Goniopora
Revisited: If We Could Keep It Alive, Do We Really Want To?
High
Levels of Toxicity in Goniopora
and Other Hard Corals
When I wrote Aquarium
Corals, I was beginning to read some papers that suggested that
stony corals, like soft corals, might produce their fair share of
secondary metabolites. By this, I mean that while early investigators
either failed to look for – or failed to find – bioactive chemicals
in stony corals, some recent investigations indicated that they are
indeed present. It had been largely assumed that, because stony corals
had a protective skeleton, that they had little need for protective
chemicals. In contrast, soft corals, sponges, and other soft bodied
invertebrates were studied extensively and found, as would be expected
of sessile animals, that a copeia of bioactive compounds were produced
and stored or released by them for a multiplicity of roles. Among these
were allelopathic chemicals used in defense, space competition, and as
anti-predation substances. Additional roles were discovered including
roles in protecting eggs, cueing settlement, attracting sperm, and
others. As massive numbers of novel compounds were found in these taxa,
stony corals remained largely ignored.
I
was able to find some direct and indirect references to the production
of these metabolites in stony corals, and one of the most direct
involved a “toxic exudate” from Gonioporatenuidens (Gunthorpe
and Cameron 1990a). Whether forgetting to
retrieve them, or not noticing the other references in that paper, I
wrongfully assumed this was all that had been written on the subject. It
was not until doing a literature search for the toxic effects of metals
on stony corals for a discussion between Ron Shimek, Randy
Holmes-Farley, and others (http://www.reefcentral.com/vbulletin/showthread.php?s=ef6e4e6f80f5ab895950901faef0ed84&threadid=100591)
that I stumbled across another paper. This time, I was observant enough
to notice that not a few, but many other articles had been written on
the subject. Interestingly, and perhaps among the reasons I had not
found these papers before, was that the majority of them were to be
found in the medical literature. Soon, I found myself completely stunned
at what I had learned, for little of this is new to science. It is
however, new to me, and I believe will be new to most.
In
the Gunthorpe and Cameron (1990a) paper,it was found that a “range of bioactivity, as aqueous
extracts from Australian specimens displayed consistent toxicity
to mice and cytolytic activity, while exhibiting interspecific
variation in antibiotic activity and ichthyotoxicity.” An
investigation was done to determine the effect of alellochemicals
previously described (Gunthorpe and Cameron 1990b) as being toxic
to scleractinians; in this study, the effects of G.
tenuidens towards Galaxea
fascicularis.
Individual polyps of Galaxea
were placed in aerated seawater with 3-4 cm portions of G. tenuidens and examined after 0, 12, and 24 hours (called
“conditioned seawater). They were then transferred to another
tank with flowing seawater and observed. “Conditioned seawater
was determined to be toxic to a test species when all corals of
that species showed signs of intoxication.” It was found that
conditioned seawater of 8 of 10 Goniopora colonies was toxic to at least one of the test species,
and the signs of intoxication were consistent in all cases. Goniopora
exudate was lethal to Galaxeafascicularis, inducing sustained polyp contraction, increased mucus
production, loss of tissue coloration, and loss of tissue from the
skeletal matrix. No Goniopora
exudate was lethal to other Goniopora.
Sub-lethal signs included polyp contraction and increased mucus
production reversed after a half hour exposure to fresh seawater.
The fact that Goniopora species could cause such a reaction and death in the
strongly aggressive Galaxea
within one day is remarkable. It is, however, only the beginning.
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Gunthorpe
and Cameron (1990c) have yet another study using
Lobophyllia coymbosa, Favites abdita, Favia matthaii, Favia
stelligera, Platygyra daedaelea, Leptoria phrygia, Cyphastrea
serailia, Hydnophora exesa, and
Astreopora myriophthalma as test subjects.
In this study, they examined toxicity to mice, toxicity to a coral
(Galaxeafascicularis),
toxicity to a hydroid (Solandaria
fusca), cytolytic activity on sheep erythrocytes and sea
urchin ova, and for antibacterial activity against eight bacterial
species. They found that regardless of species, extracts from
these corals induced sustained contraction of polyps, increased
mucus production, loss of tissue coloration, and loss of tissue
from the skeletal matrix. In summary, extracts of each colony of
each species produced a positive response in at least two of the
assays and activity was highest in the activity against corals and
mice, and also in cytolysis of red blood cells.
