Download Monitoring and Management of Harmful Algal Ihoorns: A

Monitoring and Management of Harmful Algal Ihoorns: A Global Perspective
Donald M. Anderson
Biology Dept., Woods Hole Oceanographic Institution, Woods Hole MA 02543 USA;
1 508 289 235 1; [email protected]
Gregory J. Doucette
NOAAMOSICenter for Coastal Environmental Health & Biomolecular Research,
Charleston SC 294 12 USA; 1 843 762 8528; [email protected]
Summary. Harmful algal blooms (HABs) represent an increasing threat to coastal waters worldwide. This
growing trend in the incidence of HABs poses an enhanced risk to human health, natural resources, and
environmental quality, while causing severe economic losses through impacts on fisheries and tourism. The
critical importance of our coastal waters dictates that urgent steps be taken to better monitor and manage
harmful algal species and the resources they threaten. The following topic areas comprise a framework for
considering HAB management options: prevention - environmental management alternatives for reducing the
incidence and extent of HABs prior to their initiation; control - intervention in response to bloom events to quell
or contain them; mitigation - actions aimed at reducing the losses of resources and economic values and
minimizing human health risks associated with HABs. Here we provide examples of efforts that are underway ,
in various countries to implement HAB management strategies, or to conduct research supporting such efforts.
Among the thousands of living marine phytoplankton species Are a few dozen which cause harm, either because
of the potent toxins they produce or the biomass of their "blooms". Evidence is compelling that harmfil algal
blooms (HABs) represent an increasing threat to coastal waters worldwide and thus an escalating challenge to
those charged with managing the coastal zone and its resources. ,Several authors have provided detailed
accounts of this growing trend in the incidence of HABs (Anderson 1989, Smayda 1990, Hallegraeff 1993),
which poses an enhanced risk to human health, natural resources, and environmental quality (Boesch et al.
1997), as well as exacting a large economic toll due to negative impacts on'fishery and tourist industries. Along
with the recent proliferation of harmful blooms, scientific research aimed at achieving a better understanding of
their causes and behavior has accelerated rapidly over the past decade. By comparison, complimentary efforts
focused on identifying and implementing management options for these events have generally been neglected.
The issue of HAB management is only now being viewed with a greater sense of urgency and commitment. A
recent report by Boesch et al. (1997) highlights the growing risks posed by HABs'in the United States, and
recognizes the associated need for improved precautions to protect human health, more effective management of
activities contributing to HABs, and renewed consideration of potential control strategies. That report identifies
three primary components of an effective HAB management strategy: prevention - the environmental
management options for reducing the incidence and extent of HABs prior to their initiation; control intervention in response to bloom events to quell or contain them; and, mitigation - actions aimed at reducing
losses of resources and economic values, as well as human health risks, associated with HABs. It is within this
framework that issues related to the monitoring and manakement of HABs will be discussed here.
Prevention. The prevention of bloom events before they occur presents an especially challenging problem.
given our inadequate understanding of environmental factors causing blooms and the unique characteristics of
various HAB types (e.g., high biomass vs. toxic). Regulation of environmental variables potentially influencing
HAB formation is a prevention strategy with promise, but it is not without inherent difficulties. Other
potentially important regulatory factors such as natural climatic cycles (e.g., El Nifio; Maclean 1989) remain
intractable. Nonetheless, based on a growing number of laboratory and field studies of the environmental
factors affecting the growth, abundance, and distribution of HAB species. several options for prevention are
evident. First. is the control of inputs into the coastal zone - primarily nutrient loading and freshwater inflows.
