The following regional summaries present brief perspectives on specific HABs. Written by workshop participants familiar with each region, they review available information and point out deficiencies. These are provided to document the extensive geographic scale of HAB impacts and to illustrate the diversity of the phenomena involved. In some cases, the regional summary only reflects one manifestation of a particular phenomenon, and thus understates the extent of the HAB problem. For example, macroalgal blooms in Florida are described, but similar outbreaks occur in coastal waters throughout the U.S. Similarly, cyanobacterial blooms are highlighted on the U.S. east coast, but occur on both costs as well as in rivers, lakes and ponds throughout the country.
It is obvious from these summaries that serious information gaps exist in all regions and for all organisms, but some deficiencies are similar across multiple regions. The summaries also highlight how information bases differ among regions, due to different physical regimes, causative organisms, and/or level of research. This is true even when the organisms are the same or similar (e.g., Alexandrium spp. along the Northeast and Pacific coasts).
HAB phenomena are truly diverse, and it is this diversity that must be accomodated in the ECOHAB science plan. Clearly, single investigator and multi-investigator, regional projects are required to address the many identified deficiencies. This approach can address the immediate information needs of each region, but ECOHAB will derive significant benefit from comparisons among regions and attempts to highlight common principles or mechanisms underlying many of these phenom ena.
Northeast Region: PSP
The most significant HAB problem in the northeastern U.S. is PSP caused by several closely related species in the di noflagellate genus Alexandrium. The affected resources are predominantly shellfish, but PSP toxins also affect higher levels of the food-web, including lobsters, fish, and marine mammals.
Paralytic Shellfish Poisoning. PSP is a recurring problem that has affected large areas of the region every year for over two decades. Prior to 1972, shellfish toxicity was known only in eastern Maine and Canadian waters to the north. That year, a massive bloom introduced A. tamarense to southern waters, and there have been shellfish harvesting quarantines along large sections of coastline every year since. A second expansion of the regional PSP problem occurred in 1989, when the rich shellfish beds of Georges Bank and Nantucket Shoals were found to be contaminated with PSP toxins. The size of the offshore area affected, the difficulty in monitoring an area so far from land, and the slow depuration of toxin from the affected shellfish have necessitated a permanent closure of the surf clam fishery on Georges Bank for the past five years.
One key feature of the ecology and bloom dynamics of toxic Alexandrium species in the northeast is that they include a dormant cyst stage in their life histories. Cysts germinate in the spring to inoculate overlying waters with a "seed" population.
In the southwestern Gulf of Maine, Alexandrium cell distributions are associated with a coastal current or buoyant plume formed by the outflow from rivers in southern Maine (Franks and Anderson, 1992a). The southward propagation of this plume and the entrained Alexandrium cells creates an annual north-to-south sequence of PSP toxicity, beginning in late May or early June. The plume is influenced by freshwater flow, wind, and bathymetry, with predictable consequences for the location and timing of coastal PSP events. Extensive freshwater flow in early May creates a strong, fast plume, while low river flow may preclude the formation of a coastal plume. Upwelling-favorable winds oppose the propagation of the plume, forcing it offshore and arresting its north-to-south motion. This tends to halt the alongshore propagation of toxicity, leaving the southern regions toxin-free. In contrast, downwelling-favorable winds force the plume against the coast, and accelerate its alongshore propagation. Such conditions lead to widespread toxicity, and may account for the recent occurrence of PSP on Georges Bank (Franks and Anderson, 1992b). Understanding of the physical forcings that influence the location and dynamics of the coastal buoyant plume, and information concerning the abundance of Alexandrium cells within the plume have given us a limited predictive capability of the location and timing of toxic outbreaks over large (>100 km) scales (Franks and Anderson, 1992b).
Other potential HAB Problems. The general view of the harmful algal bloom problem in New England is that PSP is widespread, persistent and expanding, while outbreaks of other harmful species cause sporadic damage on a smaller scale. A realistic concern is that HAB species already present within the region are likely to cause problems in the future. For example, an outbreak of Gymnodinium mikimotoi caused extensive benthic mortalities in 1988 in Maine, a region of New England that is rapidly expanding its salmon farming industry. This fish-killing species causes recurrent and significant financial losses to the fish farming industries throughout the world. Likewise, Pseudo-nitzschia pungens f. multiseries, a diatom responsible for ASP, has been detected in Gulf of Maine waters, and its toxin (domoic acid) detected in scallops. Over the last several years, DSP has been detected in Canadian shellfish located just to the north of New England, where DSP is not yet a problem.
Some species, identified in other regions as problem algae, are regular components of the Gulf of Maine flora. The prymnesiophyte, Phaeocystis pouchetii, is a regular and sometimes dominant component of the spring bloom, but does not reach the high cell densities recorded in western Europe, where foam on beaches, fouling of fishermen's nets, and other negative impacts are common.
Economic Impacts. The economic impact of these outbreaks is significant, though difficult to estimate in total. Shellfish monitoring programs in each of the coastal New England states have minimized illnesses from PSP-contaminated shellfish and prevented any deaths. This extraordinary level of human health protection has come at a cost that has never been directly quantified, but must be in the range of millions of dollars per year, including the annual cost of the state and federal shellfish monitoring programs (nearshore and offshore), the value of unexploited resources such as surf clams and roe-on scallops, and the loss to shellfishermen and retailers from shorter-term quarantines, including "spinoff" effects on other perfectly safe fisheries products that are rejected by consumers during red tide outbreaks. Estimates of the losses to shellfishermen and other seafood-related industries are few, but a single PSP outbreak cost the state of Maine $6 million (Shumway et al., 1988).
Significant unknowns in our understanding of Alexandrium blooms include:
· What are the geographic origins of newly germinated cells that initiate the Alexandrium populations in the coastal current and the physical/behavioral mechanisms by which they enter the buoyant plume?
· Is accumulation of cells at small-scale fronts necessary for their entrainment in the buoyant plume? What other physical -biological interactions are important to bloom dynamics on small (<10 m) scales?
· What is the nutrient physiology of the cells, their requirements, uptake rates and nutrient status during the long-distance transport?
· Is the localization of elevated Alexandrium populations within the plume a result of physical entrainment, or does it reflect an increased growth rate in response to unique chemical properties of plume waters?
