In
this column I will discuss some of the most colourful and controversial
sea cucumbers in the hobby – the sea apples.“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.
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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.
Proud sponsor of this column
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.
Proud sponsor of this column
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!
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