The well-documented increase over the past several decades in animal production. use of chemical fertilizers.
foss11fuel consumption. and sewage disposal has lead to dramatically elevated levels of plant nutrients in coastal
waters, frequently accompanied by shifts in the relative abundance of these nutrients (see Smayda and Shimizu
199 1). While a causative link between such anthropogenic nutrient inputs and the occurrence of many HABs
remains equivocal, nutrient loading may contribute to the intensity and persistence of some bloom events.
particularly those categorized as high biomass HABs. Changes are often gradual and are easily obscured by
community modifications caused by fluctuations in other controlling factors such as temperature. light or
physical forcings. The most obvious examples of change are those where the eutrophication has been severe and
rapid. In the Comacchio Lagoons (Italy), for exampre, where anthropogenic nutrient discharges into poorly
flushed waters led to a hypereutrophic state, the phytoplankton population became dominated by chain-forming,
poorly edible cyanobacteria. A drastic reduction in zooplankton, zoobenthos, and fish also occurred (Sorokin et
al., 1996), documenting the extent to which major changes in the phytoplankton component of the food web can
lead to significant alteration in ecosystem structure.
Another prominent example of the
linkage between HABs and pollution involvr the recently
discovered "phantom" dinoflagellate Pfiesteria. In North Carolina estuaries and in the Chesapeake Bay, this
organism has been linked to massive fish kills, to the presence of large, open lesions on living fish, and to a
variety of human health effects, including severe learning and memory problems (Burkholder and Glasgow
1997). A strong argument is being made that nutrient pollution is a major stimulant to outbreaks of Pfiesteria or
P'steria-like organisms. Even though this linkage to pollution remains a subject of debate, the evidence is
sufficiently strong that legislation has been enacted restricting the operations of hog and chicken farms so as to
ke
reduce nutrient loadings in adjacent watersheds on the easternshore bf the ~ h e s a ~ e a Bay.
Potential benefits of nutrient management strategies,
especially in areas of high loading andor limited
flushing/circulation, should be a decline in the frequency
and severity of blooms. An example of the effectiveness
of better managing nutrient inputs was seen in the Seto
Inland Sea, Japan. Following a ?-fold increase in algal
blooms over an eleven year period as industrial and
other developmental pressures led to pollution of that
water body, reduction of the chemical oxygen demand
by 2-fold through the implementation of sewage efflaent
controls and removal of phosphorus fiom detergents
reduced the frequency of blooms by nearly half within
five years (Fig. l ;after Okaichi 1989).
Regulation
of freshwater inflows can, in certain cases,
be considered in the context 'of HAB prevention
strategies by reducing local salinities so as to exclude
halophilic HAB species. However, such an approach
must be balanced with considerations of the nutrient
load being carried with this freshwater.
Figure 1. Red tide events in the Seto Inland Sea, Japan
before and after regulation of COD (after Okaichi 1989)
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Another area in which preventative measures may be effective in reducing HABs, especially in previously
unaffected regions, is by adopting protocols to avoid or minimize the risks associated with species introductions
andor dispersal. The primary targets of such strategies are the transfer of algal cells andor their encysted forms
via ships' ballast water, the movement of shellfish and finfish stocks (including eggs), and activities involving
.dredging. Although conclusive evidence for the introduction of a HAB species causing unprecedented blooms
in an area is lacking, unequivocal proof of ballast water transport of toxic dinoflagellate cysts has been reported
by Hallegraeff (1991). These fmdings establish the efficacy of such a distribution vehicle and point out the need
to take the precautions necessary to avoid ballast water introductions. Similarly, careful regulation of shellfish
stock transfers by incorporating risk-reduction strategies, such as prohibiting import of material from areas
affected by HABs or the cleaningldepuration of animals, is clearly warranted. In the case of dredging,
oxygenation of sediments inherent in this process provides conditions known to promote the germination of
cysts, which would otherwise remain dormant in anoxic sediments (Anderson et al. 1982). Survevs of HAB
cyst distributions and knowledge of environmental factors facilitating germination should thus be taken into
account when evaluating and managing the risks associated with dredging operations.
Control. The significant public health, economic, and ecosystem impacts of HABs would seem to make these
phenomena legitimate targets for control efforts. Yet while human efforts to control insects, diseases, and f h g i
are common agricultural practices on land, similar attempts to control unwanted plants or animals in the ocean
are rare. Several countries - notably Japan, Korea, and China - have invested research on this topic (Anderson
1997). Nonetheless, control of HABs remains largely untested on major blooms, as field trials have been
restricted to shallow ponds used for shrimp and fish rnariculture or to the waters in the immediate vicinity of fish
cages. General approaches to control include: 1) chemicals that kill or disrupt HAB cells during blooms; 3)
clays or other materials that flocculate (precipitate) and scavenge cells and other particles from the water
column, transporting them to the ocean floor; and 3) biplogical agents such as viruses, bacteria, lor parasites
which are lethal pathogens to HAB species.
