Chapter 6.
Conclusions and Hypotheses, and a project endorsed by GEOHAB, for future research.
Ciguatera benthic dinoflagellate related species, general conclusions
The study “Ciguatera in the Pacific islands, 1998 to 2008” highlights the need for more research to
be undertaken in this field and from the rest of this research presented here, the following is
highlighted as to the many questions which remain unanswered about ciguatera and its place in the
health of coral reef ecosystems. I have no doubt that ciguatera should be seen as a biomarker of
coral reef degradation. Amongst the three major hypotheses presented here which could amount to
solving such questions as why ciguatera has come about and why it should be seen as a modern
day “neglected” disease, I also present a new GEOHAB endorsed project which with funding could
be used to answer many of the questions that scientists should be researching in this field.
Studies of ciguatera dinoflagellate ecology have focused on the genera Gambierdiscus, but to
undertand what is happening at the macroalgae interface this research points out the dynamic
interplay that exists between up to four genera. At inshore and mid lagoon sites of the GBR (eg
Magnetic Island and Green Island), and at sites in Bali and Gili Trawangan, suggested System II
(Tindall & Morton 1998)
Prorocentrum and Ostreopsis were found to be the dominant
dinoflagellates with occasional localized blooms of Ostreopsis occurring. There were many
situations where Prorocentrum abundance was correlated with the DIN of the water column. At Muri
lagoon on Rarotonga, suggested System III, due to obvious high retention rates, a large bloom of
Prorocentrum and blooms of the cyanobacteria Lyngbya (personal observations) were occurring.
Again the Prorocentrum that was growing on the substrate correlated with the DIN from the pore
water of the substrate. The same eutrophication that no doubt has supported the coral reef to
macroalgal phase shift also supports the abundance of this genus. However at outer GBR sites (i.e.
Norman reef) a system I, Gambierdiscus was the dominant dinoflagellate. Here in some cases
there were correlations between Gambierdiscus and the ammonia (from the DIN) of the water
column. This correlation has also been observed by other scientists under laboratory conditions.
Perhaps the Gambierdiscus abundance at the initial stage of the phase shift could be in proportion
to the amount of fish present.
There appears to be several stages in the succession/phase shift of coral to macroalgal reef in
terms of dinoflagellate abundance, firstly the stage where macroalgae are increasing and fish are
still abundant and Gambierdiscus abundance dominates (i.e. Norman reef), we can call this type 1.
Secondly, as ciguatoxins have impacted on the fecundity of fishes and fish biomass falls, a
decrease in Gambierdiscus may occur with increases in either Prorocentrum and/or Ostreopsis
following, as eutrophication takes place. In some cases it would appear that Prorocentrum can be
dominant (type 2) before Ostreopsis, (type 3), as seen at Green Island as opposed to the reefs at
Bali or Magnetic Island. This type 3 phase shift can include the toxins from all three genera
sublethally impacting on the biodiversity of the coral reef. To include the presence of cyanobacteria
(such as Lyngba) and related toxins, who have the potential to also dominate over the macroalgae,
and hence the endpoint in coral reef degradation can occur, where blooms of toxic dinoflagellates
and cyanobacteria dominate. As found by personnel observations at the Muri lagoon field site.
Ciguatera is an ongoing problem on Rarotonga from the original “hotspot” of blooms of
Gambierdiscus and ciguatoxic fish, which occurred in Muri lagoon, and now can be found on the
other side of the island, to the dominance of sand dwelling toxic Prorocentrum and Lyngbya that
can poison other organisms that are outside the Gambierdiscus food chain. This research also
indicates that inshore reefs of the GBR have reached the type 3 stage, with some mid lagoon sites
(i.e. Upolu reef) type 2. The type 3 stage, that dominance of Prorocentrum/ Ostreopsis/
cyanobacterial blooms that can also impact on macroalgal biomass, as seen at Muri lagoon, will no
doubt as the eutrophication continues, become more apparent at the inshore reefs of the GBR,
such as at Normanby reef.
The research that does exist on the causative species of CFP has been heavily weighted towards
the physical factors impacting on the benthic ciguatera dinoflagellates and there now needs to be
research that could discover what interactions exist between the ciguatera dinoflagellates and their
biotic factors. The justification for this is to move towards a better understanding of the role toxic
benthic HABs have on the health of the coral reef ecosystem and to work towards the management
of CFP. The research undertaken in this thesis has lead to the need for clarification of what biotic
factors of benthic toxic HABs need to be addressed, the further research could include,
the
following, although not exhaustive, but be used as a starting point:
Ciguatera Ecological Hypotheses to be looked at for future research.
Biotic factors between dinoflagellates:
Is Ostreopsis a predator of either/and Prorocentrum or Gambierdiscus or vice versa and are
toxins obtained from within or from their prey? Are there any allelopathic impacts from one of
Prorocentrum, Ostreopsis and Gambierdiscus, towards one of the others? Is there any
commensalisms benefiting those not producing allelopathy from the others that do? Is there
competition for space between Prorocentrum, Ostreopsis & Gambierdiscus?
Biotic factors between Corals & benthic HABs:
Do ciguatera dinoflagellates compete with the settlement of coral larvae? What are the impacts
of the dinoflagellate toxins on coral polyps by either absorption or by filter feeding? Do benthic
HABs promote coral bleaching?
Biotic factors between Invertebrates & benthic HABs:
Which invertebrate organisms are feeding directly on these dinoflagellates on the macroalgal
surface niche and which are impacted by their phycotoxins and which are not? What
invertebrates are responsible for the phycotoxins to be moving through the food chain and
which are capable of depurating and preventing bioaccumulation? Do the phycotoxins promote
trophic cascades?
