Marine Biotoxins and Harmful Algae:
A National Plan

III. BLOOM BIOLOGY AND ECOLOGY


1. Bloom Dynamics
1.1 Background
The impacts from harmful or toxic blooms are necessarily linked to the population size and distribution of the causative algae. Efforts to manage fisheries resources affected by algal blooms or to assess the possible impacts of anthropogenic influences on harmful species requires an understanding of bloom biology and ecology.

The growth and accumulation of individual harmful algal species in a mixed planktonic assemblage are, however, exceedingly complex processes involving an array of chemical, physical, and biological interactions. Blooms can occur over wide geographic areas and may involve long-distance transport to affected resources. Harmful blooms can also occur on the ocean bottom, caused by either microscopic or macroscopic algal species. Macroalgal blooms need not produce toxins to be hamful. They can dominate planktonic or benthic communities, changing food web structure and altering habitats for many marine organisms.

Our level of knowledge about each of the many harmful algal species varies significantly, and even the best-studied remain poorly characterized with respect to bloom or population dynamics. Resolution of various rate processes integral to the population dynamics (e.g., input and losses due to growth, grazing, encystment, excystment, and physical advection) has not been accomplished, but is fundamental to the long-term management of fisheries resources or marine habitats affected by harmful algae. Many of the processes are difficult to quantify in the field because harmful species are often only a small fraction of the biomass in natural samples. The end result is that there are no predictive models of population development, transport, and toxin accumulation for any of the major harmful algal species in the United States.

Within the past two decades, the incidence of toxic blooms caused by formerly undetected taxa (the so-called "hidden flora") has increased (Anderson, 1989; Smayda, 1990). The basic biology and environmental triggers for toxic activity of these cryptic species have not been characterized. U.S. coastal waters are generally becoming nutrient enriched, often because of human influences. The impact of increased nutrients on harmful algal bloom events remains uncertain, however, and the relative importance of natural variance vs anthropogenic influences on blooms is not known (Smayda, 1990). To further confuse the issue, global changes and trends in several physical and chemical parameters, such as temperature and UV radiation, as well as nutrient enrichment, may also affect harmful algal blooms.

The long-anticipated potential of remote sensing is becoming a reality in the study of harmful bloom dynamics. Near real-time sea surface temperatures have been used successfully to identify oceanic features and water masses associated with blooms of two harmful species in two different hydrographic regimes (Keafer & Anderson, in press; Tester et al., 1991). This approach needs further refinement and should be extended to other species and regions of the United States.

There is a serious deficiency in our understanding of the physiology and genetics of toxin production. Potentially harmful algae exhibit genetic variability to the extent that toxic and non-toxic strains occur within individual species, and toxic species exhibit a range of inherent potencies. These differences in toxin composition and content are genetically and environmentally regulated, and increase the difficulty in identifying and evaluating the harmful effects of these algae. Development of molecular probes and other techniques for genetic characterization would aid in the identification and separation of harmful algae present in mixed natural populations.

1.2. Impediments and Recommendations
The Bloom Biology and Ecology working group identified five major impediments to progress in the area of algal population dynamics, biology, and ecology, and one impediment in the area of phytoplankton monitoring. The group recommended solutions to these impediments.

IMPEDIMENT: Adequate documentation of harmful algal events is difficult because of the lack of rapid, species-specific methods for counting and separating cells from natural samples.

RECOMMENDATION: Support cooperative development of molecular probes (nucleic acid and antibody-based) and other techniques for genetic characterization. Provide access to appropriate facilities and equipment; disseminate technology and probes.
Harmful and benign organisms are currently difficult to distinguish in a timely fashion. This restricts identification and separation of harmful algae for their rapid quantification and analysis within multi-species planktonic assemblages. Nucleic acid and antibody probes, which target different cellular components, offer high flexibility and specificity in their design and application. Some laboratories which have the appropriate skills, expertise, and equipment can provide training and support for others that have the need for probes but lack these resources. Equipment should be made available for the analysis of field and laboratory samples, perhaps through a dedicated facility with a flow cytometer and equipment for nucleic acid and protein analysis. Probes are in an early stage of development for several harmful species, but for most species, there is no sequence information or other biochemical characterization that can be used to design specific probes. Knowledge about one species can frequently be applied to closely related species, greatly accelerating the rate at which unstudied species can be characterized. With immediate support, species-specific probes for several harmful algae could be available within one to two years. A battery of probes against many harmful species could follow within 5 years. Once the genes involved in toxin production are identified and characterized, probes can be developed to identify only toxic species. The use of such probes in quantifying target cells requires additional studies of the physiological variability of their molecular targets under different environmental conditions.