· Are nearshore cells in the coastal current responsible for PSP offshore on Georges Bank?
· What are the hydrodynamic forcings that regulate PSP outbreaks in other areas of the Gulf of Maine?
· What effect does zooplankton grazing have on the Alexandrium populations, and what are the ecosystem impacts of toxin transfer through the food-web?
Mid-Atlantic Coastal Region: Brown Tides
Blooms of the small (2-3 µm) chrysophyte Aureococcus anophagefferens, referred to as "brown tide" due to the resulting water color, have been confirmed in many locations along the northeast coast of the United States, especially in. Narragansett Bay, RI, Barnegat Bay, NJ, and the Peconics-Gardiners Bay estuary and south shores of Long Island, NY (Cosper et al., 1989a). The figure on the next page shows the widespread distribution of this organism in the northeastern U.S., including many areas with no previous history of visible or destructive blooms (Anderson et al., 1993).
Brown tides are restricted to shallow, vertically well-mixed waters, and occur during late spring and summer at maxi mum concentrations of 3 x 109 cells l-1; bloom duration ranges from one to four months. The first outbreak occurred concurrently in New York and Rhode Island in 1985, and blooms have recurred in New York bays in subsequent years, with varying intensity, duration and geographic spread. An immunofluorescent method is used for the reliable identification and quantification of A. anophagefferens.
Severe light attenuation in Long Island bays due to the brown tide caused a significant reduction in the depth penetration and leaf biomass of eelgrass (Dennison et al., 1989), which serves as an important nursery habitat for numerous fish and shellfish. Brown tides also caused severe mortalities, recruitment failure, and growth inhibition of commercially important, suspension-feeding bivalves, including blue mussels in RI (Tracey, 1988) and bay scallops in NY (Bricelj and Kuenstner, 1989). Economic losses from the brown tide for the New York State bay scallop fishery were estimated at $2 million per year during early outbreaks.
Aureococcus adversely affects feeding of larval and adult bivalves, but only through direct cell contact. Although specific cell toxins have not yet been identified, the cell surface of this microalga contains a bioactive compound that interferes with ciliary beat and thus food capture of bivalves, a response mimicked by the common neurotransmitter, dopamine. Thus, impaired grazing by zooplankton and filter-feeding benthos are believed to contribute to bloom occurrence.
The physico-chemical conditions that contribute to the formation of A. anophagefferens blooms are still largely unknown. Low annual rainfall, and increased residence time of bay waters that lead to increased salinity (> 28 ppt) may favor the development of the brown tide, as does increased water temperature (Cosper et al., 1989b). Year-to-year persistence of A. anophagefferens in the Long Island region is partly attributed to its wide temperature tolerance and thus its ability to survive overwintering conditions. Mesocosm experiments show that this alga grows well at relatively low concentrations of dissolved inorganic nitrogen (DIN), and a negative correlation has been described between the abundance of Aureococcus and mean DIN concentrations experienced during blooms. Therefore, macronutrient loading of bays does not appear to be the direct cause of brown tide, but micronutrients, including trace metals such as iron and selenium, and certain chelators, have been implicated as growth promoters in its formation. The iron requirement of Aureococcus and its ability to grow in the presence of organic nutrients (e.g., glutamic acid) are higher than for many other common phytoplankton species. Viral particles have been described and isolated from field-collected Aureococcus cells, and viral-lysis of algal cells has been attributed a potential role in bloom dissipation (Milligan and Cosper, 1994).
A number of questions need to be answered in order to more fully understand the physical and biological mechanisms controlling the population dynamics of A. anophagefferens , and the effects of brown tides on nearshore marine communi ties.
· What role does micronutrient availability, especially via groundwater, play in controlling bloom dynamics?
· What climatological-metereological and/or hydrographic events are associated with the regional occurrence of the brown tide in the northeast?
· To what extent do biological mechanisms (e.g., grazing depression, competitive interactions with other phytoplankton, and viral lysis) contribute toward the formation of monospecific blooms and subsequent decline of the brown tide?
· Is microzooplankton grazing negatively impacted by brown tide? What are the toxins/metabolites that cause species -specific inhibition of suspension-feeding in planktonic and benthic organisms?
· What are the time- and concentration-dependent effects of brown tides on marine fauna, during various life history stages? What are the effects on submerged aquatic vegetation and its associated community (secondary as well as primary consumers)? What are the long-term impacts of recurrent brown tides on community trophic structure?
East Coast Region: Cyanobacterial Blooms
Harmful cyanobacterial blooms (HCBs) are indicative of excessive nutrient loading in oligohaline estuarine waters. These blooms represent economic and environmental threats nationally, and have occurred in several large estuarine systems (e.g., Chesapeake Bay, Albemarle-Pamlico Sound, and Florida Bay). Cyanobacterial blooms are also serious problems in freshwater systems. Here we highlight the east coast of the U.S., but cyanobacterial blooms occur in virtually every state, given the existance of toxic species in both freshwater and marine environments.
Bloom taxa include filamentous (Anabaena, Aphanizomenon ) and aggregated coccoid (Microcystis) genera, which exhibit severe neuro-, cyto-, and hepato-toxicity to a variety of mammals (including man), birds, farm animals, fish, and invertebrates (including zooplankton). HCBs accumulate as buoyant surface-dwelling, high biomass blooms. They impart negative aes thetic values, and cause taste and odor problems. These blooms rapidly terminate or "crash" in response to sudden physical perturbations (e.g., rapid drop in temperature, sudden destratification and water column turnover, or reduced irradiance associated with poor weather). When crashes occur, excessive oxygen consumption as the biomass decays can lead to anoxia. This chain of events has been responsible for major estuarine fish and shellfish kills and loss of habitat for benthic infauna (Paerl, 1988a, 1990).