Biotic factors between Bacteria & benthic HABs:
What is the role of bacteria in the toxicity of these dinoflagellates and what role could the
bacteria from sewerage waste (i.e. E. coli) be playing; are they a source of nutrition and/or toxin
production?
Biotic factors between Seagrass & benthic HABs:
Does the absence of seagrass benefit the blooms of these benthic dinoflagellates? Where
seagrass is present are more nutrients removed from the water column and therefore less to be
used by the microalgae? Does Gambierdiscus (golden brown in colour) use seagrass as a
host? Does Gambierdiscus avoid sea grass and green algae, when brown and red algae are
available as it is more conspicuous and less likely to be predated upon, where as on seagrass
and green algae it is not conspicuous and so is more easily predated upon, without camouflage,
by fish?
Biotic factors between Fish & benthic HABs:
Do Gambierdiscus or/and Ostreopsis proliferate better in the localized presence of fish and their
waste urea (and hence ammonia)?
If Prorocentrum are affected by the presence of fish and their waste (urea and ammonia) are
they unable to proliferate in waters where there is a high fish biomass?
And more generally:
Do
Gambierdiscus
cope
with
poorer
water
quality
(i.e.
greater
turbidity)
or
are
Prorocentrum/Ostreopsis better able to cope with it?
How does the presence of anthropogenic toxic chemicals such as pesticides in the water
column impact on the toxic dinoflagellate abundance and do they influence trophic cascades
that could allow benthic HABs to proliferate?
This research has led to consider three main hypotheses concerning the phase shift of coral reefs
to macroalgal reefs and the role of toxic benthic HABs, which can cause CFP.
1. Hypothesis, Impact of toxic dinoflagellates on coral reef ecosystems; the unseen influence
responsible for coral reef degradation?!
Hypotheses have been put forward as to the reasons for the toxicity of benthic epiphytic
dinoflagellates. In terms of evolutionary ecology it would make sense for an epiphytic organism to
protect its host, in this case macroalgae (or turf algae) from herbivory. Toxic dinoflagellates, like
their hosts, are at the bottom of every food chain that they are associated with when a coral reef
becomes degraded for a variety of reasons and macroalgae become more dominant. Whether it be
natural succession to algal dominated reefs due to disturbances from cyclonic weather conditions,
natural predation (i.e. crown of thorns) or from anthropogenic causes, from climate change,
eutrophication or any combination of influences, may initiate coral reef degradation.
The succession/decline of a coral reef to one that is algal (or even more advanced cyanobacterial)
dominated is furthered by dinoflagellates, whose toxins are capable of sublethal impacts(such as
fecundity) on any of the food web communities that would normally be found on a healthy coral reef.
Those toxins could be responsible, through a variety of sublethal impacts, for the potential decline
of any organism in a coral reef ecosystem subject to degradation. Hence the coral reef succession
to algal domination is reinforced by dinoflagellate toxins and as a result the coral reef community’s
biodiversity, may be rapidly lost and one output more easily recognised is further ciguatera fish
poisoning outbreaks.
Study has been done on the various toxins that have impacted on mans use of seafood from
ciguatera to the types of shellfish poisoning (e.g. DSP, ASP, NSP) in terms of identification and its
sources. Many of the toxin sources, those genera of toxic dinoflagellates, including Prorocentrum,
Gambierdiscus, Ostreopsis, and Pseudonitzschia etc are found in macroalgal samples, from this
research alone, from degrading coral reefs of the Cook Islands, Indonesia and the GBR and they
have a global tropical distribution. Whilst research has leaned towards mitigating the impacts on
human health it is now time to look into the role of these toxins in coral reef ecosystem health and
management. The conservation of coral reef ecosystems is of the highest importance and we do
need to take on board research which will look into the hypothesis presented here as it may be the
key as to why coral reefs may decline in such rapid circumstances. It may take less than a decade
for a coral reef to be altered and any reversal to its original condition, let alone its initial degradation,
may very well be dependent upon the presence of dinoflagellate toxins.
2. The Eutrophication-benthic HAB-Zooplankton Biocontrol hypothesis, and nutrient thresholds.
HAB describes a bloom of phytoplankton (autotrophic, mixotrophic or heterotrophic) species that
occur in consequence of injurious activity against other members of the ecosystem, and bloom
refers to an increase in biomass relative to background levels for that species (Flynn 2008). The
Eutrophication-HAB hypothesis can be defined as: anthropogenic nutrients and other chemical
products fluxing into coastal waters are disrupting the chemical ecology of these systems which
induces a restructuring of phytoplankton assemblages and can lead to the emergence of HABs
(Smayda 2008). Increasing linkages between nutrient loading and coastal marine HABs have more
recently been recognised (Heisler et al 2008). The evidence for eutrophication is unambiguous and
direct; coastal waters globally, are becoming enriched with anthropogenic nutrients (Smayda 2008).
A statistical correlation may not establish a causal link in the HAB-eutrophication hypothesis but the
relationship suggests that coastal eutrophication may be a causative agent of change (Heisler et al
2008). So many studies showing a relationship, when other factors (either biological, chemical or
physical) are taken into account, as they modulate a HAB response to nutrient loadings (Heisler et
al 2008), that the Eutrophication-HAB “hypothesis” should be formally recognised as a theory.
Nutrient thresholds, depending upon the type of ecosystem, should also be employed to determine
when the nutrophication is sufficient, to establish changes in the phytoplankton assemblage and to
create HABs.
