Marine Biotoxins and Harmful Algae:
A National Plan

IV. FISHERIES AND FOOD WEBS

Harmful Algal Species

Geographic Area

Affected Organisms *

• Understanding reaction products and kinetics of metabolic transformations of toxins in shellfish tissues.
  

• Anatomical/cytochemical localization and transfer of toxins among tissues, especially when only some tissues are marketed, (e.g., in scallops, surf clams and razor clams).
  
  
• Characterization of magnitude and causes of variability in toxin accumulation within a population (e.g., in relation to body size, reproductive condition, or feeding zone), and among different species.
  
  
• Development of methods to enhance the rate of toxin depuration (detoxification), especially in species of high economic value that are characterized by prolonged toxin retention (e.g., surf clams, butter clams and sea scallops).
  
  Treatment of toxic shellfish should involve relatively short time scales compatible with industry needs. Treatment methods include manipulation of natural environmental variables (e.g., temperature), development of food processing technology, or artificial methods such as treatment with ozone.
  
  
• Determine the relationship between algal population dynamics and seasonal and spatial patterns of toxicity in shellfish populations (e.g., how do vertical distribution of algal cells and benthic re-suspension affect toxin transfer?).
  
  This requires high-frequency sampling of shellfish stocks, phytoplankton populations and hydrographic features at selected field sites that are readily accessible and where toxic/noxious blooms are known to be a recurrent problem. Inter-annual variability should be determined.
  
  
• Develop predictive models of toxin kinetics (uptake and depuration by shellfish) based on integration of field and laboratory studies.
  
  Simple bioenergetics-based models have been used previously to describe and predict the accumulation of anthropogenic contaminants in aquatic systems. Modeling efforts should be especially useful in identifying the likely source and history of shellfish intoxication in areas where extensive phytoplankton monitoring is unavailable or impractical. Predicting the risk of contamination in areas as yet unaffected by shellfish toxicity episodes, but where the presence of toxic algae has already been documented, may also be possible. Models will likely aid in the design of an optimum sampling schedule for the monitoring of a particular shellfish resource.
  
  IMPEDIMENT: Information is lacking on the relative sensitivities of different life history stages to harmful algae, and on the long-term effects of algal toxins/metabolites on growth, reproductive success and recruitment of shellfish populations. Past work has largely focused on adult stages of a few species and on short-term effects on individuals.
  
  RECOMMENDATION : Assess the short- and especially long-term concentration-dependent chronic effects of harmful algae on various life history stages of shellfish (e.g., larvae, juveniles, adults). Determine the mode of action and effects of toxins on these developmental stages at both organismal and population levels.
  
  Blooms of harmful algae may exert sublethal effects on shellfish populations, and thus affect long-term persistence as well as harvestable yields of the resource. For example, toxic Alexandrium cells (Shumway and Cucci, 1987; Bricelj et al., 1991) and direct contact with Aureococcus anophagefferens cells (Tracey, 1988) can significantly inhibit feeding activity in some bivalve species. Field and laboratory studies should assess the relevance of such transient physiological effects on population fitness traits (e.g., growth rates and reproductive performance), and identify the most critical developmental stages affected. Studies involving natural populations will depend on bloom incidence in the field. Mitigation strategies such as transplanting of stocks to unaffected areas during a harmful bloom, or modification of culturing practices and schedules (e.g., early or delayed planting of seed), and stock rehabilitation efforts following a toxic episode could thus be designed to minimize adverse effects. The time frame for such studies will depend on the lifespan and growth rate of the species or developmental stage under consideration, but useful data could be provided within 2-3 years.
  
  IMPEDIMENT: The identity, mode of action, and species-specific impacts of toxins/metabolites associated with previously unimplicated harmful algae (e.g., Aureococcus anophagefferens, and Gyrodinium aureolum) have not been clearly established.
  
  RECOMMENDATION : Identify the potentially noxious bioactive compounds associated with these algae, determine their mode of action on shellfish, and develop sensitive bioassays for their rapid detection.
  
  Blooms of Aureococcus anophagefferens have recurred in New York waters since 1985, and were also documented in RI and NJ waters in 1985 (Cosper et al., 1989). Blooms of a related picoplanktonic alga recently occurred in Texas (Stockwell et al., in press). Aureococcus caused weight loss of adult bay scallops and mortality of adult mussels and recruitment failure of bay scallops (Tracey, 1988; Bricelj and Kuenstner, 1989), but only anecdotal information is available for the effects on other commercially important bivalves, such as the American oyster and hard clam. Less susceptible species might provide a viable aquaculture alternative during brown tide episodes.
  