Conditions which favor harmful cyanobacterial bloom development and persistence include: 1) enhanced P and N loading; 2) increases in water retention time; 3) water column stability; 4) relatively high dissolved organic matter content; and, 5) for nitrogen-fixing genera, molar N:P input ratios < 15:1. Typically, blooms develop in oligohaline tributaries experiencing periods of excessive spring N and P loading (via runoff, wastewater discharge, etc.), followed by decreased flushing, persis tent vertical stratification, and surface water temperatures >20°C (Reynolds and Walsby, 1975). Buoyant noxious species have photoprotective pigments that allow them to survive at the water surface where they can remain for weeks to months (Paerl, 1988b). Grazing pressure by macrozooplankton has little impact on either initiating or controlling cyanobacterial blooms. Trophic interactions and ecosystem structure are often radically altered in response to such blooms (Porter and Orcutt, 1980; Fulton and Paerl, 1987). While physiological and molecular knowledge of individual HCB species is good, knowledge of growth, reproductive, and trophic dynamics on the ecosystem level is at best fragmentary.
Informational needs include:
· What trophic alterations (e.g., community changes and food transfer) are attributable to HCBs?
· What are the dynamics of akinete (cyst) dispersion, activation, and bloom initiation?
· To what extent can known and novel HCBs (e.g., Synechococcus spp. in Florida Bay; Nodularia, Schizothrix , and Lyngbya in reefs and intertidal environments) disperse into nutrient-enriched mesohaline/euhaline waters?
· What are the genetic and physiological potentials for such species dispersal?
· How does the ability to fix atmospheric nitrogen (N 2), facilitate expansion into N-limited estuaries or freshwater systems?
East Coast Region: Fish Kills
In 1991, an ichthyotoxic dinoflagellate with "ambush predator" behavior and a complex life cycle was discovered at a fish kill in the Pamlico River, a large estuary in the Southeast (Burkholder et al., 1992, 1995). The organism, Pfiesteria piscicida (Steidinger et al., submitted; 1995), represents a new family, genus, and species of armored dinoflagellates. Its cryptic or "phantom-like" behavior was observed several years earlier when it appeared as a contaminant of unknown origin in aquarium fish cultures (Burkholder et al., 1992; Smith et al., 1989).
Unknown substances freshly secreted by finfish and shellfish stimulate P. piscicida to transform from benthic cysts or amoebae, or non-toxic flagellated stages to toxic zoospores. Highly lipophilic exotoxin(s) are released to the water and travel as micelles that narcotize finfish, slough fish epidermis, and cause formation of open bleeding sores (see photo below), while also damaging osmoregulatory function (Noga et al., in press). In some species, (e.g., striped bass), extensive hemorrhaging also occurs. This dinoflagellate has proven lethal to every fish species tested, including more than 20 native and exotic species (Burkholder et al., in press). At sublethal densities, Pfiesteria-like dinoflagellates likely cause significant chronic impacts to fish populations, affecting recruitment, reproduction, and disease resistance. Clinical research recently demonstrated that P. piscicida is the causative agent of the disease known as ulcerative "mycosis" in Atlantic menhaden (Noga et al., in press). The Pamlico is known for high incidence of fish ulcerations and up to 98% of all fish sampled in this estuary have manifested large, open, bleeding sores during warmer months.
The dinoflagellates consume bits of epidermal tissue and blood cells from affected fish while also engulfing bacteria, phytoplankton, and other microfauna. In addition, they produce gametes that complete sexual fusion in the presence of dying fish. Upon fish death, toxic zoospores and planozygotes form non-toxic amoeboid stages that feed on the fish remains, or without abundant food resources, the toxic stages encyst. In the absence of live fish, gametes and toxic zoospores revert to non-toxic zoospores that remain highly active in phosphate-enriched waters, especially when flagellated algal prey are abun dant (Burkholder and Glasgow, 1995). Surprisingly, most of the 19 known life cycle stages are amoebae that range in length from 5-250 µm. Under certain conditions (e.g., cold temperatures) some amoeboid stages become ichthyotoxic.
In enclosed laboratory conditions, human exposure to aerosols from toxic cultures with live fish has been linked to a variety of short- and long-term symptoms, including narcosis, respiratory distress with asthma-like symptoms, severe stom ach cramping, nausea, vomiting, and eye irritation. Other autonomic nervous system dysfunction such as high, localized perspiring and erratic heart beat may last for weeks. Central nervous system dysfunction, including sudden rages and other erratic behavior can last hours to days, and reversible cognitive impairment for weeks; chronic effects such as sustained asthma-like symptoms and suppressed immune system may last for months to years (Glasgow et al., in press).
The extent of P. piscicida's involvement in fish kills likely has been underestimated because of difficulty in reaching many kills when toxic zoospores are still present. Most Pfiesteria-associated field kills have occurred in quiet, upper estuarine tributaries with poor flushing rates, where both fish secreta and toxins can accumulate and be more readily detected. During the past three years, P. piscicida has been implicated as the causative agent of ca. 50% of the major fish kills in large estuaries of the Albemarle-Pamlico system, the only region where rigorous sampling protocols have been established (Burkholder et al., in press).
About two-thirds of the Pfiesteria-caused fish kills in North Carolina have occurred in the phosphate-rich Pamlico, and laboratory bioassays have shown that some life cycle stages are stimulated by organic phosphate sources. Field surveys documented significantly higher abundance of zoospores at sewage outfall sites relative to unpolluted sites. P. piscicida is euryhaline and eurythermal, with optimal growth at 15 psu and 26 oC, but with toxic activity from 2-35 psu and 10-33 oC (Burkholder et al., in press). Some stages can remain active down to 5 oC. The wide salinity/temperature tolerance of P. piscicida suggests that this species and its close relatives are probably widespread, at least in warm temperate/subtropical regions, acting as significant but often undetected sources of fish mortality and disease. This species has been documented in sediments or water from the mid-Atlantic to the St. Johns estuary in Florida. Recently, a second, apparently more subtropical, Pfiesteria-like species was identified (Landsberg et al., 1995).
Critical questions that need to be answered include:
· What is the geographic range of Pfiesteria -like dinoflagellates? Do they occur only in warm temperate/subtropical areas or do they occur in colder regions as well?
· Can molecular probes be developed to facilitate detection of the various life cycle stages and/or the toxins they produce?
· What are the toxins? What is their chemical structure?
· How do organic and inorganic nutrients control life cycle stages and/or toxicity?
· What chronic effects does Pfiesteria and its relatives have on fish recruitment, disease resistance, and survival?