Coral reef ecosystems have nutrient threshold concentrations set by the eutrophication threshold
model, where eutrophication refers to situations where nutrient enrichment increased macroalgal
growth rates to the extent that changes in the benthic community(coral to macroalgae phase shift)
structure begins. The large changes in macroalgae growth rates upon coral reefs can be caused by
very small variations in nutrient concentrations, around the nutrient threshold concentrations (Bell et
al 2007). These same thresholds should be used for epiphytic (benthic) ciguatera related HABs, in
coral reef ecosystems, due to their close mutualistic association with the macroalgae. When one
considers the potential of toxic (ciguatera related) benthic HABs to impact on the “top down”
herbivory trophic level, by way of toxins impacting sub lethally upon physiological functioning (like
fecundity of fishes), the greater the impact of the ‘bottom-up” eutrophication on the coral to
macroalgal phase shift, as herbivory of macroalgae falls. Over time less palatable macroalgae,
(combined with their epiphytic microalgae) tend to dominate inshore eutrophic reefs (Bell et al
2007).
A second phase shift needs to be considered in semi-enclosed water bodies (such as island
fringing reef lagoons, system II & III) with long retention times, and that is a further shift from
macroalgal reefs to HAB reefs, where toxic cyanobacteria, dinoflagellates and diatoms, can induce
conditions through ecotoxicological interactions, that establish a dominating influence over the
ecosystem, for their own survival. Chronic or episodic exogenous nutrients are often necessary for
such high biomass HABs to be sustained or they can be sustained on nutrients that are
regenerated and recycled (Heisler et al 2008).
Temperate estuarine studies have suggested that the biomass of phytoplankton and of copepods,
but not microzooplankton, was significantly higher in eutrophic conditions so that top-down control
of microzooplankton by copepods can cause a trophic cascade, which partially releases smaller cell
size phytoplankton from control by grazing (Stoecker et al 2008). This removal of the
microzooplankton may be initiated by a variety of factors, and not just overgrazing by larger
copepods, including the impact of pesticides in the same water body, that is subjected to
eutrophication. If such a temperate estuarine study is relative to tropical benthic localities, then
without the presence of the benthic zooplankton, some of which may even have had the ability to
depurate any toxins absorbed, then the toxins in bypassing a trophic level, are bioaccumulated and
consequently organisms are poisoned further up the food chains, (hence ciguatera fish poisoning).
This could further explain how some reefs along side others are known to carry ciguatoxic fish,
whilst the other reefs which could have their “good” populations of benthic zooplankton intact,
capable of depurating the toxins, and removing the sub sequential bioaccumulation, carry fish which
are non ciguatoxic. In the terrestrial environment we are apt to use biological controls in order to
reduce populations of pests. Shouldn’t we consider a ciguatera HAB (Gambierdiscus) to be a pest,
and if so, if we were to find a benthic zooplankton capable of depurating the HAB toxin in question,
then shouldn’t we then use that benthic zooplankton as a biological control to render the HAB
redundant?
Once established that such a situation existed under laboratory mesocosm conditions and following
the strict criteria established for the use of biological controls, the successful zooplankton could be
aqua cultured (many island groups have facilities for culturing shellfish and fish) and trials releasing
it into the natural environment, could be established in ciguatera “hot spot” smaller semi enclosed
fringing reef lagoons, to gauge their ability to control a HAB. This may be more viable than weeding
a reef of the host macroalgae or indeed preventing sources of chronic nutrification. Restoring the
imbalance of the trophic cascade related to the HAB, by using a biological control may be an
effective management tool for the control of ciguatera. Not only may we find a solution to ciguatera
but we may also restore the imbalance in ecosystem health and allow for the more immediate
reversal from a macroalgal reef back to one that is coral dominated. For removal of the
bioaccumulated toxins may create greater herbivory. We could call this the Eutrophication-HABZooplankton Biocontrol hypothesis (E-HAB-ZooB?). Needless to say an integrated management
tool would require the removal of cultural eutrophication to ensure the balance of the ecosystem
remains and the HAB does not return. It is now time for the few ecologists working on benthic HABs
to look not just at the abundance of the HAB itself in their samples but to see what invertebrate HAB
predators are present and correlate the two.
Another successful scenario (as witnessed at Gili Trawangan), is to reverse the succession from
coral to macroalgal reef by providing fresh substrate for the growth of corals (coral rehabilitation
with metallic structures carrying low current), which in turn gives the chance for fish biomass to
increase, thereby increasing the herbivory on the macroalgae.
References:
Bell P.R.F., Lapointe B.E., Elmetri I. 2007. Reevaluation of ENCORE: Support for the
Eutrophication Threshold Model for Coral Reefs. 36, 416-424.
Flynn K.J. 2008. Attack is not the best form of defense: Lessons from harmful algal bloom
dynamics. Harmful Algae 8, 129-139.
Heisler J. , Glibert P.M., Burkholder J.M., Anderson D.M., Cochlan W., Dennison W.C., Dortch Q.,
Gobler C.J., Heil C.A., Humphries E., Lewitus A., Magnien R., Marshall H.G., Sellner K., Stockwell
D.A., Stoecker D.K., Suddleson M. 2008. Eutrophication and harmful algal blooms: A scientific
consensus. Harmful Algae 8, 3-13.
Smayda T.J. 2008. Complexity in the eutrophication-harmful algal bloom relationship, with comment
on the importance of grazing. Harmful Algae 8, 140-151.
Stoecker D.K., Thessen A.E., Gustafson D.E. 2008. Windows of opportunity for dinoflagellate
blooms: Reduced microzooplankton net growth coupled to eutrophication. Harmful Algae 8, 158166.