  Gyrodinium aureolum , a species with ichthyotoxic properties, has been shown to cause mortalities in a number of bivalves (scallops, oysters and mussels) in Europe (Tangen, 1977; Partensky and Sournia, 1986) and was recently considered responsible for mass shellfish mortalities in Maquoit Bay, ME (Heinig and Campbell, 1992). Preliminary studies have shown deleterious effects of this alga on feeding of nine juvenile species, and mortality in some species (Shumway, unpublished data).
  
  Medium-term (3 years) laboratory studies are required to determine the effects of these algae on a broad range of species. Such studies should verify the existence of a concentration threshold below which no adverse effects are observed. Understanding of concentration-dependent effects will help to develop mitigation strategies (e.g., site selection for aquaculture ventures). Bioassays could be developed over the short-term (2 years), before chemical characterization of bioactive compounds has been achieved, and should determine if these active compounds are extracellular and/or intracellular.
  
  IMPEDIMENT: An extensive historical database on accumulation and depuration of PSP toxins has been collected by state and federal monitoring agencies, but this "grey" literature is scattered and not readily accessible to potential users.
  
  RECOMMENDATION : Compile, integrate and interpret existing data in order to further elucidate general patterns of toxification/detoxification in commercially important shellfish on a regional and national basis.
  
  IMPEDIMENT : Availability of isolates of toxic/noxious algae is limited. These are essential for physiological studies on effects and mode of action of toxins.
  
  RECOMMENDATION : Establish additional cultures of algal isolates/clones, and develop culture techniques where these are not available (e.g., Dinophysis spp.).
  
  For some species of harmful algae that affect the United States, only single cultures are available (e.g., Aureococcus anophagefferens ). This severely biases laboratory studies towards isolates that may not be representative of the natural populations. Efforts to culture the DSP-producing Dinophysis spp. have so far been unsuccessful. Continued research on Dinophysis species is highly desirable, but does not warrant a major investment of funds until DSP is shown to be a real rather than a perceived problem to U.S. shellfish.
  
  IMPEDIMENT : Rapid, reliable methods for field-testing of shellfish are lacking. Standards for quantification of toxins are limited and often unavailable. Analytical methods for detection and quantification of toxins in animal tissue (e.g., PSP and DSP toxins) need improvement. Lack of radiolabeled toxic compounds limits the scope of laboratory studies on toxin transfer in shellfish.
  
  RECOMMENDATION : Provide low cost, certified toxin standards; develop and test rapid methods for in situ detection of toxins; improve analytical methods and provide radiolabeled toxins for quantification of toxins in shellfish tissues.
  
  1.2. Finfish: Impediments and Recommendations
  
  IMPEDIMENT: The physiological responses of fish exposed to toxic and other marine harmful algae are poorly known.
  
  RECOMMENDATION : Complete the identification of known or suspected fish-killing algal species and their toxins or harmful metabolites. Establish the mechanisms underlying algal-caused fish kills, the routes of toxin delivery, and the varying effects on different life history stages of fish. Develop standardized laboratory bioassay techniques for key fish species. Examine bioaccumulation of toxins and possible physiological feedback mechanisms between fish and phytoplankton.
  
  Although fish exposed to harmful algae are known to die of respiratory failure in some cases, the underlying causes and physiological mechanisms may vary among species or are unknown. Severe economic damage is caused by several species of harmful algae, although the routes of toxin delivery and physiological reactions of fish are poorly understood. Modes of toxin production and ichthyotoxic action should be studied because human consumers of fish may be at risk if toxin accumulates in an unpredictable fashion in fish muscle tissue. This limits the ability to mitigate the problem for aquaculture and to understand and predict the consequences for wild fish stocks. There may be multiple causes of fish death due to harmful phytoplankton, and their relative contribution is difficult to detect or predict. For example, the raphidophyte microflagellate Heterosigma akashiwo (found on both coasts of the United States) and related species (Chatonella marina in Japan) may suffocate fish due to massive mucus production by the gills, by neurotoxin suppression of respiration, or by destruction of blood components (Onoue, 1990; Chang et al., 1990; Black et al., 1991; MacKenzie, 1991; Rensel Associates and PTI Environmental Services, 1991). Tools and methods of investigation are generally available and the above recommendations could be achieved in 5 to 7 years.
  
  IMPEDIMENT: Harmful phytoplankton blooms are a major impediment to the operation and development of marine finfish aquaculture.
  
  RECOMMENDATION : Develop more effective methods of mitigating the effects of harmful algal blooms on finfish aquaculture.
  