· What is the role of dinoflagellates in estuarine microbial food-webs in light of the discovery of multiple, benthic amoeboid stages in Pfiesteria? Might these also be found in the life cycles of other dinoflagellates?
Southeast and Gulf of Mexico Regions: NSP
The toxic dinoflagellate Gymnodinium breve has a distribution from the Gulf of Mexico (Mexico-Florida) to the South Atlantic Bight. This fragile species produces neurotoxins and hemolytic substances that can cause mass mortalities of marine animals, neurotoxic shellfish poisoning (NSP), and human respiratory irritation. Blooms are usually seasonal, starting in late summer/fall and lasting 3-4 months; they impact fishing and tourist industries and alter population levels or recruitment potential of affected marine animals. These recurrent bloom events cause an economic loss of approximately $18-24 million per episode (Steidinger and Vargo, 1988; Tester et al., 1991). Associated with this economic impact is an unquantifiable "halo" effect that results in reduced sales of all seafood products within the region of the bloom and even outside the region.
The most likely scenario for the development of G. breve blooms in the Gulf of Mexico and South Atlantic Bight is the following. The source of the blooms appears to be on the west Florida shelf in the eastern gulf where the Loop Current may entrain bloom patches and transport them into the South Atlantic Bight via Loop Current filaments/eddies and the Gulf Stream system (Steidinger and Vargo, 1988; Tester et al., 1991, 1993). Eddies can also transport entrained blooms to the western gulf. Blooms are initiated in association with Loop Current intrusions accompanied by upwelling on the west Florida shelf. These blooms develop on the leading edge of the Loop Current front where the boundary layer is ideal for near -monospecific growth of G. breve. Typically the cyanobacterium Trichodesmium precedes or co-occurs with G. breve at bloom initiation and its presence may condition the water mass and enhance G. breve growth as well as reduce grazing pressure. Bloom initiation is followed by population growth in excess of predation, natural mortality, and advective loss, then by sustained growth (maintenance), and finally by dissipation by advection or mixing of water masses. The physical integrity of the water mass appears to be the key factor controlling growth and maintenance of G. breve blooms. Offshore populations of G. breve can be transported shoreward with winds and inoculate inshore waters. Nutrient availability in the nearshore waters then contributes to the duration and intensity of blooms. Although G. breve is more concentrated in surface waters, it is distributed throughout the water column down to >50 m depths.
A conceptual framework for understanding G. breve blooms thus exists, but there are a number of questions that need to be answered:
· In the life cycle of G. breve, does sexual reproduction only occur in the zone of initiation, and are resting cells such as cysts or zygotes present in sediments or at pycnoclines?
· Are there "hot spots" within the zone of initiation on the west Florida shelf that retain resting stages?
· Can molecular probes be used to detect toxins in seawater or identify different strains of G. breve?
· Is zooplankton grazing inhibited at moderate to high G. breve cell concentrations when brevetoxins or other substances are released? Does G. breve regulate plankton community structure?
· Are there multiple hydrographic features that are requisite for bloom initiation that can be detected using moored instru ment arrays and remote sensing?
· Does Trichodesmium condition the water prior to G. breve blooms?
· What are the roles of macro- and micronutrients in the initial growth phase of blooms and how does the situation change over time with bloom development?
Tropical Regions (Florida, Puerto Rico, U.S. Virgin Islands, Hawaii): Ciguatera
Ciguatera fish poisoning (CFP) is the most frequently reported non-bacterial illness associated with eating fish in the United States and its territories. The actual number of cases is, however, estimated to be 2-5-fold higher, since there is no confirma tory laboratory test, and diagnosis depends on a patient's clinical presentation. Southern Florida, together with Puerto Rico and the Hawaiian islands, account for the majority of documented CFP incidents in the U.S. In the Virgin Islands, it is estimated that nearly 50% of the adults have been poisoned at least once. Many CFP intoxications have been reported from temperate "inland" locations in the U.S., resulting from the commercial distribution of sub-tropical and tropical fish species.
Gambierdiscus toxicus, an epibenthic dinoflagellate, is the organism primarily responsible for ciguatera fish poisoning (Yasumoto et al., 1977). G. toxicus produces ciguatoxin precursors and analogues that are biotransformed during food-web transfers into ciguatoxin, the causative neurotoxin (Lewis and Holmes, 1993). The ciguatera toxins are transported through herbivorous fish to carnivorous species, where they accumulate and persist over extended periods. Fish exposed to ciguatoxin exhibit impaired swimming behavior, and as a result may be subject to increased predation. Other toxic dinoflagellates, including species of Prorocentrum, Ostreopsis and Coolia, share the same epiphytic habitat and entry routes into the food chain as G. toxicus, but remain only circumstantially linked to CFP since their toxins are not known to occur in fish at levels that can affect humans.
G. toxicus does not form pelagic blooms of motile cells, but is most prolific in shallow waters (3-15 m) primarily as an epiphyte on red and brown macroalgae associated with coral reefs and protected embayments. Field and laboratory studies have established the temperature and salinity ranges of G. toxicus as 20-34 oC and 25-40 psu, respectively. Ciguatera endemic areas in both the Caribbean and Pacific are characterized by oceanic salinities and are primarily associated with island land masses; CFP is essentially absent along continental perimeters. In Florida, most cases of ciguatera are contracted in the summer, which is consistent with the elevated G. toxicus abundance observed during this period. By comparison, in the Virgin Islands neither the number of CFP incidents nor G. toxicus abundance exhibit notable fluctuations. Overall, the spatio -temporal variability of CFP in a local area corresponds largely to the patchiness of G. toxicus populations; however, it is difficult to explain the often rapid, localized changes in the concentration of this species based on a response to any one environmental factor (e.g., temperature, salinity, nutrients, etc.). The variable, localized occurrence of ciguatoxic dinoflagel lates within a region may also be related to their rafting on drift algae, which is considered to be a primary means of dispersal.
Phenotypic variation in toxicity observed between clones from distinct geographical areas are stable in acclimated cultures and thus are indicative of genetic differences. For CFP cases occurring in the Caribbean and eastern Atlantic, gastrointestinal symptoms occur first, while the characteristic neurological manifestations of ciguatera develop later and may persist for weeks to months or even years, producing chronic disabilities. Conversely, in the Pacific, neurological symptoms are exhibited first, while gastrointestinal symptoms are minor or absent. These patterns in symptomology may reflect different geographic distributions of individual CFP toxin(s).