The
next Gunthorpe and Cameron paper (1990b) examined aqueous extracts
of 58 scleractinian species from 11 families (Table 1).
Acanthastrea
(1 species)
Symphyllia
(3 species)
Lobophyllia
(3 species)
Favites
(5 species)
Favia
(7 species)
Cyphastrea
(2 species)\
Platygyra
(1 species)
Montastrea
(3 species)
Goniastrea
(5 species)
Leptoria
(1 species)
Leptastrea
(1 species)
Oulophyllia
(1 species)
Australogyra
(1 species)
Echinopora
(1 species)
Porites
(1 species)
Goniopora
(1 species)
Hydnophora
(1 species)
Merulina
(1 species)
Pavona
(2 species)
Astreopora
(1 species)
Acropora
(5 species)
Coscinarea
(2 species)
Psammacora
(2 species)
Galaxea
(1 species)
Acrhelia
(1 species)
Fungia
(1 species)
Pocillopora
( 1 species)
Seriatopora
(1 species)
Turbinaria
(1 species)
Table 1. Genera used in bioactivity and
toxicity assays (Gunthorpe and Cameron 1990b)
This
experiment utilized several toxicity assays. In the first, mouse
toxicity was determined by effects of coral extracts in
producing loss of physical responses, lethargy, reduced body
temperature, diarrhea, and death by respiratory paralysis (with
the heart still beating post-mortem). They found at least one
extract from 93% of the species examined was toxic to at least
one test species.Results showed that 38% of 274 colonies assayed were
toxic to mice (at least one colony of 41 species). The most
toxic was Favites abdita
and the least toxic was Leptoriaphrygia. The extracts were found to be slow acting toxins, although
there was a range; Pavonadecussata induced
death to mice in 1.3+/- 0.4 hours and Gonioporatenuidens induced
death within 45 minutes. Extracts of 71% of the toxic colonies
caused death within 24 hours, 28% within 6 hours. The amounts of
extract provided by injection to mice were 0.5 ml of an extract
prepared from the tissue digest of samples or small colonies in
100 ml of water. For example, a single Fungia would produce enough toxin to kill 200 mice within 24 hours
– and Fungia was not
nearly the most toxic coral in this study!
The second toxicity
assay was done by determining ichthyotoxicity to the
mosquitofish, Gambusia
affinis, by placing the fish in 70 ml of water with 500 mg/l
concentrations of the extracts. Only four species (Seriatopora hystrix, Acropora cuneata, Goniopora tenuidens, and Pavonadecussata) were toxic to the mosquitofish. Signs of toxicity
included hypoactivity, ataxia, and reduced visual response to
stimuli.
The third toxicity
assay examined the ability of 500 mg/l
concentration of coral extract to lyse sheep red blood cells. At
least one colony of 49 separate species of 57 tested (153 of 240
colonies, or 64%) was lytic. A majority (73%) were potent lysins,
lysing more than 90% of erythrocytes. Favites
flexuosa was the most lytic, and Goniastrea
australensis was the least lytic.
A final antimicrobial
activity assay was done, and results were similar to those in
Koh (1997a, 1997b, and many others with soft corals and
gorgonians), in that most species showed some to considerable
activity against bacteria. Only five species were found to be
inactive, and this may be due to the types of bacteria used in
the tests – that these species may not have activity against
those tested but may have antibiotic effects against others as
Koh found. In general, Lobophyllia
and Symphyllia extracts were highly antibiotic in this study.
It
is worth mentioning that nematocysts were considered in this
study, and no relationship between discharged nematocysts and
incidence or type of activity of the extracts was found. The
type of toxicity and activity found here is very similar to the
degree, ranges and types of activity found in sponges, soft
corals, algae, and other sessile reef invertebrates (McCaffery
1988, Coll et al. 1982, Bakus 1986 and others listed in
references). In conclusion, the study found that toxins and
cytolysins are widespread in stony corals, although variations
in strength exist within and across species (Table 2).
Areas of densely packed
stony corals (above) and soft corals (below), sometimes
referred to as "coral gardens" are common on
coral reefs. However, both communities produce bioactive
chemicals that have many effects, including toxic ones.