  Catastrophic losses of aquaculture fish have occurred in the United States in recent years due to species of harmful phytoplankton previously not recognized as toxic or present (Horner et al., 1990). Monitoring by fish farmers in coastal waters provides a valuable link and permanent sampling platforms for assessing the frequency and trends of harmful blooms. Mitigation based on physical movement of water into net-pens or oxygenation is feasible and already practiced in some cases, but once the underlying causes of fish mortality are known, other types of mitigation will be possible. Such strategies are necessary for harmful algal species that often occur throughout the water column or are difficult to detect in aerial or boat surveys. The time lines involved in developing effective mitigation techniques are short-term (2-4 years), depending on the species involved.
  
  IMPEDIMENT: Investigators of fish-kills involving algal blooms often lack training, specialized equipment, and communication networks needed to detect, investigate, and determine causes.
  
  RECOMMENDATION : Promote and expand communication among aquatic user groups, resource agencies, and specialists. Develop field sampling protocols and streamlined physiological or pathological assays to determine which algal toxins or species were responsible for fish losses. Establish systematic reporting and data base management of marine fish kill data.
  
  Marine user group and resource agency personnel are generally not experienced or trained regarding harmful marine phytoplankton blooms. Fish kills often occur quickly, before agency or research personnel are able to react. As a result, little knowledge about the causes of algal-related fish kills has been gained. Although fish kills may be increasing in frequency, determination of actual trends is impossible at present. Many resource agencies will investigate fish kills first for anoxic/hypoxic water conditions, or will suspect diseases, chemical spills or pollution before searching for other causes. Phytoplankton sampling and/or testing for toxin content is often a low priority or is not attempted. Development of handbooks similar to those used to investigate fish kills in freshwater (e.g., Meyer and Barclay, 1990) will allow agency staff or volunteers to collect fish tissues in a proper manner for analyses. Fostering communication between university or federal experts and aquatic user groups (fishermen, aquaculturists) will expedite reporting and accurate assessment of the causes and extent of fish kills. This is a short-term efffort that will require periodic review.
  
  1.3. Food Web Effects: Impediments and Recommendations
  
  IMPEDIMENT: Investigative responses to kills of marine animals are often ineffective.
  
  RECOMMENDATION: Establish rapid response research capability and associated geographic information system (GIS) data base.
  
  Present studies of sudden toxic bloom events and resulting contamination and kills of marine biota are not pre-planned, are poorly coordinated, and often take place too long after the event to be useful. Thus, determination of the causative organism(s), the routes of toxin transfer, the nature of the effects on marine animals, and the risks to public health is difficult or impossible. As such, these responses are usually reactive, not proactive. By the time stricken animals arrive at analytical facilities, toxins may no longer be present at detectable levels. Infrastructure and funding should be provided to enable the investigation of toxic and noxious blooms at their peaks in terms of toxin assays of plankton, intermediate vectors, fish, and other wildlife. Selected species should be assayed over time to determine duration of toxin retention and changes in toxin profiles. Professionals in the fields of wildlife veterinary medicine and biology, and toxin analysis, should be trained in sampling protocols aimed specifically at marine biotoxins. Regional rapid response teams should be coordinated with the simultaneous efforts of similar teams investigating blooms and the origin and fate of the toxins (see below). All results could be stored as overlays in a GIS data base. This type of archive and retrieval system offers the most effective means of linking spatially-related data and testing hypotheses about the importance of oceanographic processes, land-use practices, and environmental factors to harmful algal bloom dynamics and food web effects.
  
  IMPEDIMENT: Risks of biotoxins to marine animals or to public health resulting from the movement of toxins through the marine food web chain currently cannot be addressed.
  
  RECOMMENDATION: Develop quantitative models of the fate and consequences of biotoxins in the marine food web.
  
  Important pathways of toxin transmission have not been identified, nor has toxin accumulation potential and sensitivity been determined for many key marine species (i.e., species that are either commercially important, endangered, or serve as major food web links). The information necessary for development of these models could be obtained primarily by multi-disciplinary, rapid response groups investigating bloom dynamics and toxin transmission in the food web, coordinated with other supporting studies (e.g., laboratory and field feeding and observational studies).
  
  2. Shellfish Monitoring Programs
  
  2.1. Background
  
  In the United States, the monitoring of marine biotoxins and/or associated phytoplankton in seafood and the environment has been primarily the responsibility of state-sponsored programs. The relative success of these programs can be measured by the lack of overt public health morbidity or mortality from consuming contaminated seafood (Ahmed, 1991; Bean et al., 1990). However, the sampling programs of individual states vary in magnitude (Table 3), dependent upon the degree of seafood production or import, commitment of resources, and political will.
  