Presently, no coordinated, systematic monitoring progams exist for CFP in the U.S. and its territories. This poisoning syndrome has a significant impact on commercial and recreational fishing activities in the U.S. and throughout the world.
Questions for future research include:
· Are there environmental factors that promote G. toxicus blooms or cause increases in the toxicity of this dinoflagellate? and, if so, can they be incorporated into predictive indices of CFP events?
· Can human activities such as reef destruction or pollution increase the scale of the problem?
· What roles do toxic species of Prorocentrum, Ostreopsis and Coolia play in CFP?
· Where and how are ciguatoxin precursors and analogues biotransformed in herbivorous and/or carnivorous fish? How do ciguatera toxins affect food-web function?
· Are there genetic markers that define the toxin content and profile of individual dinoflagellate clones?
Southeast Region: Macroalgae
Macroalgae cause problems throughout the coastal waters of the U.S. This summary for southern Florida provides one example of the nature and scale of the problem.
Over the past several decades blooms of macroalgae (seaweeds) have been increasing along many of the world's develop ing coastlines in response to nutrient enrichment associated with coastal eutrophication. In southern Florida, a diverse group of opportunistic macroalgal species outcompete, overgrow, and replace seagrass and coral reef ecosystems that are adapted to stable, oligotrophic conditions. Moreover, once they are established, the macroalgal blooms may remain in an environment for years to decades until the nutrient supply decreases. This is in contrast to phytoplankton blooms that are usually relatively short-lived (days to weeks).
The negative effects of eutrophication include nuisance blooms of macroalgae and attached filamentous epiphytes that reduce light availability to seagrasses (Sand-Jensen, 1977; Twilley et al., 1985; Silberstein et al., 1986). This results in lower seagrass productivity, habitat loss from hypoxia/anoxia, and eventual die-off of sensitive species (LaPointe et al., 1994).
Nutrient enrichment of Florida Bay and the Florida Reef Tract results from multiple nutrient sources and supply mecha nisms, including: 1) advection of phosphorus-rich water from the eastern Gulf of Mexico into Florida Bay; 2) nitrogen-rich inputs from land-based agricultural activities that enter coastal waters through the Everglades via groundwater discharge and surface runoff; and 3) nitrogen and phosphorus-rich domestic wastewater generated in the Florida Keys that enters coastal waters via groundwater discharge (septic tanks, cesspits, and injection wells) and surface water outfalls. This cumulative nutrient enrichment can cause high biomass algal blooms, which include the red algae Laurencia intricata and Spyridia filamentosa, the brown algae Dictyota sp. and Sargassum filipendula, and the green algae Enteromorpha sp., Codium isthmocladum , and Halimeda sp.
Macroalgal blooms in South Florida, as well as other factors, have contributed to the marked decline in extent and vigor of seagrass ecosystems that provide a vital nursery habitat for pink shrimp, spiny lobster, and finfish. These commercially -valuable marine species support multi-million dollar recreational and commercial fisheries that have undergone drastic de clines over the past decade. The Florida Reef Tract, the third largest coral reef in the world and the only coral reef system in North America, supports the largest recreational dive industry in the world. This valuable reef system is being overgrown by macroalgal species. The trend could lead to ecological collapse of the Florida Reef Tract, with subsequent economic losses in the tourist-related industries that support the most visited coral reef and largest marine sanctuary in the world.
Questions for future research include:
· What are the physiological and ecological mechanisms that regulate the ability of macroalgae to alter the patterns of nutrient storage and primary production by reducing the role of benthic macrophytes (seagrasses) and increasing the importance of pelagic phytoplankton communities?
· How does increased macroalgal biomass accelerate nutrient release from sediment pore waters underlying seagrass com munities, and how does this lead ultimately to seagrass die-off?
· What are the mechanisms for benthic-pelagic coupling of nutrients and primary production? How does increased nutrient availability mediate a shift in primary production from reef corals to macroalgal HABs?
· What are the existing nutrient inputs and their relationship to the initiation, growth, and maintenance of macroalgal blooms on the Florida Reef Tract? How does nutrient enrichment affect the early life histories of bloom-forming macroalgae?
For over 5 years, regions of the South Texas coast centered around the Laguna Madre have experienced a continuous, dense algal bloom referred to as the "brown tide." The nearly monospecific bloom has been caused by high densities (1-5 x 10 9 cells/L) of a small (4-5 µm diameter) chrysophyte similar to Aureococcus anophagefferens that causes brown tides on the U.S. northeast coast. Brown tide blooms occur in shallow (1-2 m depth) embayments and lagoons that have minimal advective transport and/or dispersion. The onset of the bloom was preceded by a drought (that increased the salinity) and severe freezes during periods of extremely low tides (Whitledge, 1993). Declines in invertebrate populations and widespread fish kills were associated with these conditions. High ambient concentrations of nutrients, especially nitrogen in the form of ammonium, resulted from the decaying fish. Ammonium is important because the Texas brown tide species cannot utilize nitrate (DeYoe and Suttle, 1994). Although bloom initiation depended on the increased ammonium, its persistence was facilitated by severe declines in grazer populations and continued low rates of advection and physical dispersion (Buskey and Stockwell, 1993). However, generalizations about nutrient effects, flushing, and trophic antagonism are not sufficient to predict the occurrence, persistence, or long term effects of the brown tide.
The environmental and economic impact of the Texas brown tide stems from effects on several components of the food -web. Zooplankton and larval fish do not eat the brown tide alga, but more importantly, after a threshold cell density is reached, their mortality increases. Eggs of important estuarine fish species (e.g., red and black drum, spotted seatrout) have reduced hatching and the young larvae rapidly die from lack of food. Large declines in the abundance of benthic filter feeders have also been observed. Exudate(s) from the brown tide organisms are thought to be responsible for these effects, but specific inhibitory compounds have not yet been identified. Another harmful effect of dense brown tides is a decline in the abundance of seagrasses due to light absorption by the microalgae. Severe long-term ecological changes thus result from the combination of loss of seagrass habitat and the reduced abundance of secondary consumers in the water and sediments. The economic losses to tourism and recreational fishing caused by the Texas brown tide are estimated to be several million dollars annually.