IMPEDIMENT: Population dynamics, including the rate processes required in predictive models of harmful blooms, cannot be adequately described or predicted, although this information is of fundamental importance to effective resource management.

RECOMMENDATION: Determine biological rate processes and initiate studies of coastal hydrography and water circulation for development of physically/biologically coupled models at temporal and spatial scales appropriate to harmful algal blooms.
Despite the fundamental importance of predictive models for harmful algal blooms in different regions, no such models exist for U.S. problem species. Knowledge of the rate processes that determine the net accumulation of cells and physical models of the regional hydrographic features that influence the initiation, distribution and maintenance of blooms are both indispensable to such models.

Information on bloom dynamics can be gained through laboratory and field studies that define nutrient uptake kinetics, growth rates, loss terms, and life cycle dynamics. While field conditions such as circulation, meteorology, and water chemistry have long been recognized as critical elements in blooms of some toxic species, neither the initial boundary conditions, nor the hydrographic regimes within which harmful blooms occur are clearly understood. Regional multi-disciplinary field efforts, adequate to characterize the physical circulation models, are needed. Ideally, these would be 3-5 year programs. The ultimate goal is to couple population dynamics with physical circulation models for a given hydrographic regime, and to refine the physically/biologically coupled models using field bloom observations and toxicity patterns. Laboratory studies could be accomplished within about 2 years per species. Field studies can be greatly facilitated by timely accessibility to archived and in situ environmental information.

IMPEDIMENT: Competitive outcomes in species selection and succession cannot be predicted, nor can the relative effects of natural vs. anthropogenic factors be resolved.

RECOMMENDATION: Undertake experimental studies on factors regulating selection and succession, emphasizing grazing, nutrients and related anthropogenic variables, and allelopathic effects of toxins.

Prediction of harmful species occurrences and evaluation of potential stimulation by anthropogenic influences are essential for effective resource management. The few available long-term data sets strongly suggest a link between nutrient enrichment and increasing occurrences of known harmful species as well as formerly undetected taxa ("hidden flora").

Prediction of the outcomes of competitive interactions between harmful algae and other food web components depends upon understanding the processes regulating growth, toxicity, and encystment of individual harmful species. Laboratory experiments (2-3 years) can be used to examine growth across gradients of nutrients (i.e., absolute concentrations and variable supply ratios), temperature, salinity, light, mixing, and grazing by appropriate predators. Given this knowledge, experiments can be expanded to include natural communities (e.g., in mesocosms, field enclosures; 5 years) in order to examine competition, grazing, allelochemical effects, and other influences on selection and succession of harmful algae. These field data can be used to estimate rate constants for accumulation and loss terms which, in turn, would enable construction of mathematical models needed to assess mitigation strategies under variable environmental conditions.


Understanding the influence of anthropogenic effects will require analysis of data bases for phytoplankton communities and tractable anthropogenic variables such as inputs of nutrients and other pollutants. Initiation or expansion of long-term monitoring programs of at least 10-years duration must include both episodic events and nutrient time-series studies. Short-term and long-term correlations between pollutant inputs and abundances of harmful algal species, together with information from the autecological studies, will provide a basis for mesocosm-scale experiments. These experiments (3-5 years duration) are needed to test potential mitigation strategies and strengthen interpretations about the influences of anthropogenic variables on bloom species selection and succession.

 IMPEDIMENT: There is insufficient knowledge of the physiology of algal growth and toxin production in response to environmental variables.

RECOMMENDATION: Conduct experimental studies of organism physiology, emphasizing environmental tolerances and factors which influence growth and toxin production. Expand culture collections to include broad geographical representation of all potentially harmful species; include multiple clones from single populations.

Tolerance ranges and optima for growth and toxin production in response to environmental variables such as salinity, temperature, and light must be determined for multiple toxic and non-toxic (if available) clones of each species in batch culture. In addition, classical steady-state analyses of nutrient requirements and uptake rates and toxin physiology (including content and composition) of each species are necessary. This work will depend upon a supply of appropriate isolates, our ability to manipulate them in culture, and the availability of sensitive and reliable methods of toxin analysis. Physiological experiments can be carried out in tandem with studies of tolerance ranges and optima once the basic individual growth requirements are determined, and will take 3 yrs to complete for each species.

