The Scottish Government

« Previous | Contents | Next »

Listen

4.0 ALEXANDRIUM BLOOMS AND PARALYTIC SHELLFISH POISONING

4.1 Nature of Paralytic Shellfish Poisoning ( PSP)

Ten of the 30 recognized species of the dinoflagellate genus Alexandrium produce neurotoxic paralytic shellfish toxins ( PST), three of which have been recorded in Scottish coastal waters: Alexandrium minutum, Alexandrium ostenfeldii and Alexandrium tamarense (Table 4). Gymnodinium catenatum and Pyrodinium bahamense var. compressum also produce PST, but neither has been reported from Scotland. Of these, Gymnodinium catenatum is a major bloom species along the Iberian peninsula (Hallegraeff and Fraga, 1998); P. bahamense var. compressum is confined to the Pacific Ocean. The taxonomy of Alexandrium is still being resolved. Morpho- and geno-species and their various intergrades confound Alexandrium taxonomy. It is often necessary to refer a particular bloom episode to species complex, such as the Alexandrium tamarense / catenella / fundyense "species complex", rather than to a particular species (Scholin, 1998).

Table 4.Alexandrium species reported to produce paralytic shellfish toxins ( PST).

⁺ reported in Scottish coastal waters

At least 21 derivatives of the parent compound, saxitoxin ( STX), occurring in various combinations and concentrations have been associated with paralytic shellfish poisoning (Cembella, 1998; Landsberg, 2002). These include the carbamate toxins, neosaxitoxin ( NEO) and the gonyautoxins ( GTX1-4). Their decarbomoyl ( dcSTX, dcNEO, dcGTX1-4) and deoxycarbomoyl analogues ( doSTX, doGTX2-3) are of intermediate toxicity. The structural chemistry of PST is very complicated, and further altered as PST are vectored through the food web. PST are highly lethal: thay have an LD ₅₀ in mice (intraperitoneal injection) of 10 µg kg ^-1, which is a 1,000-fold more toxic than sodium cyanide, which has an LD ₅₀ of 10 mg kg ^-1 (Landsberg, 2002).

PSP-induced human illness and death accompany consumption of toxic shellfish and, on occasion, gastropods and crustaceans and, more rarely, toxic fish. PST are potent neurotoxins that affect the sodium channel, blocking the influx of sodium and restricting signal transmission between neurons. Clinical symptoms of PSP include paresthesia, facial numbness, nausea, dizziness, among others, and, in high doses, respiratory paralysis and death can result (see Hallegraeff, 1993). More relevant to the present review is the extent to which blooms of PST-producing Alexandrium spp. in Scottish coastal waters may be stimulated by fish farm activities and, conversely, compromise mariculture and the indigenous biota in these waters. Fish farm phytostimulation of blooms is considered in Section 10.

Toxic Alexandrium spp. typically produce more than one STX derivative, but no single strain is known to synthesize the entire suite of saxitoxin and its 21 derivatives (Cembella, 1998). Nor is a species' toxicity fixed; toxic and non-toxic strains occur, as found with A. tamarense strains isolatesd from UK waters (Higman et al., 2001). Cellular toxin levels and composition vary with life cycle stage, irradiance, temperature and (particularly) nutritional status. PSP toxins are N-rich compounds (ca. 30% by weight). In highly toxic strains of A. tamarense, A. minutum and G. catenatum, as much as 5 to 15% percent of the total cellular N is bound in PST (Cembella, 1998). Phosphorus (P) appears to be more important in toxin biosynthesis even though it is not contained in PST molecules. Toxicity of Alexandrium cells, for example, often increases during P-limitation (see Cembella, 1998). This importance of P in the expression of toxicity during dinoflagellate blooms in coastal waters is surprising given the traditional view that coastal waters are N-limited. [The question of whether harmful ( PSP toxic) dinoflagellate blooms are under closer regulation by P than diatom blooms is unresolved.] There is some evidence that intracellular bacteria may be sources of the PST found in dinoflagellates (see Landsberg, 2002).

It is important to recognize that the factors controlling blooms of PSP toxic dinoflagellates most likely differ from those that control PST synthesis. Blooms are stimulated responses, e.g. result from adequate irradiance, nutrients and reduced grazing, while toxicity is often the result of stress or inhibition of growth, e.g. nutrient limitation.