Important questions for future research include:
· To what extent do external nutrient sources and their elemental composition moderate brown tide blooms?
· What external or internal factors besides nutrient availability lead to the decline or dissipation of a brown tide bloom?
· To what extent do brown tide organisms modify environmental conditions so as to enhance their survival?
· What is the nature of the growth and feeding inhibition associated with brown tide blooms? Are toxins involved?
Pacific Coast Region (California and Oregon): PSP, ASP
Paralytic Shellfish Poisoning (PSP). Paralytic shellfish poisoning has a long history on the U.S. west coast, having been reported by early European explorers and coastal Indian tribes. The dinoflagellate, Alexandrium catenella is apparently the primary PSP producer in open coastal environments of the California and Oregon coasts, but relatively little is known about its bloom dynamics due to a lack of field surveys focused on this species. What little is known has been gleaned from shellfish -toxin monitoring programs (Price et al., 1991). In California, blooms of A. catenella cause toxicity nearly every year. PSP toxins are usually highest during July and August with most toxic events occurring from May to October. PSP is known to accumulate in numerous benthic filter feeders, and there is considerable variability among species with respect to toxin retention (Price et al., 1991).
Hydrographic mechanisms underlying the PSP problems along the west coast are poorly understood. A good case can be made that PSP outbreaks in some areas of California occur following the relaxation of seasonal upwelling. This moves offshore waters and their established dinoflagellate populations rapidly to the coast, causing increases in toxicity far faster than can be attributed to in situ growth alone. A similar mechanism linking shellfish toxicity to changes in upwelling condi tions has been reported for the northwest coast of Spain (Fraga et al., 1988), where hydrographic conditions resemble those along the northern California coast.
A number of questions underlying California and west coast PSP outbreaks remain to be resolved:
· Where are the source populations for the coastal blooms? If cysts are involved, where are the seedbeds located? Do blooms spread from one or a few points of origin or do isolated blooms develop simultaneously in several locations in response to similar hydrographic conditions? Do blooms originate in offshore waters, to be advected onshore with changes in meteoro logical conditions?
· What are the important meteorological or hydrographic forcings underlying toxicity in the different regions along the coast?
· If outbreaks are tied closely to transport of offshore waters and cells to coastal sites, can those events be detected and predicted using moored instruments and weather forecasts?
· What effect do recurrent blooms of toxic dinoflagellates have on west coast ecosystems, at all levels from zooplankton to fish and marine mammals?
Domoic acid-producing diatom blooms. Domoic acid poisoning (DAP) , associated with ASP in humans, first became a concern along the west coast of North America in September, 1991 when more than 100 brown pelicans and cormorants were found dead or suffering from unusual neurological symptoms in Monterey Bay, CA (Fritz et al., 1992; Work et al., 1993). This event was attributed to a bloom of the pennate diatom, Pseudo-nitzschia australis (Buck et al., 1992; Garrison et al.. 1992). At the peak of the 1991 bloom, domoic acid levels were >10 µg/L and P. australis reached over 106 cells/L. Since the 1991 autumn bloom, domoic acid has been detected in both autumn and spring plankton assemblages in Monterey Bay, but with domoic acid concentrations usually < 1-5 µg/L, and P. australis densities of 104 -105 cells/L. Blooms during the 1991-1994 period often have been comprised of two or three potentially toxic species (i.e., P. australis, P. pungens f. multiseries, and P. pseudodelicatissima); however, P. australis is believed to be the main source of the toxin. Domoic acid production from locally-isolated clones has only been confirmed for P. australis (Garrison et al., 1992) and P. pungens f. multiseries (Villac et al., 1993).
Monitoring studies in Monterey Bay suggest blooms of P. australis are most common and persist longer during the summer to autumn months (Buck et al., 1992; Walz et al., 1994). Hydrographic conditions during this period are characterized by warmer sea-surface temperatures, thermal stratification, and lower concentrations of organic nutrients. In contrast, P. australis blooms in southern California appear to be most common in the late spring to early summer months, and may be associ ated with upwelling pulses (Lange et al., 1994).
The 1991 domoic acid producing bloom in Monterey Bay was somewhat unusual because toxin was transmitted through the pelagic food-web via Northern anchovies to seabirds. Anchovies are also consumed by marine mammals, several finfish (Morejohn et al., 1978), and are occasionally eaten by human consumers. Domoic acid has also been found in other grazing zooplankton (Buck et al., 1992; Haywood and Silver, 1994). With the exception of seabirds, nothing is known of the effects or impact of domoic acid on the pelagic food-web.
It is difficult to assess the costs associated with the domoic acid blooms. In California, much of the cost of the domoic acid blooms is associated with the monitoring program conducted by the California Department of Health Services (Langlois et al., 1993) and U.S. Food and Drug Administration (FDA). The California Department of Health Services presently monitors domoic acid in conjunction with its established PSP monitoring program, using intertidal mussels as "sentinel" organisms. This strategy may prove to be inadequate because mussel monitoring is apparently not able to detect domoic acid when it is present in planktonic assemblages in low concentration (Walz et al., 1994). Mussel, rock crab, and razor clam harvesting is a small sport fishing activity in California and their monetary losses from blooms are difficult to assess.
Domoic acid-producing blooms are a relatively new phenomena in U.S. waters. Unanswered questions about these blooms include:
· What are the sources of domoic acid in West Coast waters? How many species of Pseudo-nitzschia are toxic? Are there other sources?.
· How is domoic acid production related to bacteria?
· Is domoic acid production in natural populations triggered by nutrient stress?
· How is domoic acid transported in marine food-webs? Are there effects on consumers at all trophic levels?
Other Potential HAB Problems. Dinoflagellate species (e.g., Dinophysis spp.) associated with diarrhetic shellfish poison ing (DSP), noxious bloom- forming species such as Phaeocystis pouchetii, and setose diatom species (e.g., Chaetoceros convolutus and C. concavicornis ), that damage gills of pen-raised finfish (see below) are found throughout the California Current region. Red-tides, apparently all caused by non-toxic species, are common during the summer months.