3. The cause of “modern day” Ciguatera, a discourse on the hypothesis: “that anthropogenic
radiation mutations, due to atomic weapons testing, upon coral reef inhabiting dinoflagellates and
their bio invasive nature, together with the coral reef to macroalgal phase shift, are responsible for
the occurrence of the “new age” of Ciguatera fish poisoning in Oceanica.”
Hypothesis brief: That the atomic weapons testing that occurred on Pacific Islands, was
predominantly responsible for Ciguatera fish poisoning (CFP), as the principal organism (genus
Gambierdiscus) that produces the ciguatoxin, mutated to a more toxic strain/species on any one of
those islands, where the radiation blasts occurred, and has bio invaded nations of the Pacific
Ocean region, traveling predominantly by boat ballast transfer and shipwrecks.
Hypothesis detailed: That the American, French and British atomic weapons testing (220 tests
across 6 islands in the Marshall Islands, French Polynesia and Kiribati and many naval bases on
and surrounding these) that occurred, since world war II, has been responsible for the “new age” of
Ciguatera fish poisoning as the principal dinoflagellate (Gambierdiscus) that produces the
responsible ciguatoxin, had mutated to a more toxic “super” strain/species from the radiation blasts.
And that the activities associated with such testing, assisting changes from coral reef to
macroalgal(phase shift) substrates due to harbor infrastructures and port facilities and
eutrophication from an increased anthropogenic source, had also provided conditions for the HABs
(both macroalgal with associated epiphytic toxic dinoflagellates) to occur, enabling such a mutated
“super” toxic dinoflagellate to bloom.
The ability of the mutated toxic super species of Gambierdiscus to survive in boat ballast together
with ship wrecks, shipping movements and the proliferation of structures associated with shipping
installations, has permitted the spread of CFP throughout Oceanica. Approximately one in four
native inhabitants of the Pacific Island nations, over the past 40 years has had CFP.
Can the following ideas support this hypothesis?
Genetics vs. Environmental.
•
Personnel communication with Professor Takeshi Yasumoto: who believes that genetic
factors are more prominent than environmental, that plays a major role in Gambierdiscus
toxicity; if genetics plays a major role then perhaps a mutated gene for higher toxicity could
be responsible for a “super” strain/species.
•
Personnel communication with Professor Michael Holmes: who believes that a “super” strain
of Gambierdiscus is responsible for CFP; could this “super” strain be derived from a radiated
source associated with atomic weapons testing?
•
Through the work of Dr Mirielle Chinain we now know that one species, that she has
described, G. polynesnsis is more (“super”) toxic than the other species. This species is not
found in the Caribbean. But may now appear dominant in more regions due to
biogeographical range extensions as it is now found in Indonesia, Malaysia and the Great
Barrier Reef of Australia.
•
Personnel communication with Professor Richard Lewis who had realized that we have toxic
and non toxic blooming strains of Gambierdiscus, could those toxic blooms be derived from
a species that originated from a radiated source and the others from natural sources?
•
It is generally known that reefs may be patchy and have random sources of ciguatoxin and it
may be random as to where a bio-invasive “radiated/super” species may end up, and
become more dominant in a habitat?
•
The “environmental” coral reef phase shift to macroalgal reef, which supports the toxic
dinoflagellates, due to a variety of causes, co-incident with a super toxic strain/species of
dinoflagellate is the cause behind CFP.
•
The potential of toxic (ciguatera related) benthic HABs to impact on the “top down” herbivory
trophic level, by way of toxins impacting sub lethally upon physiological functioning (like
fecundity of fishes), can re-enforce the coral to macroalgal phase shift as herbivory would
decline in the HAB presence.
Bioinvasive.
•
Personnel communication with Professor Gustaaf Halegraaf who has found that
Gambierdiscus amongst other dinoflagellates, can be transported in boat ballast; it is
possible then that a more toxic species generated from a radiated/atomic weapons testing
source could have first traveled by naval vessels to other ports and hence further a field?
•
Ciguatera in French Polynesia is more likely found on and near islands with French navy
facilities. Two islands in FP were blasted with radiation for more than 30 years.
•
Conversely what proof is there that a benthic (bottom dwelling HAB) such as Gambierdiscus
can travel in open oceans and have colonised islands with relatively recent geological
histories and not have traveled by recent boat ballast introductions.
•
Macroalgal rafts would also include benthic microzooplankton grazers that would feed on
benthic epiphytic dinoflagellates (who can’t travel open oceans by other means), until they
would exhaust their food supply in such a small enclosed habitat, pre-emptying any
colonization of far flung islands by natural means.
•
Shipwrecks dump boat ballast on a reef and disturb the reefs substrate assisting a localized
region of coral to a macroalgal phase shift, if they were carrying the radiated/super toxic
dinoflagellates species, then those islands may have then, had their first CFP outbreaks
(Cooper 1969, Randall 1958)?
•
A previous hypothesis of the explosion of Crown of Thorns outbreaks, not researched,
suggested that a mutated/radiated form of CoTs becoming more dominant in the coral reef
environment due to the ability of a mutated larval stage to locate around adult CoTs; CoTs
outbreaks assisted phase changes from coral to macroalgal reefs for the radiated/ “super”
Gambierdiscus to bloom; both the CoTs larvae and the “super” strain together being spread
by boat ballast around the same time period and such CoTs and the following CFP
outbreaks occurring in the same regions?
Regional Toxicity.
•
Personnel communication with Dr Marie-Yasmine Bottein: who knows that there are
differences between Pacific and Caribbean ciguatoxins; could this be related to a radiated
source for a Pacific “super” species that has not been found in the Caribbean.