The effect of dilution by sheer ocean volume is probably
is a primary reason for the existence of such crowded
conditions in the wild. Aquariums, with small closed
water volumes, lack this advantage and may suffer from
the consequences of high levels of toxins produced by
all manner of marine plants and animals, including stony
corals. Photos: Eric Borneman
Assaynumber of speciesnotable
Toxic to mice
71%
of 58 species
Goniopora
and Pavona highly toxic
Haemolytic
activity
86% of 57 species
Fungia
and Oculinidae not
haemolytic
Antimicrobial
activity
65% of 55 species
Lobophyllia
and Symphyllia highly
active
Ichthyotoxic
activity
9% of 45 species
Bioactivity,
total
91% of 58 species
Table 2. Summary of results of Gunthorpe
and Cameron (1990b)
An
even earlier study found aqueous extracts from Goniopora
gracilis, G. tenuidens, G. planulata, Cyphastrea chalcidicum, Pavona
ebtusata andan Acropora sp. were
toxic to mice (Hashimoto and Ashida 1973). A later study by Kaul et al.
(1977) found substances pharmacologically active on mammalian
cardiovascular, motor, and CNS systems to be produced by Acropora
cervicornis, A. paniculata, A. palmata, Fungia fungites, Goniastrea
retiformis and Montipora
marshallensis. Grozinger (1983) found a biologically active compound
in Madracismirabilis that is
also found in nudibranchs and sponges. Stony corals can also inhibit
growth of marine algae (De
Ruyter van Steveninck 1988). Finally,
Sheppard (1979) concluded that non-contact necrosis between nearby stony
coral colonies resulted from allelopathic chemicals produced by the
stony corals.
The Goniopora spp.
in the author's tank is an unusual long-term survivor,
having been acquired from another aquarist's tank where
it had survived for several years. However, the genus is
known to produce strong allelopathic substances that can
negatively affect other corals, fish, invertebrates and
even aquarists.
Fearon
and Cameron (1997) later produced a study where five species of
stony corals (Platygyra daedaelea, Gonaistrea favulus, Favia matthai, Pavona decussata,
and Fungia fungites)
were collected, and extracts tested for their effects on the
gametes and planulae of G.
favulus, P. daedaelea, P. decussata, Oxypora lacera, and
Pocillopora damicornis. They were testing to see if extracts
were able to inhibit settlement of other coral larvae. They
found that the extracts of all five species were lethal to
larvae of at least two species at one or more of the
concentrations of 62.5, 125, and 250 mg/l.
Larvae were found to change their shapes, shrink, cease
swimming, and eventually die. Between this study and others (Fearon
and Cameron 1996, Koh 1995), larvotoxins produced by stony
corals can be summarized below (Table 3). Even though it is now
recognized how potently toxic Goniopora tenuidens is, its activity against coral larvae was less
than some of the species studied here.
ProducersNon-producers
Goniopora
tenuidens
Porites
cylindrica
Tubastraea
faulkneri
Seriatopora
hystrix
Platygyra
daedaelea
Goniastrea
favulus
Pavona
decussata
Favia
matthai
Fungia
fungites
Table 3. Stony corals production or
non-production of larvotoxic substances
With regard to Goniopora
toxin, the chemical is a polypeptide toxin (19,000MW) that is a
voltage dependent Ca2+ channel activator, and is
highly active at the 5mM
level (Qar et al. 1986). It is found in varying amounts in all Goniopora
examined to date, and its levels seem to vary temporally and
according to external or environmental factors (as is the case
with the secondary metabolites of most marine organisms). In the
study mentioned above, 95g of Goniopora tissue was sufficient to conduct a large number of tests
on a variety or tissues and organisms, including lethal dose
assays on mammals. During work for an unpublished thesis by
Meredith Peach, she remarked that simply working with Gonioporatenuidens in her
studies on feeding ecology produced a reaction on her skin
severe enough that she had to wear gloves during contact with
the corals or even the water of aquariums housing them (Peach
pers. comm.). Many other studies involving the effects of Goniopora
toxin on physiological and biochemical processes are listed in
the references at the end of this article.
Symphyllia spp. are
one of many stony corals that have been found to produce
toxic secondary metabolites. Photo: Eric Borneman
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At this point, it should be
quite apparent that no longer can we assume that toxicity effects
in closed systems are only by certain commonly maintained
organisms like soft corals. The fact that the aqueous extracts of
stony corals causes polyp contraction, bleaching and tissue loss
in other stony corals within 24 hours, and that merely putting Galaxea
in a tank with Goniopora
can cause it to die within hours should put us at a new state of
awareness and alert. As with soft corals, it may be difficult to
say with certainty that coral species x will have a particular
effect on coral species y. As with other organisms, variability in
both production and effects on other species seems to be the norm.