PST is ingested by ciliates, zooplankton and benthic filter-feeders when grazing on dinoflagellates, when not lethal, and vectored to higher trophic levels. Zooplankton play a major role in the initial vectoring step, although exposure to PST can be lethal to copepods, elicit avoidance reactions, repress grazing, or have other adverse effects (Huntley, et al., 1986; Ives, 1985; Teegarden and Cembella, 1996a; White, 1979; 1981a,b). Since PSP illness of humans usually results from eating shellfish, it is usually assumed that bivalves are not affected by the high levels of STX that they can accumulate. This view has a neurological basis: neuromuscular functions in bivalves are regulated by calcium channels, whereas the neurotoxicity of STX results from its sodium channel blocking activity (Landsberg, 2002). However, bivalves exposed to high levels of PST exhibit a variety of behavioral and physiological stress responses (Shumway, 1990), and even mass mortality. Mass mortality of molluscs occurred during toxic blooms of A. catenella (Horstman, 1981) and A. tamarense (Adams et al., 1968; Ingham et al., 1968), the latter dieoff occurring around the Farne Islands. In contrast, crustaceans, including crabs and lobster, appear to escape ill affects when exposed to PST (see Landsberg, 2002).

Fish were once considered not to suffer adverse effects when exposed to PST (Prakash, 1971). Some examples from the literature show that this is not the case. First feeding and late larval stages of many fish species depend nutritionally on dinoflagellates. The larvae of 15 of 20 fish species collected from natural populations began to feed on dinoflagellates while still in their yolk sac stage, with herring, sprat and sand lance continuing to feed on dinoflagellates until reaching 8 mm in length (Last, 1980). The larvae of at least seven commercially important species died after ingesting toxic dinoflagellates (see Smayda, 1992). Recurrent kills of Atlantic herring ( Clupea harengus harengus) in the Gulf of Maine, and mortality of larval herring, capelin and red sea bream, and other adverse physiological and behavioral responses of fish during experimental exposure to A. tamarense or as a result of toxin vectoring during its blooms have been documented (White, 1977, 1980, 1981a,b; 1984, White et al., 1989). The LD ₅₀ for herring, cod, flounder, pollock and Atlantic salmon is 4 to 12 µg STX per kg body weight, when introduced intra-peritoneally. Shellfish, in contrast, commonly accumulate 6,000 µg toxin per 100 µg body weight without physiological impairment; i.e., a body burden about 5,000 times greater than that tolerated by fish and other vertebrates (White, 1984).

Over evolutionary time scales, regional fish spawning strategies, i.e. migrations, were probably influenced by whether or not toxic blooms were encountered within this migratory range and period (Gosselin et al.,1989). Recurrent larval dieoffs during toxic blooms would provide selective pressure to evolve bloom avoidance strategies. In regions where toxic blooms are new events or have become more frequent, recruitment may be compromised because the locally effective spawning and feeding strategies developed may no longer confer protection against synchronous spawning with toxic bloom events. In agreement with Gosselin et al., there is reason for concern that the present global expansion of toxic blooms may threaten larval survival and recruitment in some coastal fisheries by " narrowing the spatio-temporal window" within which sucessful spawning and recruitment can occur.

The derivative question is whether fish farming operations in Scottish coastal waters increase this potential. Stagg et al. (1998), who evaluated the 96 hr LD ₅₀ of farmed Atlantic salmon ( Salmo salar) injected with saxitoxin, suggested that PST is poorly metabolized. This incapacity, combined with loss of vagility of penned fish, would make them vulnerable to PST blooms. Farmed fish are vulnerable not only to naturally occurring harmful blooms, but blooms that might be stimulated by fish farm operations via a feedback loop of excreted nutrients stimulatory to toxic blooms that are then harmful to the farmed fish. This prospect is considered in more detail in Section 10 which deals with fish farms and harmful algal blooms ( HABs).

4.2 Toxic Alexandrium species and PSP in Scottish coastal waters

Alexandrium tamarense is the major species of the three toxic Alexandrium spp. recorded in Scottish waters; A. minutum and A. ostenfeldii are infrequently reported. The following section summarizes the main occurrence patterns and blooms reported for these species in the waters of Scotland and contiguous UK and Northern Ireland, including descriptions of major PSP outbreaks. Alexandrium bloom behavior elsewhere in European waters, and additional discussion of A. tamarense dynamics in Scottish waters are presented in the section Scottish Coastal Waters as Open Systems [Section 11].

4.2.1 Alexandrium tamarense

Paralytic shellfish poisoning has occurred in the waters off west and east Scotland (Figure 7; Wyatt and Saborido-Rey, 1993; Tett and Edwards, 2002) and Belfast Lough in Northern Ireland (Ayres et al., 1982; McCaughey and Campbell, 1992; Taylor et al., 1995). PSP outbreaks elsewhere in the UK are relatively rare despite the widespread presence of A. tamarense, the species considered to be the cause of these PSP episodes. PSP toxicity and the presence of A. tamarense in Republic of Ireland coastal waters were first observed in 1996, in Cork Harbour (Furey et al., 1998). The first toxic A. tamarense bloom in Spain occurred in 1984 at a shellfish cultivation site (Blanco et al., 1985).