Gambierdiscus has a restricted survival time in boat ballast, just as scientists have trouble
delivering live specimens, and not have had the ability to traverse the canals of the central
American land mass from Oceanica to the Caribbean or perhaps the dominance of
Ostreopsis in the Caribbean has not permitted the radiated/super species of Gambierdiscus
to become dominant in the environment.
•
Ciguatoxin is more highly toxic than other natural toxins, could this be due to the radiated
“super” toxic species that has an anthropogenic radiated mutated form rather than a
naturally occurring source?
•
Can we be certain that ciguatoxins, of today’s potency, occurred prior to the era of atomic
weapons testing? Early CFP in the Caribbean was misnamed by a toxic mollusc, “cigua” that
more likely could have caused DSP by the genera Prorocentrum?; on at least one occasion
Capt. Cook was poisoned by a puffer fish (tetraodon poisoning), his naturalists notes verify
this (it was not ciguatera as some papers would have us believe); their would have been a
lack of refrigeration leading to more cases of scromboid poisoning and in some cases a prior
lack of knowledge of other seafood toxins, such as saitotoxin in past centuries.
•
It is not to say that ciguatoxin and Gambierdiscus did not occur prior to the atomic weapons
testing, as early outbreaks such as Samoa may have been due to large blooms of the
original lesser toxic species and others, but that a more toxic mutated species rapidly
evolved to dominant the coral reef environment since WWII.
Pacific vs. Caribbean CFP.
•
Perhaps CFP in the Caribbean is now more likely due to a greater percentage of toxins
other than CTX, such as Palytoxin from Ostreopsis, as a greater proportion of deaths due to
CFP have been implicated in that region.
•
The Caribbean may be going through a new phase of succession in habitat toxicity, as there
could appear to be a shift in the dinoflagellate assemblage (away from the pioneering
Gambierdiscus of initial coral to macroalgal phase shifts to more abundant Ostreopsis and
Prorocentrum) at more well established macroalgal reefs, due to high anthrogenic sources
of nutrients, as this has also occurred on inshore reefs of the Great Barrier Reef.
•
CoTs outbreaks did not occur in the Caribbean and yet a sea urchin “Diadema die back” did
occur in the 80’s which may have been due to Ostreopsis which has been known in recent
times to destroy sea urchins in Brazil (research of Professor Graneli & Yasumoto) and in
New Zealand, and hence Ostreopsis is more likely to be dominant culprit in Caribbean CFP
(supported by Tosteson).
Biodiversity
•
The source of biodiversity for the Oceanica region (corals/fish etc) exists in SE Asia and
decreases going east through the Pacific, without anthropogenic causing bio invasives
perhaps we should expect the same for dinoflagellates or is their biodiversity greatest at
sites of weapons testing (Marshall Is / Kiribati/FP) where radiation mutated dinoflagellates
could be found?
•
The biogeography of seagrasses, deficient in the eastern pacific and more prevalent in SE
Asia may have slowed the occurrence of CFP to the SE Asian region, as they have slowed
the coral to macroalgal phase shift by absorbing excessive nutrients around coral reefs.
Epidemology
•
The CFP Oceanica epidemiology points to and could with further study highlight how, the
first “new age” CFP outbreaks, first originating in those archipelagos, where atomic weapons
testing took place (eg Marshall Is., French Polynesia and Kiribati and associated naval
bases) and then radiating to the north (Hawaii) and south and spreading westward with the
worst outbreaks now occurring in Fiji and Vanuatu. In South East Asia, the CFP outbreaks
have been more recently recorded in the Philippines and are now being recorded in
Indonesia and Malaysia.
Other
•
Merely changing nutrient ratios changes morphology of Gambierdiscus in culture and
perhaps toxicity, why not expect radiation to mutate dinoflagellates to be “super” toxic?
•
In Earth’s history, the original habitat when dinoflagellates evolved would have been higher
in radiation, dinoflagellates may have the ability to survive at certain differing distances from
radiation blasts and mutate?
•
Many Polynesians (& Micronesians?) believe that CFP was caused by atomic weapons
testing. And now this scientific hypothesis could support that belief?
•
Solutions? An idea for (IAEA or other) a marine laboratory to test non/low toxic species with
radiation is to see if it impacts their toxicity and slight changes in plate size and shape
morphology?
•
Gambierdiscus was first located in islands of the central Atlantic in the 1950s but then not
found again until the 1970’s in the Gambier islands, close to the French atomic weapon
testing site.
A study of this hypothesis could be carried out by finding the dinoflagellate biodiversity around
the original weapons testing sites and relating this to shipping movements and shipwrecks
through the Pacific region together with the history of CFP (as started with some questions
within the questionnaire in chapter 6).
4. Further CFP research.
Future research about what has been presented here, has been discussed with senior researchers
who have similar concerns, with a view to gaining funds for research which would include the toxic
dinoflagellate monitoring of coral reefs, either with research already established in coral reef
conservation and management or indeed to establish such research either on a local scale or
regional scale. This research is intended to answer some of the questions put by the three
hypotheses above. An application was submitted to the IOC/UNESCO GEOHAB program,
presented here which has been endorsed:
G E O H A B APPLICATION FORM FOR ENDORSEMENT OF ACTIVITIES
Date: September 2009
PROJECT TITLE:
Oceanea Ciguatera GEOHAB,
"The Biogeographical and Biodiversity Assessment of Toxic Benthic Dinoflagellate Stocks in the
Pacific Ocean and Implications of Bioinvasion on Marine Foodwebs".
Planned duration of activity, from: mid 2011 to: 2014.
