The Role of Allelopathic Chemicals in the Spatial Patterning of Benthic Communities

ABSTRACT. Terrestrial, freshwater, and marine plants and animals are known to 
produce secondary metabolites which may act as chemical signals between 
interacting species. The role that chemistry plays in terrestrial ecosystems is 
better understood then its role in the ecological processes of marine 
ecosystems.  Sessile, marine organisms and terrestrial plants  have the similar 
pressures of competing for light, space, and essential macro and micronutrients 
leading to similar strategies for space acquisition and maintenance.   In order 
to compete for these resources, many plants have adopted strategies that involve 
the use of allelochemicals.  Allelochemicals are chemicals produced by an 
organism that inhibit the ability of another organism to share the same habitat.  
Many competitors pose a threat by settling near an established organism and 
growing and competing with it in the near future.  Allelochemicals are toxins 
that are effective against the potential sessile competitor.  Because this type 
of competition is shared by terrestrial plants and marine sessile organisms, 
defense mechanisms analogous to those in terrestrial ecosystems are expected in 
their marine counterparts, benthic communities.  Numerous new compounds have 
been isolated from marine organisms and there is evidence that these compounds 
may be part of the ordering mechanism for benthic assemblages. There is much 
evidence that the release of larvotoxic allelochemicals might be common to many 
colonial sessile invertebrates. These toxic chemicals have been found in 
Platygyra daedalea, Goniastrea favulus, Favia matthai, Pavona decussata, and 
Fungia fungites.  This paper will address the role of toxic compounds found in 
hermatypic corals which make up much of the coral reef environment. Whether 
these toxins affect the behavior, settlement, or survival of coral larvae or the 
rate of growth of recently metamorphosed coral spat will also be explored.  By 
exploring the role of allelochemicals insight will be gained into the spatial 
patterning of these benthic communities.

 INTRODUCTION

        The struggle for survival among organisms is often a brutal and fierce 
competition resulting in the death of one organism or even the extinction of 
many organisms.  Generally, when we think of this brutal struggle for survival a 
predator-prey relationship typically comes to mind.  We don't often think of 
this fierce interaction as involving deadly weapons, or as being played out by 
organisms that never even move. Ironically, the most brutal battle may not 
involve a predator-prey relationship at all, but may be a fiercely waged war 
between sessile organisms over the acquisition of space.  It is among sessile 
organisms that these battles are fought in the struggle for survival in highly 
competitive systems such as tropical ecosystems, and marine coral reefs. 

        Although, tropical ecosystems are dominated by plants, and in contrast 
to that, marine systems are dominated by animals (Endean and Cameron, 1983),  
both are similar in that many of the organisms competing for resources are 
sessile. Even with the hazard of predation, and viruses and bacteria, the 
greatest potential threat to sessile organisms is being settled on or overgrown 
(Cameron, 1974). Their most limiting factor is not food or predation, but space 
(Cameron, 1974, Endean and Cameron, 1983, Jackson and Buss, 1975, Benayahu and 
Loya, 1981). As a consequence,  some of the terrestrial plants and marine 
organisms have parallel mechanisms for spatial competition (Jackson and Buss, 
1974).  Some of these mechanisms for acquisition and holding of space are, 
overgrowth, extracoelentric feeding by corals, aggressive behavior among mobile 
animals, and allelopathy (Endean and Cameron, 1983).  

        It is well known that terrestrial, freshwater, and marine, plants and 
animals, produce secondary metabolites which can act as chemical signals between 
interacting species (Maida et. al, 1995).   It is these chemical signals that 
are the deadly weapons in the war for space among sessile organisms.  These 
signals can be either inhibitory or stimulatory.  It is through inhibitory 
chemicals that earlier residents can make the physical environment more or less 
favorable for later arrivals (Breitburg, 1985).  In sessile organisms, 
competitors pose a threat just by settling near an established organism and 
growing and competing with it in the near future (Fearon and Cameron, 1997). In 
the highly competitive environment of a coral reef,  it is an advantage to have 
toxins that are effective against potential sessile competitors.  Such toxins 
are known as allelochemicals, and inhibit the ability of another organism to 
share the same habitat (Fearon and Cameron, 1997).  They have been referred to 
as "the ordering mechanism of benthic assemblages" (Fearon and Cameron, 1997). 