  The responsibility of the state programs can extend to products from international waters and interstate imports. These programs can implement the closure of a fishery based upon existing action limits for only two marine biotoxins, paralytic shellfish toxin and amnesic shellfish toxin, or they can exercise other policy considerations such as the lack of sufficient information about a fishery. Presently, closure limits based on the presence of other marine biotoxins have not been established. When few monitoring stations are employed to cover large coastal areas and the frequency of sampling is relatively low, program officials close large fishery areas as a conservative measure to protect the consumer and consumer confidence in the seafood industry. This is the case especially when health officials attempt to deal with toxic effects from an
  TABLE 3
  
  1989 STATE PSP MONITORING STATIONS
  
  STATE NUMBER OF SAMPLES
  (NO. STATIONS)
  Maine 3500 (200)
  Washington 1900 (50)
  California 1100 (not fixed)
  Oregon 780 (16)
  Massachusetts 700 (98)
  Alaska 654 (40)
  Connecticut 51 (5)
  Rhode Island 40 (8)
  New Hampshire 34 (1)
  
  
  unidentified toxic substance. Monitoring is not only important in the closure process, but is critical for establishing re-openings.
  
  International imports are subject to routine inspection by United States Customs and can be embargoed if found to be contaminated. On the other hand, international exportation of seafood products from the United States are subject to the seafood importation standards at the point of destination.
  
  The collection of a sample can be accomplished in many ways. Sub-samples can either be taken by program personnel, delivered from commercial harvests at the point of landing, or before delivery to market. State programs support "sentinel" species programs whereby specific or mixed species of molluscs (e.g., mussels for PSP) are strategically placed along coastal areas that are subject to harvesting activity. These sites are sampled regularly to provide an early warning of the presence of toxins. The relative effectiveness of a sentinel program can be measured by the number of sampling sites per area covered and the frequency of sampling. In addition, with few exceptions, sentinel sites typically are positioned near-shore and do not provide information about offshore toxin distribution. In practically all cases, the analyses for marine biotoxins are carried out by state or federal laboratories, the exception being the availability of uncertified commercial laboratories that conduct analyses for domoic acid.
  
  Within state programs, however, the responsibility of seafood monitoring can be decentralized, with different programs charged with the management of different seafood industries (e.g., shellfish industry, finfish industry, crab industry, etc.). The specific mandates of each of these sub-programs may present a narrow focus to a particular biotoxin problem, depending upon the region and indigenous biotoxins present. While focused programs may provide adequate protection to the consumer, these efforts can be inflexible when attempting to respond to the presence of newly-recognized biotoxin threats. Communications between state programs and interagency entities can at times be tenuous, even during crises.
  
  Ideally, these efforts are designed to lead to a proactive response. That is, the toxins are detected within the seafood prior to commercial sale of product. In practice, this may be viewed as reactive, since a toxic sentinel site or product is already contaminated and the monitoring effort is not 100% for all seafood (nor should it be). The State of Florida exercises a "preemptive" monitoring program, which combines seafood and phytoplankton monitoring with aspects of remote sensing to recognize algal blooms prior to their impact on fisheries.
  
  2.2 Impediments and Recommendations
  
  IMPEDIMENT: Current monitoring efforts are too limited and inflexible to measure the full impact of marine biotoxins. The extent of the distribution of marine biotoxins in consumed seafood products is not known.
  
  RECOMMENDATION: In those instances where newly-recognized toxins impact a fishery, state and federal resources should be made available to aid monitoring programs. Various seafood products should be surveyed on a region-by-region basis for the most important biotoxins and the products affected.
  
  Existing routine monitoring programs are, by design, limited to managing specific resources. On those occasions where marine biotoxin crises arise, routine state and federal funding mechanisms are inadequate to address the immediate concerns. This places a huge burden on state and federal agencies to redirect resources from predetermined programs to deal with the crisis. Contingency funds and a mechanism for rapid deployment are needed to help state and federal programs respond to crises such as toxic plankton blooms, fish kills, and marine mammal kills. Time is of the essence if these efforts are to be effective.
  
  All coastal areas contain various types of marine life and biotoxins. The utilization of existing biotoxin monitoring elements to address all biotoxin concerns may not be appropriate. Therefore, the search for affected seafood products and additional biotoxins will be an evolving process. The ultimate goal of this effort will be to create more efficient and cost-effective programs.
  