APPLICANTS:
Name: Prof. Richard Lewis
Address: Institute of Molecular Bioscience, University of Queensland, St. Lucia, Queensland 4072,
Australia. E-mail: r.lewis@imb.uq.edu.au
Name: Assoc. Prof. Paul Bienfang, SOEST, University of Hawaii, Manoa, Honolulu, Hawaii, USA
E-mail: bienfang@soest.hawaii.edu
Name: Mark Skinner
Entox, National Research Centre of Environmental Toxicology, University of Queensland, Kessels
Road, Coopers Plains, Queensland, 4108, Australia.
E-mail: mark_skinner59@yahoo.com.au
Key invited persons:
Invited applicants
Expertise & Role (anything to add, please?)
Prof. Gustaaf Hallegraeff, University of
HAB specialist, advisory.
Tasmania, Australia.
Dr Wayne Litaker, NOAA, NC, USA
HAB ecology & taxonomy, advisory.
Prof. Matti Lang,
Molecular genetics, advisory.
Dr Ian Stewart &
Bioassay specialist, N2A component.
Dr Wasa Wickramasinga, Entox, UQ,
Bioassay specialist, co-coordinator.
Prof. Ove Hoegh-Guldberg,
Coral reef scientist, advisory.
Assoc. Prof. Ron Johnstone &
Coral reef scientist, program co-ordination.
Assoc. Prof. Norm Duke, Centre of Marine Mangrove
Studies, UQ, Australia
&
Biogeography
specialist,
advisory.
Dr Marie-Yasmine Bottein &
Ciguatoxin analysis, advisory.
Dr Steve Morton, Marine Biotoxins Unit
HAB Collection & Taxonomy, advisory.
NOAA, SC, USA
Dr Miriele Chinain ILM, FP
Ciguatera specialist/regional co-coordinator.
Dr Peter Vroom, Pacific coral reef Coral reef monitoring specialist, regional
monitoring, NOAA, Hawaii, USA
collection co-ordination.
Dr Florence Boisson, IAEA, Monaco
Assay specialist, advisory.
Dr Michael Holmes, NUS, Singapore
Ciguatera specialist, regional co-coordinator.
Dr Being Yeeting, SPC, New Caledonia
Fisheries specialist, Regional co-ordination.
Dr Glen Shaw, Griffith University, Australia
Regional co-ordination.
Dr Bill Aalbersberg, CMS, USP, Fiji.
Regional centre co-coordinator.
Dr Angela Capper &
Ecotoxicology scientist, trophic interactions.
Dr Kirsten Heinmann, JCU, Aust.
Microalgae taxonomy.
GEOHAB CATEGORY, Applying for endorsement of Targeted and Regional Research.
It is anticipated that as funds become available there will be more opportunities for research on a
regional basis, as the program elements can be taken up by postgraduate research students, within
their nation and supervised by invited specialists, within this field of research.
PROJECT DESCRIPTION:
Statement of the Problem.
The
negative
impacts to
human
populations
of benthic
dinoflagellate
toxins in
tropical
coastal fisheries products are well known, these impacts and increasing frequency are most felt in
indigenous coastal populations that rely on fish for subsistence and export. At the most recent CFP
workshop in Noumea 2008, led by SPC, most of the delegates of the island countries represented
declared their CFP problem to be serious and needed help with monitoring, taxonomy and
ecotoxicology etc, and that there was no funding to deal with the problem. Resolution and/or
prevention of such impacts have been hampered by the complexity of toxin(s) chemistry,
inadequate detection capabilities, and ambiguity related to the taxonomy and toxin production
among dinoflagellate species/genera.
Exotic and invasive species have been identified by scientists and policymakers as a major threat to
marine ecosystems, with dramatic effects on biodiversity, biological productivity, habitat structure
and fisheries. One factor that may contribute to the success of exotic species is when the recipient
ecosystem (coral reefs) is heavily destabilized, by anthropogenic causes; from climate change,
eutrophication, pollution, over fishing, crown of thorns outbreaks, maritime installations, etc or any
combination of such influences, which may initiate coral reef degradation to a macroalgal phase
shift. In coral reef studies the phase shift to macroalgal reefs due to human disturbance has been
well documented. Those disturbances have aided the ability of benthic, mixotrophic and toxic
microalgal epiphytes to flourish upon renovated macroalgal reefs. Toxic microalgae, like their hosts
are at the bottom of every food chain that they are associated with, when a coral reef becomes
degraded and macroalgae become more dominant. The succession/decline of a coral reef to one
that is algal(or even more advanced cyanobacterial and HAB) dominated, could be furthered by
microalgae, whose toxins are capable of sublethal impacts(such as decreased fecundity of fish) on
any of the food web communities that would normally be found on a healthy coral reef. Hence the
hypothesis that coral reef succession to algal domination is reinforced by dinoflagellate toxins
needs to be researched; if it is supported, as we know the coral reef community’s biodiversity is
rapidly lost and one consequence more easily recognised, is ciguatera outbreaks; then such toxic
microalgae may be partly responsible for the decline of coral reefs and possibly responsible for
preventing any reversal of phase shifts.
It is now an appropriate time to consider a program on the biogeography of the causative
microalgae as it may be that certain species or clades of genera of ciguatera causative microalgae
(Gambierdiscus, Ostreopsis, Prorocentrum) are greater toxin producers than others; there is a need
to research the hypothesis of super toxic species (or clades/strains), how common are they and
what is their distribution? Such a program would also test the hypothesis of whether the CFP
causative organisms are bio-invasive in nature; whether or not there are range extensions due to
climate change and whether they have far reaching impacts on coral reef food webs and the role
they may have in coral reef phase shifts. This program would also be used to support those island
states and countries that participate, with their needs in dealing with CFP and monitoring their
situation.