        Sessile organisms and plants may have similar pressures which determine 
the evolution of toxic compounds causing inhibition of growth of sessile 
competitors (Becerro, 1995).  Recently, there has been an increasing interest in 
understanding the ecological role of the toxins found in marine ecosystems 
(Becerro, 1995). Although, we have a better understanding of the role that 
chemistry plays in terrestrial chemical ecology, defense mechanisms analogous to 
those in terrestrial environments are expected in their marine counterparts 
(Becerro, 1995).  So far this has been found to be true.  As a matter of fact, 
according to Endean and Cameron (1983), there are more toxic species in the 
coral reef system then in any other system.  Martin and Uriz (1993) looked for 
antimitotic and cytotoxic activities in extracts from 32 species of benthic 
organisms and found that only 12 were not active.  Some examples of highly toxic 
marine organisms are the crown of thorns, Acanthaster planci, the stonefish, 
genus Synanceia, the mollusc, Canus geographus, and the crab, Zosimus aeneus 
(Endean and Cameron, 1983).  Reasons for the high incidence of toxicity in coral 
reef systems may be the great species richness, an abundance of stationary 
animals, and colonial organisms (Endean and Cameron, 1983). Typically, chemical 
defenses are found in organisms that don't have other means of defense such as 
the ability to escape.  Toxicity is correlated with sessile or slow moving 
habitat in coral reef organisms (Bakus, 1981).  This paper will explore the role 
of allelochemicals among sessile organisms in the fierce battle for the 
acquisition of space in the coral reef environment.  

DISCUSSION

        Different strategies for space acquisition and maintenance influence 
spatial patterning (Becerro, 1995),  spatial heterogeneity (Cameron, 1974), as 
well as diversity (Bakus, 1986).  Marine organisms competing for space may 
crowd, undercut, crush, digest, overshadow, overgrow, or poison their neighbors 
(Bakus, 1986).  Soft corals actually leave trails moving over hard corals and 
killing them (Bakus, 1986). The first demonstrated release of an allelochemical 
from a marine organism was from an Australian soft coral (Coll et al, 1982a).  
Because so many marine organisms posses toxins, this paper will focus only on 
the corals themselves and their role in the chemical ecology of the coral reef.  

Settlement

        Corals spawn seasonally (Harrison et. al, 1983), and the life cycle of 
corals includes a planktonic larval phase that can last anywhere from minutes to 
months (Pawlik, 1992).  That means that some larvae may travel for only meters 
while others may travel for hundreds of kilometers.  There are two kinds of 
larvae.  Planktotrophic larvae feed and have long developmental periods. In 
contrast, lecithotrophic larvae do not feed and only last for a short period of 
time (Pawlik, 1992).  According to Pawlik (1992), eighty percent of marine 
invertebrates produce larvae that develop while in the plankton, making most 
marine invertebrates planktotrophic.  Settlement is a general term which refers 
to the entire transition from planktonic larvae to benthic juvenile.  The 
metamorphosis from larvae to juvenile is included as a part of settlement.  Due 
to the intense competition for space in marine ecosystems, the location in which 
the larvae choose to settle is extremely important.  Failure of larvae to locate 
food or other resources results in death, and larvae should avoid settling in 
hostile, highly competitive areas (Young and Chia, 1981). Previously it was 
thought that settlement occurred at random, but evidence that marine organisms 
choose where they settle was proposed by Grosberg in 1981.  He observed that 
barnacles settle in gregarious settlements which insure cross-fertilization, 
predators settle near their prey source and parasites near their host, bryozoans 
and polychaetes settle near algae insuring survival for their young, and some 
arborescent bryozoans also settle gregariously enhancing their interspecific 
competitive ability. Young and Chia (1981) demonstrated that an avoidance 
response to settling in certain areas may be an important part of the strategy 
for survival among sessile organisms involved in spatial competition.