Individual clones of a single species exhibit marked variation in numerous characteristics, including growth and toxin production (Maranda et al., 1985; Bomber, et al., 1989; Cembella et al., 1987; Hayhome et al., 1989), and thus may not be representative of local or regional populations. A few laboratories in the United States have initiated "syndrome-based" culture collections of harmful marine microalgae. Presently, isolates housed in these collections do not adequately represent the full range of variants characteristic of each harmful species. It is essential that new clones be established from throughout the geographical range of each harmful species. Establishment of clones should be accompanied by basic screening programs in order to select ideal clones for physiological and toxicological studies.

Production of toxins in quantities sufficient for their purification and characterization requires identification and culture of "high performance" clones and knowledge of their growth requirements. Such collections could be established within a 3-year period. Completion of basic screenings may extend each project into a fourth year.

There are anecdotal and circumstantial accounts of bacterial involvement in toxin production by harmful algal species, but only one set of published data demonstrates bacterial synthesis of PSP toxins (Kodama, 1990). The existence of toxigenic bacteria and their association with harmful algal species must be investigated. This work will rely on the isolation of bacteria and the development of techniques that optimize our ability to detect toxin production. Verification of toxigenic bacteria will take about one year for each species of harmful algae once methods are accepted for unequivocally demonstrating the presence or absence of the bacteria.

2. Phytoplankton Monitoring

2.1. Background

Testing shellfish and other seafood for possible toxins is expensive and time-consuming. Further, current seafood monitoring efforts are often limited by cost and geographic area covered and may not even test the food product most affected by a particular toxin. An easier and possibly more effective approach involves regular, routine sampling and analysis of phytoplankton samples, especially in areas where aquaculture and/or recreational harvesting are common. If potentially toxic phytoplankton species are found, then more expensive seafood testing must be done.

Routine phytoplankton monitoring would provide long-term data on the occurrence of harmful algal species and foster the development of testable hypotheses and insights into the status and trends in harmful algal bloom events. Retrospective analyses of the few existing historical data sets and initiation of time-series will allow assessment of the role of improved monitoring programs and strategies. This information will also promote development of badly needed mitigation methods.

2.2. Impediments and Recommendations
IMPEDIMENT: Coastal environmental programs are inadequate for bloom detection, monitoring and mitigation of bloom effects.
RECOMMENDATION: Identify regional expertise and facilities. Establish species-specific monitoring programs on a regional scale, using shipboard techniques and remote sensing where appropriate. Identify sentinel species appropriate for each specific toxin and habitat type. Organize regional response teams and logistical support for unexpected events, and reporting centers to accommodate rapid response. Develop practical response protocols for protecting aquaculture sites on a regional and/or species-specific basis. Coordinate and develop national and regional training programs (e.g., sampling and identification methods). Develop and disseminate adequate reference materials.
Adequate phytoplankton monitoring programs can serve as early warning systems to moderate the effects of blooms on public health, aquaculture, and fisheries. Response teams, organized by region using existing expertise and maintained as part of a national program, should augment species-specific monitoring programs in areas of recurring bloom events. In-water monitoring and remote sensing provide the early warning systems needed by the aquaculture industry and government officials. Further, long-term data sets are needed for trend analyses. These recommendations are a high priority and must be implemented through federal/state/
academic/private industry partnerships.

A network of sentinel sites might be composed of local residents and user groups who are often the first to recognize a bloom event and notify local government agencies. Other sentinel sites could be located at coastal aquaculture facilities. Government and/or industry personnel must be able to sample and quickly identify the causative organism and determine whether it is a known or potentially toxic species. Samples must be sent to taxonomic experts for verification. Technical training will provide the expertise needed for early warning systems and local response. Training should be structured at several levels.

These recommendations should be implemented immediately and continue indefinitely, although possibly on a somewhat reduced level after 5 years, depending on trend analysis and local needs. The Canadian domoic acid experience has shown that phytoplankton monitoring can be an effective component in a program to protect seafood consumers from marine biotoxins.

IMPEDIMENT: The causes and effects of harmful blooms of benthic and planktonic macroalgal species are poorly understood.

RECOMMENDATION: Evaluate the manner in which macroalgal species composition can be influenced by nutrient enrichment, coastal erosion, and other human activities. Determine the effects on habitats and food-chain structure that are associated with macroalgal blooms.

Much of the focus in this program is on microscopic algal species which bloom in surface waters, but harmful blooms of macroalgae also occur. These can cause harm by altering benthic habitats through the displacement of indigenous species, and by changing food-chain structure and dynamics. One manifestation of coastal nutrient enrichment is the enhancement of benthic (and, on occasion, planktonic) macroalgal abundance, with certain opportunistic species often dominating. Not only will studies of benthic algal species succession and dominance be necessary for effective management of coastal resources, but the changing distribution and abundance of these species through time and space may provide strong evidence of the extent of human impacts on algal populations in general.