Description of Prospective Work.
The prospective project (see research framework in appendix) would describe the biogeography of
Gambierdiscus, Ostreopsis and Prorocentrum species from at first the invited collaborators shared
record of SEM Gambierdiscus work, that already has taken place from different localities. Secondly,
in a large number of localities throughout the Pacific, using up to date taxonomy tools/information
and with a coordinated approach for "collections of opportunity" among various collaborating island
nations, where sampling efforts and monitoring can be established, with the provision of
postgraduate researchers or government staff to undertake such monitoring and collections, a
record of the organisms biogeography can be achieved. As has been done within Hawaii, we would
establish a coordinated network of stakeholders to target geographically broad localities, arrange
for appropriate sampling/preservation efforts, and then perform the taxonomic assessments to
describe the relative abundances and distribution of these species.
To enable assessment of the role of ballast water in the bioinvasiveness of these genera, special
efforts will be made to identify areas representing a wide range of ship access, and shipping
intensity; for example, within the Hawaiian Archipelago we anticipate the coordination of sampling
with both the Main Hawaiian Islands, and the uninhabited Northwest Hawaiian Islands. Results of
this work is also expected to dovetail and leverage future planned work on toxic benthic
dinoflagellates within GEOHAB, to be coordinated by this collaboration; and to involve scientists
from beyond the Pacific: the Caribbean, Indian Ocean, Mediterranean Sea and the archipelagos of
Indonesia and the Philippines.
A second target of the work will collect dinoflagellate materials from some selected sites to
isolate/culture and/or extract toxins and measure the MW of toxin material produced. Given that
this effort will require substantial control over the collections, it is anticipated that the participant
nations employ postgraduate research students for this collection and monitoring efforts, and where
possible be coordinated with coral reef monitoring projects (such as Reef Check or NOAA’s coral
reef monitoring). We envisage correlating microalgal biogeography and ecotoxicology with coral
cover, where coral monitoring coincides with microalgal collection.
The third target of this research will focus on examination of food web effects of the extracted toxin
material produced. Implementation of this facet will require considerable amounts of extracted toxic
material. We anticipate using the growth rate of juvenile fish and/or shrimp as dependent
ecosystem variables; we believe we may also have means to assess responses by corals to
introduction of dinoflagellate toxins.
Brief description of research strategy:
Research Institutes (regional ciguatera research centres) have in place the infrastructure to support
ciguatera research within regions around the Pacific. As a model, the Institute de Louis Marlarde in
French Polynesia (East Polynesia) has a microalgal toxin unit where, Dr Miriele Chinain and staff
support their research programs and with funding support postgraduate students to undertake
research. Associate Professor Paul Bienfang, Ciguatera Project Leader, Centre for Oceans and
Human Health, University of Hawaii, has the infrastructure that would be able to support regional
research in Micronesia and North Polynesia. In Fiji, the University of the South Pacific has the Marine
Studies Centre which, if funding was available, could support research students in the ciguatera field,
in those island nations (West Polynesia and South East Melanesia), who take part in the program. This
can be supported by various institutes at the University of Queensland that have facilities: for
identification, such as the Centre of Microanalysis & Microscopy (SEM); Centre of Marine Studies,
(genetic sequencing & culturing); assays and toxin extraction and detection, Entox & QHSS,
(bioassays, MS) and the Institute of Molecular Bioscience (bioassays, MS).
Brief description of the draft activity plan:
2010. Approach GEOHAB for endorsement. Invite researchers to collaborate and their students to
participate.
2012. Apply for funding. The first step in the implementation of this plan is to have a practical ciguatera
workshop, to carry on from the workshop in Noumea in 2008, to bring together all current and
prospective researchers, including students from prospective island nations, to present the most up to
date research, taxonomy and monitoring protocols and put forward and implement regional plans,
based around students carrying out a biogeographical study of toxic dinoflagellates, in their country,
that will promote further collaboration with research institutes and government, so that island nations
obtain assistance in dealing with their CFP problem. Such a workshop could be held at the University
of Hawaii.
2012. Research student training and pilot monitoring and benthic microalgal biogeographical
collections.
Research students (Masters) from their island nations continue field work in their prospective nations,
establishing monitoring programs with their appropriate government agencies, using up to date
technologies. Coral reef food web pilot ecotoxicology trials.
2013. Completion of monitoring and return of students (PhD), from selected nation localities, to their
institutes for toxin analysis of samples, taxonomical work and food web mesocosim trials.
2014. Completion of student research thesis and report writing. Completion of manuscripts for
publication and presentation at another ciguatera workshop/conference.
Brief overview of Outputs.
- At the completion of the biographical study an historical record of CFP outbreaks can be used to
determine if there has indeed been a pattern to the CFP and the causative species, which in turn
will determine the microalgae’s bio invasive nature and their possible range extension due to global
warming.
- A better understanding of the biogeographical nature of ciguatera outbreaks would enable the
environmental managers responsible; to better redefine the limits of those regions responsible for
and related to anthropogenic inputs into coastal CFP outbreak areas.
-The fishing community and industry could more accurately target the exclusion of high-risk
localities of species whilst reducing unnecessary wastage and avoiding disease outbreaks and
possible litigation.
- Provide the input of knowledge to improve public support for imported seafood products and help
protect export markets of reef fish and maintain the health of the public who supports this industry.
- Assist in ensuring the stability of the fishing industry and promote the development of
environmentally sustainable jobs.
- Establish some key environmental indicators that can be used by Governments, agencies and
island communities to reduce anthropogenic factors that increase ciguatera prevalence.
-Assisting in the development of an integrated approach to coastal and fisheries management.