However, and as I have stated frequently, it becomes a matter of
risk assessment. Soft corals known to be prolific producers of
toxins, or those known to have certain effects on certain species,
should be maintained in aquariums with careful consideration of
the potential consequences. It appears the same is true for stony
corals. In particular, Goniopora
is well recognized to produce toxins that are wide-ranging and
consistent in their effects on vertebrates and invertebrates.
Perhaps this is fortunate news, given the fact that they survive
so poorly in aquariums (Borneman 1997, Toonen 2001). Perhaps our
search for the methods to keep these corals alive should be
ameliorated or ended in light of their obvious toxic potency. Even
more, the continued death of these corals in tanks will certainly
result in the release of the total amount of toxins in the tissue
throughout the tank. Given the fact that a single colony possesses
enough toxins to kill hundreds of mice, this is no small matter of
concern for those who purchase these animals in unlikely hopes of
having such beautiful corals survive in their tank. Equally as
disturbing are the number of other stony corals that may have
similar, equal, or even more potent toxicity across various
assays. Not that this is really any great surprise to me, although
seeing it all spelled out in the aforementioned studies was
impressive. I noted in numerous places in Aquarium Corals (2001)
where I had observed what seemed to be allelopathic effects by
stony corals in my own aquariums – notable Echinophyllia,
Oxypora, and Pachyseris species. Similarly, reports of aquarists over the years
would lend further support of such effects in closed systems.
For
many years, noted authorities have suggested that keeping aquariums
with lots and lots of miniature species, eventually bound upon
survival to compete with each other in a small closed volume of
water, was asking for trouble. Now, more than ever, the effects of
such allelopathic competition, even in tanks that do not house
significantly large or numerous soft corals, is a very likely
occurrence for which a contingency plan should be devised prior to
the purchase of numerous, and especially highly toxic, species of
corals. I would also suggest that the use of activated carbon maybe
among the more effective ways of dealing with such secondary
compounds, as it has been found to be effective in the absorption of
similar compounds from terrestrial plants. Studies should also be
undertaken to determine the composition of protein skimmate to see
how efficient these devices are at affecting water concentrations of
the organic chemical soup that characterizes out indoor reefs.
Addendum
Terry Siegel kindly asked me
to expound on some of the material in the last two paragraphs of this
article.He notes quite correctly in an email to me that, "There
are many reef keepers, myself included, that have very dense coral
growth, and corals that I've had for more than 15 years. Why are we
able to get away with this?" Before proceeding, I would also note
that Siegel also wrote several excellent articles not too long ago
about "old tank syndrome," and has communicated to me
numerous times about losses of corals.
Like him, I think most of us
with long-term corals in our tanks might wonder about allelopathic
effects, and if they are significant.I would add that, while many of us may have dense coral growth
and may have many relatively "old" specimens in our tanks, I
feel safe saying this same period has been punctuated by many losses,
some of them without obvious explanation. What follows is largely
speculative on my part in terms of aquarium topics, but also based on
a fairly thorough review of literature on natural products, wastewater
treatment, and studies of allelopathy in both terrestrial and aquatic
environments.
With that,
I would like to further explain the nature of many of these
metabolites across taxa, not solely those of stony corals. A single
species may have from a few to over a hundred chemicals it produces,
some or many of which may have intentional or incidental allelopathic
actions. In some studies, there is always damage of species x on
species y.In some case,
damaging effects may also occur on species a and species c, but never
on species b.Thus, their
action on tank inhabitants may not be predictable, much less known for
certain as relatively few of these compounds have been tested
extensively for their action on all but a handful of other species. It
is not a requirement that the producer has effects on related species,
either.By example, a
coral metabolite might have an effect on echinoderms, but has never
been reported.By and
large, compounds produced by organisms to have an allelopathic role
tend to be geared towards organisms that compete with the producer,
and this means that related species are often the target - but not
always.