Questions related to potential HAB problems include:
· What are the effects of high-density, monospecific blooms of non-toxic "red tide" forming species on food-web structure?
· What are the occurrences and distributions of the potentially harmful species in California coastal waters?
· How are HAB species dynamics related to hydrographic events on short-term, seasonal, and interannual time scales?
· What is the importance of meso-scale features and short-term events on bloom dynamics?
· How do the life cycles of the HAB species influence their distribution and population cycles?
Pacific Coast Region (Washington): PSP, ASP, Finfish Mortalities
In the Pacific Northwest, public health and economic problems from HABs are related to paralytic shellfish poisoning (PSP), domoic acid poisoning (DAP), and mortalities of pen-reared salmonids; diarrhetic shellfish poisoning (DSP) is a poten tial but as yet unverified problem for the area.
Paralytic Shellfish Poisoning. Following the deaths of three people and mass mortalities of seabirds in 1942, the Washing ton coast from Dungeness Spit on the Strait of Juan de Fuca to the mouth of the Columbia River is closed each year from 1 April through 31 October for the harvest of bivalve molluscs. PSP was not a problem in Puget Sound until 1978, but since then, it has apparently spread southward with some closures now happening every year in central Puget Sound. The first closure in southern Puget Sound occurred in 1988 and in northern Hood Canal in 1991.
The causative organisms are members of the dinoflagellate genus Alexandrium. Species known from the area are A. catenella, A. acatenella, and A. tamarense . Two other potentially toxic species, A. ostenfeldii and A. hiranoi have been identified recently in British Columbia (Taylor and Horner, 1994).
Hydrographic mechanisms underlying the PSP problem in western Washington are poorly understood. There have been no sustained field programs, so bloom dynamics and physical forcings remain significant and important unknowns. PSP along the ocean coast and in coastal bays appears to be caused by blooms originating offshore. In Puget Sound, blooms originate in situ and toxicity may be widespread or very localized (Nishitani and Chew, 1988). A combination of physical factors and nutrient supply may explain why PSP has not been a problem in central and southern Hood Canal (Rensel, 1993). Some PSP outbreaks have been correlated with El Niño events (Erickson and Nishitani, 1985).
Economic impacts include the costs of shellfish and phytoplankton monitoring by state health officials, the closure of many beaches to the recreational harvest of shellfish during the summer months, and lost tourist trade. Commercial sales may be affected if the public thinks shellfish are contaminated. Recently, the harvest of non-traditional shellfish, such as predatory snails, has become a problem (Matter, 1994).
Important questions concerning PSP outbreaks in western Washington include:
· Where are the source populations for the blooms? Are cysts involved? If so, where are the seed beds?
· What meteorological or hydrographical forcings affect toxicity? Are outbreaks related to upwelling events or other transport of offshore waters and cells to coastal areas? Can those events be detected/predicted? What hydrographic conditions are necessary for blooms in inland waters?
· Do nutrients regulate/limit blooms in some areas?
Amnesic Shellfish Poisoning. Domoic acid was first found in razor clams on the Oregon/Washington coasts in late October 1991, and both commercial and recreational harvests of razor clams were halted. Other bivalves, including comercially grown oysters and mussels were tested and did not contain the toxin. However, domoic acid was also present in the viscera of Dungeness crabs and their commercial harvest was closed for a short time. Since 1991, the fall and spring recreational seasons for razor clams have been delayed, shortened, or not opened due to domoic acid. Furthermore, depuration of domoic acid from razor clams is apparently slow (Drum et al., 1993; Horner et al., 1993). In November 1994, domoic acid was found for the first time in mussels from southern Hood Canal.
The causative organisms have not been identified with certainty, but it has been assumed that species of the diatom genus Pseudo-nitzschia are to blame. Known toxin-producing species present in Washington waters include P. australis, P. pungens f. multiseries , and P. pseudodelicatissima. Both P pungens f. pungens and P. pungens f. multiseries were present in the bloom in Hood Canal when domoic acid was found in mussels.
As with PSP, hydrographic conditions related to domoic acid occurrence are not known. Pseudo-nitzschia spp. are rarely seen in samples collected in nearshore waters when razor clams are most toxic, but perhaps the cells originate offshore and are advected to the coast. There has been no offshore sampling since the 1991 incident. It is possible that a series of Pseudo-nitzschia blooms occurred, extending from California to Alaska, linked to unusually warm weather conditions associated with an ENSO event in 1991.
The 1991 domoic acid incident caused an estimated $15 - $20 million in damages to the Oregon/Washington coastal economy. Losses included health effects, lost and/or delayed sales, lower prices, lost jobs, bankruptcies, and lost recreational opportunities and tourist trade. No estimate is available for losses since 1991.
Unanswered questions with regard to domoic acid and ASP include:
· What are the causative organisms? Are Pseudo-nitzschia spp. the only ones involved or are other diatoms and/or macroalgae also culprits?
· What is the source of the organisms? Is there an offshore bloom that is advected to inshore localities? In Puget Sound, are there local seed populations in some areas?
· What is the life cycle of the Pseudo-nitzschia spp.?
· What environmental conditions are needed for domoic acid production by the cells?
· How do the razor clams and Dungeness crabs obtain domoic acid? How long does it take them to depurate domoic acid? Under what conditions?
· Has the Washington incident been one event with slow depuration or is there continual reintoxication?
Finfish Mortalities. Catastrophic losses of cultured and wild fish sometimes occur due to species of phytoplankton that do not cause illnesses in humans. Blooms of the raphidophyte flagellate Heterosigma carterae (sometimes called H. akashiwo or, erroneously, Olisthodiscus luteus ) have occurred in British Columbia every year since the early 1960s and fish kills have been reported most years since 1986; in Washington, fish kills occurred in pen-reared fish in 1989 and 1990, and wild fish in 1994. Losses to the fish growers are about $4-5 million per year when blooms occur. The way Heterosigma kills is not known, but superoxide radicals may be involved because fish can be protected with the addition of superoxide dismutase (Yang et al., 1993). This organism is a vertical migrator, usually occurring in surface waters during the day and at depth during the night. Vertical stability of the water column is probably an important factor in maintaining blooms.