Scientific: Researchers of program elements to promote their results through posters and seminars at
regional ciguatera and international GEOHAB and International HAB seminars and conferences
(ISSHA).
Training: At regional workshops training provided to assist postgraduate researchers and local
government staff to monitor and research ciguatera HABs. Specific training to be provided for activities
in taxonomy (i.e. IOC/UNESCO course in HAB taxonomy), toxin extraction and bioassays. With
courses open to participants from a range of backgrounds from regional nations.
Planned dissemination of results: International journals (Harmful Algae, Marine Pollution Bulletin etc),
conference presentations (ISSHA, Pacific Science Congress, ciguatera workshops) and local news
items.
Management contact (contact person, if applicable): Mark Skinner, mark_skinner59@yahoo.com.au
BENEFITS FROM GEOHAB:
Feel free to comment on how the activity could benefit from endorsement by GEOHAB, and/or how the
SSC might assist the activity:
GEOHAB is a highly respected international program and endorsement upholds a high level of
scientific rigor to the proposed activities. This targeted research program, when implemented, will gain
international recognition and itself further the backbone on which GEOHAB gains credibility in the
tropical region nations. Acting to solve some of the environmental problems associated with ciguatera
which has been ignored by the scientific community at large, as sourcing funds for research has been
a major obstacle and hence a lack of researchers now exist in this field.
The SSC may assist the activity by providing support to sourcing funds so that research, workshops
and training may be implemented.
LINKAGES WITH OTHER PROGRAMMES:
Is the project part of a National Program? No, but contacts will be established.
Is the activity part of, coordinated with, or affiliated with, other international/regional programs? Not
at present.
FUNDING
Has funding been obtained? No
(Prospective) source(s):
regional basis.
APPENDICES
Invited participants to assist where sources of funds may be found, on a
HUMAN IMPACTS TO CORAL REEFS:
Bleaching or damage from Global Warming,
CoTs, Ocean Acidification, Over fishing,
Maritime Installations, Chemical & Biological
Pollution, Eutrophication, Sedimentation, etc.
Physical: current, salinity, shading
WATER
temperature, dissolved oxygen,
QUALITY
PARAMETERS light intensity, turbidity, stratification.
Chemical: pH, salts, B.O.D., ammonia,
nitrites, nitrates, metal chelates,
phosphates. Biological: bacterial.
PHASE SHIFT
CORAL
REEFS
Symbionts, Mucilage, Bacteria, Plankton
Impacts on
FOOD
WEB
BIODIVERSITY
MACROALGAL
REEFS,
(Brown & Red Algae)
Rubble & Sediment
Herbivory?
CIGUATERA
TOXIN IMPACTS (sublethal
& lethal) on BIODIVERSITY?:
assimilation, biotransformation,
bioaccumulation & excretion.
MIXOTROPHIC,
EPIPHYTIC
MICROALGAE
TOXIN UPTAKE
TOXIC DINOFLAGELLATES:
GAMBIERDISCUS, PROROCENTRUM
& OSTREOPSIS
(toxic cyanobacteria & toxic diatoms?)
Mutualistic,
habitat niche with
micro flora, micro
fauna, bacterial &
detrital benthos
associations.
BIOGEOGRAPHY & MONITORING
Species, strain, abundance, toxicity, distribution,
natural & boat ballast transfer, range extension & bioinvasiveness.
Ciguatera research framework, linkages of toxic microalgae to coral reef phase shifts, by Mark Skinner
The response from GEOHAB (IOC/UNESCO) to this application, written by Mark Skinner & Paul
Bienfang with editing by Richard Lewis, was endorsement, please see the response below:
15 June 2010
Dear Professor Lewis,
I am responding to your request for GEOHAB endorsement for the research project "The
Biogeographical and Biodiversity Assessment of Toxic Benthic Dinoflagellate Stocks in the Pacific
Ocean and Implications of Bioinvasion on Marine Food webs".
I am delighted to respond that the GEOHAB Scientific Steering Committee has unanimously
endorsed the project in the category Targeted Research. I apologize on behalf of the SSC for the
fairly long delay in responding to your request—we have been dealing with some structural issues
with the website, and your endorsement was put on hold while that was straightened out. As you
may be aware a list of endorsed projects is put on the GEOHAB website (www.geohab.info) with
some basic information about them. We therefore request URL links for your endorsed project(s)
and we can then insert it/them in the website. Increased project visibility is just one of the benefits of
GEOHAB endorsement. We will be contacting you concerning further basic information on your
project to place on the website, and if you have any other suitable materials we can place them
there also. In the meantime, if you are able to identify other relevant projects of interest that could
be entrained into GEOHAB I would be very grateful.
As you are no doubt aware, GEOHAB activity within the next year involves establishment of a new
CRP on Benthic HABs, as well as participation in the International HAB Meeting. Rest assured that
you and your endorsed project partners will be added to the GEOHAB mailing list. As your project
progresses, we would be delighted to receive updates or highlights. GEOHAB submits an overview
article annually to Harmful Algae News, and we also report to IOC, SCOR, IPHAB, etc. annually on
our progress. As part of these reports we keep track of all peer-reviewed publications that
acknowledge GEOHAB or the CRPs.
To date, there are more than 100 such citations, which we also post to the website. We will include
any publications by your group if you either let us know of your publications, or as part of our annual
update (using keyword search in Google Scholar). One of the chief aims of GEOHAB is to
encourage studies and analysis of comparative ecosystems. GEOHAB welcomes any advice on
what the Steering Committee can do to facilitate this.
With very best wishes,
Professor Raphael Kudela,
Chairman GEOHAB SSC.