        The settlement process of planktonic larvae is influenced by many 
environmental factors. Davis et al (1991) actually followed larvae using SCUBA 
in order to observe their settlement behavior.  Most larvae was found to settle 
on their first encounter with the substratum (63%), and 6.7% of the larvae made 
ten or more contacts before settling.   Some of the physical factors influencing 
larval settlement may include light, gravity, hydrostatic pressure, temperature, 
and salinity (Pawlik, 1992). Properties of the substratum such as, contour, 
texture, and temperature may also be involved (Pawlik, 1992).  Also a 
prerequisite for larval settlement is a surface film of microorganisms (Pawlik, 
1992).  Along with these physical cues are chemical cues which may induce or 
inhibit  larval settlement.   In only a few species have the inducers been 
identified (Pawlik, 1992), and this paper will focus on the inhibitory 
allelochemicals.   

Evidence for allelochemicals

        Toxins are biological products inimical to organisms other then those 
that produce them, and any discussion of toxins needs to include some component 
of a biological interaction (Cameron, 1974).  The chief reef building, or 
hermatypic corals are scleractinian corals (Fearon and Cameron, 1997). 
Bioactivity in scleractinian corals was first reported by Hashimoto and Ashida 
in 1973 (Gunthorpe and Cameron, 1990b).  Larvotoxins have been demonstrated in 
species of hermatypic corals from the families Favidae, Fungiidae, Agariciidae, 
Portidae, and Dendrophylliidae (Fearon and Cameron, 1997). An example of the 
bioactivity of scleractinian coral is a study by Gunthorpe and Cameron (1990a).  
They found that among the Scleractinians 71% of 58 species tested were toxic to 
mice, 86% of 57 species tested had hemolytic activity, 45% of the 55 species 
tested possessed antimicrobial activity, and 9% of 45 species were ichthyotoxic 
(Gunthorpe and Cameron, 1990a).  The role of these larvotoxins may be to affect 
the settlement and recruitment of potential competitors (Fearon and Cameron, 
1997).  Invertebrate larvae may recognize established competitive species and 
avoid settlement in their area (Pawlik, 1992), or the allelochemical may kill 
the larvae of potential competitors after settlement. 

        Fearon and Cameron (1996 and 1997) tested whether toxins possessed by 
hard corals affect the behavior, settlement, or survival of coral larvae. They 
also tested the rate of growth of recently metamorphosed coral spat.  Coral spat 
is metamorphosed planulae.  They found that the rate of metamorphosis of the 
coral larvae Pocillopora damicornis in the presence of coral extracts from 
Goniopora tenuidens was significantly lower then the controls.  They also found 
two incidences of demetamorphosis (the settled spat reverted to a motile 
planula-like form).  After two days all of the spat that had been exposed to the 
coral extract had died, and their mean diameter was significantly decreased.  At 
the lowest concentration of the extract used (3.9 mg per litter) the larvae 
showed the sublethal effect of behavioral modification.  The change to their 
behavior included contractions along their long axis making them disk shaped, 
and affecting their swimming coordination. Gunthorpe and Cameron (1990a) also 
made behavioral observations.  They observed that corals react to toxins with a 
sustained contraction of polyps, increased mucus protection, lose of tissue 
coloration, and loss of tissue from skeletal matrix.  So, extracts form coral 
affected coral larvae in a variety of ways. At low concentrations it affected 
the behavior, reducing coordination and causing demetamorphosis.  At higher 
levels it significantly decreased growth and eventually proved lethal to larvae.  
not these toxins are being released in the natural environment of the coral 
reef.  Although these hard corals clearly contain toxins, the question remains 
whether or not these toxins are being released in their natural environment.  As 
pointed out by Jackson and Buss (1975), toxins may just be stored inside the 
organism and not release into the environment at all.  

Allelochemicals in the natural environment

        Much of the research done with coral in its natural environment involves 
the highly toxic soft corals and their effect on hard corals. Sammarco et al 
(1983),  observed sixty-six different areas where alcyonocean and scleractinian 
corals occurred in close proximity to one another. They found that in seventeen 
percent of the observed cases, necrosis of tissues was observed in scleractinian 
coral in the immediate vicinity of the soft coral that was in the reef area.  
Fifty-two percent of the observed cases showed the sub lethal effects of growth 
inhibition or stunting. 