  IMPEDIMENT: The public health community and seafood industry require early warning of toxic/harmful phytoplankton blooms to protect seafood consumers and producers.
  
  RECOMMENDATION: Identify the best indicator species within specific regions. Identify the best sites and sampling strategies for these indicator species.
  
  Presently, bivalve molluscs (e.g., mussels, oysters or clams) are employed as the primary sentinel organisms. These species may or may not reflect accurately the true nature of a toxic algal bloom. For example, mussels have been employed as sentinel organisms for the detection of domoic acid (Haya et al., 1991). They may not, however, always be the best predictor of the presence of domoic acid, as was shown on the West Coast when razor clams were toxic but mussels were not (Wood and Shapiro, 1992). A primary sentinel species may, in fact, be a non-consumed species with characteristics of toxin uptake, distribution, and retention that provide useful data for particular toxins. Further studies on a regional basis are required to determine which species best accommodate specific biotoxins and analyses. These studies should be conducted locally to account for regional variations and should identify species with both long-and short-term retention times. These studies would take 2-3 years for completion.
  
  Monitoring programs are only as good as the analytical support they receive. Present laboratory support is limited by the number of facilities and methods currently available. In addition, in those instances where newly-recognized toxins are found, a full understanding and characterization of the toxin must be obtained before an appropriate sentinel organism can be identified.
  
  In order to identify sites and sampling strategies, models that describe temporal and spatial distributions of toxins must be developed. The presence of biotoxins in marine life is subject to the effects of regional hydrographic conditions. In order to develop the model and account for the environmental conditions, the distribution of toxins among sites and individual organisms must be evaluated statistically and include both nearshore and offshore locations.
  
  IMPEDIMENT: The collection, preservation, and handling of naturally-occurring toxic seafood and algal samples for use by researchers and public health officials is hampered by a lack of standardized procedures.
  
  RECOMMENDATION: Develop internationally accepted and appropriate collection, preservation, and shipping protocols.
  
  With the lack of standardized handling and shipping methods, the implementation of public health measures is hampered. Furthermore, the development and refinement of methods for biotoxin detection are also impeded. In particular, it is necessary to understand the fate and stability of biotoxins in natural seafood matrices. Currently, the methods used for the collection and handling of contaminated seafood are not standardized. It is not known how these conditions affect toxin stability. If sample integrity is compromised, analytical results are questionable. This could be easily tested by conducting spiking studies or splitting contaminated samples prior to shipment. The initial method development and subsequent collaborative studies could be completed within 2-3 years.
  
  Due to increasing interest and awareness of marine toxins and algal blooms on the part of the general public, scientists, and public health officials, we can assume that in the future, new toxins or the extension of known toxins to new seafood items will be documented. As the public and health professionals inevitably begin to associate illness with the consumption of a seafood product, there will be increasing demands to "explain the cause of the sickness". There is a need for the development of standardized, generic laboratory procedures, techniques, protocols, and surveys that could be compiled and be "ready-to-use" by local and state public health agencies to meet and deal with these inquiries.
  
  IMPEDIMENT: Slightly different policies for dealing with fishery closures due to a marine toxin outbreak can lead to industry problems in contiguous states sharing the coastline and the toxin problem.
  
  RECOMMENDATION: Encourage the states to form regional communication networks and harmonize risk management policies.
  
  If one state closes a fishery while the others do not, processors and fishermen move from the affected state to the state where the fishery is still open. This places stress on the open industry and appears to place the closed state at a competitive disadvantage. In addition, if the toxin outbreak does impact several states, regulatory tracking of risk species becomes virtually impossible due to lengths of coastline, mobility of fishermen, and multi-state licensing of fishing boats. It is better if states sharing coastline and toxin risks develop a harmonized closure action plan.
  
  IMPEDIMENT: Authority for dealing with both known and new marine toxins occurring in seafood is sometime fragmented within state management agencies, leading to inter- and intra-agency jurisdictional overlap and confusion.
  
  RECOMMENDATION: Encourage the states to streamline programs dealing with marine toxin risks by placing monitoring and management control in a single regulatory agency.
  
  In many states there is a fragmentation of authority between state agencies for action on a fishery due to the presence of a toxin. For example, in some states, authority is divided among the Departments of Agriculture (for crustacea and finfish), Health (molluscan shellfish), and Fisheries (resource closures). There may be a variety of good reasons for this fragmentation; nonetheless, when a toxin such as PSP is found in a "non-traditional" species such as Dungeness crab, it becomes difficult for the state to formulate and take appropriate action. States should be encouraged to streamline their programs in dealing with marine toxin risks, i.e., place monitoring and control in one agency.