 250-300 g / m2 (Ramofafia et al. 1997). Although this is difficult to convert to a specific recommendation for stocking densities in an average reef aquarium, something on the order of 3” of cucumber per 20 gallons of reef aquarium seems to be a good rule of thumb to follow in case of doubt (e.g., Sprung 2001, Toonen 2003). It is rare that people stock multiple sea apples into a tank, but because few people feed phytoplankton at densities approaching natural concentrations (typically on the order of 100,000 cells per ml, see Toonen & Pawlik 2001), and because these animals require a substantial amount of phytoplankton food to maintain themselves, it is easy to overstock them as well. If in doubt, an understocked aquarium is always better than an overstocked one…

Well, hopefully that provides you with sufficient information to make an educated decision about whether or not your aquarium is suitable for a sea apple. If you decide that you would like to add one of these beautiful and fascinating animals to your tank, I also hope that the information that I have provided here will allow you a good chance at keeping it healthy and happy for a long time in your aquarium!


Literature Cited

  1. Britaev, T.A., & E.A. Zamyshlyak. 1994. The biology of a commensal polychaete Gastrolepidia clavigera (Polychaeta, Polynoidae) with remarks on the biology of host holothurians (Holothuriidae, Stichopodidae). Zoologicheskii Zhurnal 73:39-53.
  2. Bryan, P.J., J.B. McClintock, & T.S. Hopkins. 1997. Structural and chemical defenses of echinoderms from the northern Gulf of Mexico. Journal of Experimental Marine Biology and Ecology 210:173-186.
  3. Chanas, B., & J.R. Pawlik. 1995. Defenses of Caribbean sponges against predatory reef fish. II. Spicules, tissue toughness, and nutritional quality. Marine Ecology Progress Series 127:195-211.
  4. Friese, U.E. 1973. Marine Invertebrates. T.F.H. Publications, Inc., neptune City, NJ.
  5. Hamel, J.F., & A. Mercier. 1998. Diet and feeding behaviour of the sea cucumber Cucumaria frondosa in the St Lawrence estuary, eastern Canada. Canadian Journal of Zoology-Revue Canadienne De Zoologie 76:1194-1198.
  6. Hamel, J.F., & A. Mercier. 2000. Cuvierian tubules in tropical holothurians: Usefulness and efficiency as a defence mechanism. Marine and Freshwater Behaviour and Physiology 33:115-139.
  7. Hamel, J.F., P.K.L. Ng, & A. Mercier. 1999. Life cycle of the pea crab Pinnotheres halingi sp nov., an obligate symbiont of the sea cucumber Holothuria scabra Jaeger. Ophelia 50:149-175.
  8. Hammond, L.S. 1982. Patterns of feeding and activity in deposit-feeding holothurians and echinoids (Echinodermata) from a shallow back-reef lagoon, Discovery Bay, Jamaica. Bulletin of Marine Science 32:549-571.
  9. Herrero-Perezrul, M.D., B.H. Reyes, F. Garcia-Dominguez, & C.E. Cintra- Buenrostro. 1999. Reproduction and growth of Isostichopus fuscus (Echinodermata: Holothuroidea) in the southern Gulf of California, Mexico. Marine Biology 135:521-532.
  10. Lindquist, N., & M.E. Hay. 1996. Palatability and chemical defense of marine invertebrate larvae. Ecological Monographs 66:431-450.
  11. Marini, F. 2002. The Breeders Net: Phytoplankton Culture. in Advanced Aquarists Online Magazine. Aug 2002.
  12. Parmentier, E., M. Chardon, M. Poulicek, J.C. Bussers, & P. Vandewalle. 1998. Morphology of the buccal apparatus and related structures in four species of Carapidae. Australian Journal of Zoology 46:391-404.
  13. Pawlik, J.R., B. Chanas, R.J. Toonen, & W. Fenical. 1995. Defenses of Caribbean sponges against predatory reef fish. I. Chemical deterrency. Marine Ecology Progress Series 127:183-194.
  14. Pelletreau, K.N., & G. Muller-Parker. 2002. Sulfuric acid in the phaeophyte alga Desmarestia munda deters feeding by the sea urchin Strongylocentrotus droebachiensis. Marine Biology 141:1-9.
  15. Rabindra, S., B.A. MacDonald, P. Lawton, & M.L.H. Thomas. 1998. Feeding response of the dendrochirote sea cucumber Cucumaria frondosa (Echinodermata:Holothuroidea) to changing food concentrations in the laboratory. Canadian Journal of Zoology 76:1842-1849.
  16. Ramofafia, C., T.P. Foyle, & J.D. Bell. 1997. Growth of juvenile Actinopyga mauritiana (Holothuroidea) in captivity. Aquaculture 152:119-128.
  17. Sewell, M.A., & P.R. Bergquist. 1990. Variability in the reproductive cycle of Stichopus mollis (Echinodermata: Holothuroidea). Invertebrate Reproduction and Development 17:1-17.
  18. Sprung, J. 2001. Invertebrates: A Quick Reference Guide. Sea Challengers, Danville, CA.
  19. Stachowicz, J.J., & M.E. Hay. 1999. Mutualism and coral persistence: The role of herbivore resistance to algal chemical defense. Ecology 80:2085-2101.
  20. Takeda, S., S. Tamura, & M. Washio. 1997. Relationship between the pea crab Pinnixa tumida and its endobenthic holothurian host Paracaudina chilensis. Marine Ecology-Progress Series 149:143-154.
  21. Toonen, R. 1998a. Green Water: The Culture of Marine Phytoplankton. in GARF Reef Aquarium Farming News. No. 13(2).
  22. Toonen, R., K. Batchelor, & T. Mai. 2002. Planktonic Foods for Reef Aquaria: If you feed the tank, are these foods for you? Marine Fish & Reef USA Annual 2002:18-31.
  23. Toonen, R.J. 1998b. Cucumber Defenses. www document:
  24. Toonen, R.J. 2002. Invertebrate Non-Column: The Medusa Worms. in Advanced Aquarists Online Magazine. November 2002.
  25. Toonen, R.J. 2003. Invertebrate Non-Column: Sea cucumbers – Part II. in Advanced Aquarists Online Magazine. January 2003.
  26. Toonen, R.J., & J.R. Pawlik. 2001. Settlement of the gregarious tube worm Hydroides dianthus (Polychaeta : Serpulidae). II. Testing the desperate larva hypothesis. Marine Ecology-Progress Series 224:115-131.
  27. Wilkens, P. 1998. Death in a Colorful Package. in Aquarium Frontiers Online May 1998.

1 Comment

  1. Ethan

    How has no one replied to this 18 year old article yet??? It’s brilliant! Incredibly indepth and helpful, thank you!


Submit a Comment

Your email address will not be published. Required fields are marked *