        Sammarco et al (1983) also found that the response of hard corals to 
soft corals was highly species specific by relocating soft corals into areas 
already occupied by hard corals. Lobophytum pauciflorum was found to cause 
necrosis in Porites andrewsi in contact and non-contact situations, Lobophytum 
was also found to be lethal in contact situations to Pavona cactus but had no 
effect without contact.  Xenia caused necrosis in hard coral when in contact, 
but had no effect otherwise.  Sinularia pavida was lethal when in contact with 
Porites.   

        Maida et al (1995a, 1995b) observed that some soft corals can depress 
local recruitment of scleractinian coral spat in their vicinity depending on the 
direction of prevailing microcurrents.  They found that the alcyonacean 
ocotocoral, Sinularia flexibilis , had a directional inhibitory effect on coral 
recruitment. The lowest level of recruitment of scleractinian corals was found 
down current from the soft coral, Sinularia flexibilis.   Hard corals tested did 
not have this inhibitory effect.  Whether the coral larvae sensed the 
allelochemicals from Sinularia flexibilis  and avoided the area, settled and 
then rejected the substratum, or settled and then died before secreting a 
calcium carbonate skeleton, is not clear.  Maida et al (1995a, and 1995b) came 
to these four conclusions as a result of their studies.  Soft corals 
(Alcyonacea) can be effective competitors for space against scleractinian corals 
by causing localized mortality in the latter.  Mortality can be caused by direct 
contact or through the water from a distance (allelopathic exudates).  
Competitive abilities vary in a species-specific manner.  And, susceptibility of 
scleractinian corals also varies in a species-specific manner.

Chemicals

        In many of the studies involving these marine toxins, the specific 
chemical or chemicals involved are not yet known.  Most of these studies were 
performed using crude extracts from corals to be sure to include any synergistic 
effects that might be involved (Martin and Uriz, 1993, and Fearon and Cameron, 
1997).  An example of synergism between toxins of different species was found to 
occur in toxic extracts of the green sponge, Halidona viridis and a toxin  from 
the holothurian, Actinopyga bahamousis (Endean and Cameron, 1983).  The toxicity 
of the two together is greater then either one alone.   It is possible that 
different components of the individual coral extract may be working 
synergistically in a similar manner.  The secondary metabolites that are 
involved in plant defenses in terrestrial ecosystems, such as, terpenes, 
alkoloids, steroids, carotenoids, and phenolics are expected to also be involved 
in marine defenses.  The diterpenes flexiblide, dihydroflexibiled, and 
sinularide were found to be secondary metabolites in the algonacean soft coral, 
Sinularia flexiblis (Maida et al. 1993). The terpenoids were extracted from 
freeze dried coral in dichloromethane (DCM).  They were then chromatographed on 
a small silica gel column and eluted with a mixture of acetonitrile-DCM (3:2, 1 
ml each). The fraction was then compared between samples by HNMR spectroscopy. 
Maida et al. (1993) found, isolated, and demonstrated that these terpenoids have 
an inhibitory effect on coral recruitment.

        Earlier work by Coll et al. (1982a) also isolated flexibilide and 
dihydroflexibilide, as well as the terpenes, Sarcophine and Sarcophytoxide from 
the sea water around the two soft corals, Sinularia flexibilis, and Sarcophyton 
crassocaule demonstrating that these compounds are being released into the 
water.  Along with these terpenes, lipids and sterols were also isolated from 
the sea water surrounding soft corals.  None of these are very water soluble, so 
it has been hypothesized that the ability to pass into water may be due to the 
accompanying release of mucus by the organism (Coll et al. 1982a).  Further 
evidence for terpenoids as allelochemicals comes from the fact that they are 
known to inhibit the growth of cultures of marine, unicellular algae (Bak and 
Borsboom, 1984).  Terpenoid compounds have been isolated from algae, sponges, 
coelenterates, molluscs, and echinoderms (Bakus et al. 1986).   