Furthermore,
in the scope of marine organisms, very few compounds have even been
isolated.Because a
species is known to produce a compound does not mean it doesn't
produce a dozen others that have not been isolated or identified. Not
all chemicals produces are released, and some are stored in the
tissues of organisms.In
these cases, the toxic effects may not be seen until partial or total
mortality of the organism occurs.This is perhaps well illustrated with sexual spawning in
Caulerpa or some corals when spawning results in massive tank
mortality. Allelopathy is, for lack of a better phrase, a "grab
bag" of chance in most situations.
Compounding
these variables are the various environmental factors that affect the
production of bioactive compounds.Some are produced seasonally, during reproduction, under
stress, under conditions of limiting nutrients, under conditions of
abundant resources, when the animal or plant is being grazed, when
directly involved in competition, etc. Thus, it is very hard to
predict the levels of production of even a species known to produce
toxic metabolites.It
could very well be that production remains low, and something as
relatively simple as a new addition or an injury or a new food causes
the animal to ramp up production of various compounds.
In the
interest of explaining why tank inhabitants don't keel over on a
regular basis from allelopathic organisms present in aquariums, it may
be that environmental conditions, including our deliberate avoidance
of predators of specimens we keep in tanks, or the stability of some
systems, limits their production. Also likely is a habituation
response, whereby either a tolerance to various compounds develops
among the other inhabitants, or where the producer habituates to the
presence of its co-inhabitants and no longer senses them as an
immediate "threat."I
am postulating here, for I do not know for certain what happens in all
the potential interactions, but am basing these thoughts on likely
scenarios that also occur in nature.
It may also
be possible that we are doing an adequate job of removing secondary
metabolites from the water. Many of the more toxic compounds studied
across terrestrial and marine systems occur in the polar aqueous
fractions of extracted tissues. This is not to say that nonpolar
compounds with deleterious effects do not exist, but that the majority
seems to be polar.As
such, they may be more likely to be removed by foam fractionation. In
reading literature dealing with allelopathy in both terrestrial and
marine systems, as well as copious literature and material from the
wastewater industry, it appears that a number of media sources can be
employed to remove secondary metabolites.The most commonly employed in scientific methods seems to be
activated carbon. While wastewater industry uses activated carbon,
they also employ activated clays such as bentonite. Papers in the
natural products literature tend to use more sophisticated devices,
but the equivalent of deionization cartridges may be useful.In other words, it might work to pump water through various
resins if they could be designed to benefit tanks.I am also aware of polymers that selectively absorb
compounds, and the aquarium product PolyFilter relies on this
technology. The polymers are not specifically designed primarily for
these chemicals, but rather those more commonly associated with tank
water chemistry issues.However, filters for classes of chemicals could probably be
designed and tests of PolyFilters seem to indicate that absorption of
similar organics is possible by the products. Obviously, water changes
would also be effective in removing levels of metabolites in
proportion to the volume of water exchanged.This is probably the simplest, easiest and perhaps most
effective way of dealing with such bioactive substances.
There
is no reason to suspect that allelopathy, and the simultaneous
production of many other compounds that may have other effects, is not
occurring in our tanks. Various effects may result, from reactions by
other organisms that range from acute toxicity, to a general
"failure to thrive," to no visible effects (even though
there may be very significant effects that are simply not visible to
the aquarist, such as changes in respiration or photosynthesis rates).There may also be cumulative effects, with low levels
produced increasing over time so that levels that initially had no
effects begin being expressed over time on various organisms, perhaps
in various ways. Such a progressive increase of metabolite
concentrations could help explain the "old tank syndrome"
Siegel mentioned in his articles, and although there are a host of
other potential explanations, the signs are consistent with what one
would expect from allelopathy. Finally, allelopathy may likely be a
part of the reason for relatively low levels of sexual reproduction
occurring in our aquariums, especially among corals.Once again, I have no reason to suspect that this is THE
reason, but studies would suggest it is at least possible if not
probable.The number of
observations by the reef aquarium community provides substantial
anecdotal evidence of such events occurring, but unfortunately only
become noticed when conditions in the tank are quite dramatically
affected.It is my
purpose here not to create widespread panic, or complacency, but to
make the aquarium community aware of the widespread occurrence of
marine organisms producing scores of bioactive compounds, and to
briefly describe the possible effects they produce. In summary, it is
my belief that our aquariums are under potentially significant
influence by such compounds, and further examination of the
effectiveness of methods that mitigate their effects should be a
priority.
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