Attempts to use chemicals to directly control red tide cells in blooms encounter many logistidal problems and
environmental objections. It will clearly be difficult to find a "magic chemical bullet" that will somehow kill
only a specific, targeted HAB species, as it is difficult to imagine a unique physiological target for a chemical
that is characteristic only of one phytoplankton species. Chemical control of blooms is thus an area where '
considerable research is needed. Even if a chemical is found with ideal properties, environmental objections are
likely to be significant. Each candidate chemical will require extensive testing for lethality, specificity, and
general safety, and each must surmount significant regulatory hurdles. Although direct chemical control of red
tides may not be a strategy of choice given other more benign alternatives, the success of this approach in
terrestrial systems suggests that it should not be complptely ruled out.
A flocculant is a material that, when added to water, precipitates and scavenges CO-occurringparticles as it falls
to the sediments below. One inexpensive, non-chemical flocculant that shows considerable potential for HABs
is clay. The variable physiology/biochemistry of different algal species affects the degree to whioh they can be
removed by flocculation, and the structure and charge of various types
of clay can affect the specificity of flocculation as well. The Japanese
(reviewed in Shirota 1989) and Chinese (Yu, pers. comm.) have
studied the theory behind clay as a flocculant in seawater, and both
groups have tested a variety of natural and treated clays on red tide
species in culture. Depending on the treatment used, removal of 95:
99% or more of the targeted cells in cultures has been accomplished
with clay additions. In field trials, the Japanese have successfully used
clay to treat natural red tide blooms on both small (e.g., fish cages) and
0 0.2 0.4 0.6 0.0
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large scales (Shirota 1989). Laboratory studies exploring the use of
clays for HABs affecting U.S. coastal waters have been initiated
clay concentration (glL)
recently, and show promise in the case of several HAB species,
including the Florida red tide dinoflagellate, Gymnodinium breve '
(Fig. 2; Anderson unpublished results). While issues with respect to Figure 2. Removal efficiency of IMC-P
the cost of the clay, storage of the clay on-site, and dispersion phosphaticclay for G. breve (D. Anderson
methods remain to be addressed, control strategies based on use of un~ubl.results)
flocculants appear worthy of further consideration.
'
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There are a variety of organisms that could conceivably be used as biocontrol agents for HABs, but in reality,
this approach has many logistical problems and is far from the application stage. Biological control is used
extensively in agriculture, but there is still considerable opposition to the concept of releasing one organism to
control another. Despite examples where such an approach has had negative long-term consequences on land,
there are cases where the approach has been both effective and environmentally benign (Anderson 1997). The
concept thus deserves consideration in marine systems.
One obvious group of organisms to consider is the zooplankton which
CO-occurwith algae and eat them as food. However, Steidinger (1983)
provides calculations that illustrate the logistical impracticality involved
in growing zooplankton predators in the laboratory in sufficient quantity
to control blooms. Viruses also have potential to be highly specific and
effective control agents. In reality, however, viruses are sometimes so
host-specific that they are unable to infect different genetic strains of the
same host species, a situation likely to be encountered in algal blooms.
Another concern is that environmental regulations concerning the release
of a viral pathogen might be severe. There are a variety of different
parasite species that can infect marine organisms, inchiding algae. The
highly virulent nature of parasite infection of dinoflagellates has led to
the suggestion that these might be effective in controlling red tide
populations (Taylor 1968). A key issue once again is host specificity? as
it would be ideal if an introduced parasite would only attack the targeted
red tide organism and then die-off after the demise of the bloom. This
is. however, an area where little is known with respect to HAB species. Figure
. 3. Killing of^. breVqeculture b!