Evolution

        Toxic compounds in sessile organisms may have evolved as part of a 
strategy of stationariness (Cameron, 1974).  According to Bakus (1981), the 
ultimate causal mechanism of toxicity in tropical organisms is most frequently 
considered to be natural selection under high intensity fish predation. Much 
evidence supports the idea that these toxic compounds in soft corals serve both 
in antipredation and competition for space (Bakus, 1986).   Based on analogies 
with terrestrial systems one would expect to find variation in quality and 
quantity of allelochemicals in response to changes in the environment or 
shifting selective pressures (Feeny, 1976).   Bakus (1981) found that a higher 
incidence of toxicity occurs in species where fish predation and grazing are 
more intense, and that coral reef sponges, soft corals, or ascidians that lack 
allelochemicals have a hardened body or secrete huge amounts of mucus (Bakus et 
al. 1986).  These mechanical defenses may eliminate the need for chemical 
defenses against predation.                   Beccero (1995)  found evidence for 
quantitative differences in toxicity with variation related to size and habitat.  
The sponge Crambe crambe was found to have more toxicity when living in shaded 
areas where competition for space was higher.  Its levels of toxicity were lower 
in areas where there was a high turnover of bare patches of substratum.  Small 
and large sponges were found to have lower levels of toxicity then medium size 
sponges.  Small sponges may be investing more into somatic growth and space 
acquisition, while larger sponges may be investing in reproduction (Beccero, 
1995).  This example of variation of toxicity in the sponge parrallels what is 
known about terrestrial plants and their use of chemical defenses.  Continued 
study in this area may shed more light on the process of evolution of chemical 
defenses in sessile organisms.   

CONCLUSION

        Although many studies of toxins have been performed using crude extracts 
from coral, much more needs to be studied in the natural environment of the 
coral reef.   Because a certain type of coral has a toxic chemical does not 
necessarily mean that it is releasing this chemical into the water or that this 
chemical  is involved in allelopathy.  More studies need to follow in the 
footsteps of Maida et al, (1995a, 1995b), Sammarco et al, (1983), and Coll et 
al, (1982a), who performed carefully designed experiments in the natural 
environment.  It is difficult to determine if bioactive substances are exuded 
under natural conditions (Fearon and Cameron, 1996), but knowing more about 
these allelochemicals has far reaching implications for the determination of the 
community structure of corals.  Even if exudates are not lethal, they may limit 
growth or physiology which gives the established colony an advantage (Fearon and 
Cameron, 1997).  The ability to detect and avoid exudates which may later be 
lethal after chronic, long term exposure is an advantage to the larvae (Fearon 
and Cameron, 1997).  Variation in the susceptibility of larvae to coral extracts 
could contribute to the complexity on the ordering of coral assemblages (Fearon 
and Cameron, 1996).  There is also a need for research into the larval stage of 
coral development.  At this time, it is not known how the larvae respond to 
their environment.   Not much is known about the chemosensory organs and 
receptors of invertebrate larvae (Pawlik, 1992).  Before electrophysiological 
techniques can be applied to the task of exprloring the organs and receptors of 
invertebrate larvae, the chemical signals that cause responses in larvae need to 
be identified (Pawlik, 1992).  More of the chemicals involved in inducing or 
inhibiting larval settlement need to be isolated and identified.

        Well over 2000 natural products have been described from marine 
organisms (Faulkner, 1991), and many more are being added to that list all the 
time.  Although some of the chemicals involved in the allelopathic interactions 
of these marine organism are known, many more still need to be isolated.  Davis 
et al. (1989) points out that many questions still need to be answered.  Some of 
the questions he poses are, where are these compounds stored, how are they 
stored and released without hurting the host organism, what controls the 
production and release of these compounds, and how costly are they for the 
organism producing them? The  more we know about the chemicals involved, the 
responses of larval settlement, and the evolutionary mechanisms behind these 
interactions, the more we will know about the structure and organization of 
these benthic communities.  The existence of species-specific mechanisms of 
allelopathy may provide a basis for the maintenance of diversity in space-
limiting systems without a predator, or a physical disturbance (Jackson and 
Buss, 1975).  The battle over space, involving allelochemicals may be a built in 
mechanism to maintain diversity in marine ecosystems.  Understanding these 
interactions will provide invaluable insight into the workings of marine 
ecosystems. 

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