The harmful diatom species Chaetoceros concavicornis , C. convolutus, and perhaps C. danicus have long setae armed with short secondary spines and may kill at fairly low concentrations (<10 4 cells/L). Chains of cells apparently become lodged between secondary lamellae in the fish gills and cause blood hypoxia as a result of mucus production. These diatoms may be restricted to near-surface waters or mixed throughout the water column depending on local hydrographic conditions. Most fish growers have their own phytoplankton monitors who sample at the pen sites on a daily basis from April through Septem ber. They also rely on reports from other phytoplankton monitoring programs. Economic losses are about $0.5 million per event.
Unanswered questions here include:
· What environmental conditions cause blooms of Heterosigma?
· Does Heterosigma produce a toxin? If so, what is it? How does it kill the fish? What environmental conditions are needed for toxin production?
· Are fish killed by Heterosigma safe to eat?
· Are Chaetoceros concavicornis and C. convolutus the only Chaetoceros species that kill fish or can any species with second ary spines (e.g., C. danicus) or capilli (long, hairlike siliceous spines, e.g., C. radicans) on the setae kill fish?
· Can harmful Chaetoceros species and/or other harmful phytoplankton species influence the distribution and abundance of finfish in inland waters of Washington State?
· What environmental factors affect the timing and magnitude of harmful Chaetoceros blooms in inland waters?
· Are phytoplankton associated with summer mortality of finfish? If so, which species?
Other HAB problems. Ceratium fusus and Gymnodinium sanguineum have been linked to mortality of oyster larvae and adults (Cardwell et al., 1977, 1979) and spot prawns (Rensel and Prentice, 1980) in southern Puget Sound. There is no indication of a chemical toxin and mortality may be due to mechanical means or oxygen stress when blooms decay.
The major questions for these species are:
· How do they cause mortality?
· How often do they cause shellfish mortality? Could these dinoflagellates, or other phytoplankton species, be implicated in summer mortality of oysters?
Pacific Coast Region (Alaska): PSP, ASP, Bitter Crab Disease
Alaska, with 54% of the U.S. coastline, has a significant problem managing the impacts of HABs. Although some baseline information is available, virtually all studies have been either of short duration and/or restricted to small geographic areas. No studies have critically and specifically evaluated HABs on a broad geographic scale.
Paralytic Shellfish Poisoning. PSP is the most significant HAB problem in Alaska. Numerous beaches, bays, and coves in the southeast and east are periodically or perpetually plagued with high levels of saxitoxins in blue mussels, butter, little necks, and horse clams, geoduck, oysters, and cockles. Commercially valuable crabs are also affected. The causative species is apparently Alexandrium catenella, but other toxin-producing species may also be present. Toxic blooms have been reported in almost every month of the year, making it difficult to ascribe bloom conditions to any particular environmental or hydrographical condition. One frequently reported trend is that shellfish from headwaters of estuaries have more toxin than those collected near the mouths, perhaps suggesting that blooms originate or grow better near the headwaters. It is certainly possible that the rising tide or certain wind patterns may push toxic algae into shallow areas, but there is a growing perception that blooms originate offshore and move inland. Despite the prevalence of PSP, large areas of the coast remain relatively free of toxins.
In 1917, 5 million pounds of shellfish products were harvested from Alaskan waters, but today the state's commercial bivalve industry is virtually nonexistent. The destruction of the clam industry, estimated at 25-50 million pounds of bivalves per year, is in large part a result of product contamination by PSP (Neve and Reichardt, 1984). Other commercially valuable species, such as Dungeness crabs, are also affected by PSP, presumably from consumption of tainted bivalves. Other economi cally valuable crustaceans have not tested positive for PSP.
Only commercially harvested shellfish are presently tested for PSP on a routine basis. Recently, the Alaska Department of Conservation (DEC) instigated a multicomponent program to detect PSP and identify blooms. The program relies on local fish farmers trained to identify toxic dinoflagellates from their swimming patterns, satellite imagery to identify and track blooms, and a citizen monitoring program with an 800 number for reporting PSP illnesses, discolored water, fish kills, unusual behavior of seabirds or mammals, etc. This program needs to be coupled with physical, chemical, and biological oceano graphic studies being conducted on the coast to provide insights into bloom formation, spread, and collapse.
Questions that need to be answered with regard to PSP in Alaska include:
· What algal species are involved?
· What are their seasonal and geographic distributions?
· What hydrographic and environmental factors contribute to blooms?
· What information is needed to guide the development of a shellfish industry in a region with extensive PSP problems?
Domoic Acid. Alaska does not have a severe problem with domoic acid, but low levels have been found in razor clams and Pseudo-nitzschia pungens and P. australis have been found in Alaskan waters. Whether they produce domoic acid is not known.
While domoic acid is not yet a problem in Alaska, some questions are still pertinent:
· Do blooms of Pseudo-nitzschia occur in Alaskan waters? Are any of the populations toxic?
· What are the seasonal and geographic distributions of Pseudo-nitzschia spp., and what controls their abundance and toxic ity?
Other potential HAB Problems. Phaeocystis blooms occur occasionally in Alaska, and under conditions that are not well understood. This alga can be a major component of the spring bloom or form a second, smaller bloom later. It produces both acrylic acid and DMSP, but the ecological and environmental impacts of these compounds are not known. Southeastern Alaska shares with Washington State the presence of several potentially harmful diatoms, e.g., Chaetoceros convolutus and C. concavicornis , however no problems have been associated with these species, since fish farming is not yet a major industry..
A parasitic dinoflagellate, Hematodinium sp., has been of increasing concern since 1985 because it causes "bitter crab" disease. The parasite infects crabs during their molt (Love et al., 1993; Meyers et al., 1987). Once established, it is 100% lethal and the crab meat becomes unmarketable before the crabs die.
Questions with regard to Phaeocystis and Hematodinium include:
· How extensive are the blooms, and what hydrographic/environmental factors favor them?
· What are the economical/societal costs of Phaeocystis blooms?
· What oceanographic conditions favor growth and survival of the parasitic Hematodinium sp. during its life cycle when it is not within the host Tanner crab? What natural controls are there to Hematodinium abundance?