Finally. a body of new work suggests that bacteria could play an adding algicidal bacteria(D0ucette et al.
important role in controlling HABs (reviewed by Doucette et al. 1998). in press)
,
,
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An intriguing example is a bacterium isolated at the ehd of a Gymnodinium mikirnotoi bloom, exhibiting strong
and very specific algicidal activity against this dinoflagellate species (Ishida 1998). Another study has
described an algicidal bacterium targeting Gymnodinium breve, which produces a dissolved compound capable
of killing cultures of this species within 24 hours of introduction (Fig. 3; Doucene et al. in press) and thus far
showing a high degree of target specificity. As with other approaches to biological control of HABs, studies on
bacteria have ,been confined to basic scientific investigations of the nature of the interaction, with no attempts
, ,
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involving practical applications.
Mitigation. The area of HAB mitigation includes those activities aimed at reducing losses of resources and
economic values, as well as minimizing human health risks resulting from blooms not otherwise prevented or
controlled (Boesch et al. 1997). Several of these activities, including monitorinp/su~eillance,forecasting, and
se,veral action alternatives (e.g., public education and information), are more likely to prove effective in the
short term than many of the prevention and control strategies outlined above, and should thus be pursued
vigorously as management options for1 HABs. Monitoring/surveillance programs targeting HABs have
traditionally been aimed at detection of toxins in contaminated fishery resources. These programs have proven
highly effective and continuing advances in toxin detection methodology (see Cembella et al. 1995) promise to
further enhance the efficiency of this process. While this approach provides data on the current toxicity of a
resource, it nonetheless precludes any measures to preempt exposure to a toxin that might be possible given
advanced warning of an impending toxic event. Thus, efforts are being made in several countries to augment
toxicity testing With phytoplankton monitoring programs for the detection of HAB species (see Andersen 1996).
Considerable work is also being directed at the development of advanced technologies, such as species-specific
molecular probes (Scholin 1998), some of which are currently undergoing field trials and are ultimately ,aimed at
automating the process of identifying and enumerating cells of HAB species. Development of forecast models
for HABs is presently in its early stages. Predictive modeb 'integrating both biological (e.g., life cycles,
physiology) and pbsical (e.g., circulation, meteorology) components show the most promise and are currently
being developed by several research groups. Integrating certain types of data collected on a near-real time basis
by automated, in situ instrumentation, with forecast models represents a potentially powerfil management tool
that warrants the attention of both the research and regulatory communities. Finally, given the public confusion
over HABs and their effects, and the resulting negative impacts on fishery and tourism industries, efforts to
better inform and educate citizens should be primary targets of mitigation strategies. The recent Pfzesteria
outbreaks in the southeastern U.S.are a prominent example of the extensive public and political attention that
can arise from an unexpected and highly publicized outbreak. This is but one of many cases worldwide in
which the economic impacts of a HAB are multiplied significantly through misconceptions and over-reaction.
A comprehensive HAB management plan should thus include both communication and education programs,
involving researchers, resource managers, public health oEcial, the medica community, and the general public,
with an emphasis on dissemination of timely and accurate information.
'I
We have outlined several examples of efforts that are underway in various countries to implement HAB
prevention, control, and mitigation strategies, or to conduct research supporting such efforts. Nonetheless,
continued development of methods to more effectively deal with HABs and their impacts will require a global
change in the "mind-set" of scientists and funding agencies alike. Research and pilot studies with outcomes
aimed specifically at enhancing the capabilities of coastal zone managers in the area of HAB management are
needed, as is targeted support for such work (but not at the expense of fundamental HAB science). It will also
be prudent to enlist the help of those experienced in managing the impacts of terrestrial pests, given the long and
successful history of such efforts in land-based agricultural practices. Lastly, it is imperative that practical goals
be set, not only to take advantage of those tools and technologies currently in place for mitigating the effects of
HABs, but also to provide a foundation upon which to base future work in this area.
Acknowledgements
The presentation of this paper at the ICES 1999 Annual Science Conference was sponsored by the IOC Harmful
Algal Bloom Programme
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