Although there is a long history of episodic PSP outbreaks in Scotland, and occasionally of high intensity, they are rather infrequent. A PSP outbreak may have occurred in 1827 following consumption of mussels collected from the Firth of Forth (Berry, 1997; Combe, 1928). Thereafter, excluding a minor episode recorded near Glasgow in 1958 (Gemmill and Manderson, 1960), PSP toxicity of shellfish was not reported until May, 1968 (Wyatt and Saborido-Rey, 1993). A major PSP outbreak then developed: 78 clinical cases were recorded among those who consumed mussels ( Mytilus edulis) harvested from Budle Bay located north of Newcastle-upon-Tyne (Figure 7A; Ayres and Collum,1978; Wyatt and Saborido-Rey, 1993). Alexandrium tamarense was identified as the bloom species (Robinson, 1968). The 1968 outbreak sparked the initiation of weekly (approximately) monitoring (from March to August) for paralytic shellfish toxins ( PST) in mussels collected at 15 to 20 sites along the east coast between Aberdeen and Bridlington, 57°N to 52°N (Ayres and Collum, 1978). In the subsequent 23-year period, from 1968-1990, the quarantine level was exceeded 17 times, without reports of clinical PSP cases (Wyatt and Saborido-Rey, 1993).

The monitoring programme revealed that the time of the first appearance of PSP within years was variable; it could begin as early as mid-March or not until late-June, with May the predominant month of first occurrence (see Table 1 in Joint et al., 1997). The geographical location of the first record of PSP in each year also varies along the 300 km coastline where the monitoring stations were positioned. In 1968 and 1975, significant mortality of sea birds (shags, cormorants, fulmars) occurred in the Farne Islands attributed to vectoring of PST through the food web (Armstrong et al., 1978; Coulson et al., 1968). In June-August 1990, an unusually intense, regional bloom of A. tamarense and PSP outbreak developed along the north east coast of the U.K., western Scotland and Northern Ireland (Wyatt and Saborido-Rey, 1993; Joint et al., 1997). The geographic extent of this PSP outbreak was the greatest recorded during the 1968 to 1992 monitoring years. Initially, A. tamarense bloomed almost synchronously along a 300 km stretch of coastline extending south to the Firth of Forth (Joint et al., 1997). It then spread northwards along the Banff coast and Highlands Sounds (Figure 7A), resulting in the first PSP outbreak recorded for that region. In the waters of western Scotland, between Tiree and the Sound of Sleat, extremely high toxicity (11,000 to 16,500 MU 100 g ^-1) was found in the Loch Ardtoe and Loch Kentra mussel populations two months after bloom initiation in north-east Scotland (Wyatt and Saborido-Rey, 1993). Substantial levels of toxin were also detected in shellfish and some crabs in the region between Ardnamurchan and Little Loch Broom. The high PST levels in bivalves and crustaceans persisted into 1991 along the north-west coast (Tett and Edwards, 2002). In Belfast Lough, Northern Ireland, high toxicity levels were found in early July.

The widespread distribution of toxic mussels, whose PSP levels exceeded quarantine levels, is shown in (Figure 7B). Toxicity was not limited to mussels; low level PSP toxicity was detected in scallops, crabs, lobster and prawns. This diverse faunal intoxication is another unusual feature of the 1990 PSP outbreak (Wyatt and Saborido-Rey, 1993). Mortality of farmed salmon does not appear to have accompanied the PSP outbreaks and A. tamarense bloom events in Scottish waters, based on the literature reviewed. In contrast, an A. tamarense bloom (reported as Gonyaulax excavata) in the Faroe Islands caused 77% mortality of the farmed salmon population, PSP toxicity of mussels, and mortality of wild flat fish and whelks (Mortensen, 1985).

The environmental trigger(s) of the 1990 PSP bloom is unknown, but the bloom pattern suggests an overriding regional stimulus. While the accumulation of PST by mussels was favored by neap tides, periods of weak winds and, perhaps, runoff, this combination does not fully explain the 1990 event (Wyatt and Saborido-Rey, 1993). An anomalous weather pattern during the 1990 spring/summer through its affect on regional hydrography may have been a factor in addition to the locally altered biological (e.g. grazing) and/or chemical (e.g. nutrient enrichment) conditions. That is, the 1990 bloom might have commenced and persisted under meteorological stimulation, and facilitated by the advection and regional seeding of bloom starter populations. However, the bloom, which began more or less synchronously in north-east coastal waters, developed much later off western Scotland. This spreading from east to west is contrary to the expected direction of transport based on the prevailing west to east flow of the coastal currents (see Figure 4 in Rydberg et al., 2002). This opens the possibility that the 1990 PSP outbreak was actually the result of two separate bloom events, an eastern and a western outbreak linked more by their temporal continuity than spatial coherence. This is not to say that A. tamarense is not indigenous or widely distributed in the waters off western Scotland, or that its blooms develop there allochthonously rather than as the responses of local populations. Alexandrium tamarense is widely distributed in east and west Scottish coastal waters beyond the occurrences noted during the 1990 bloom (Figure 7A), including Orkney (Wilkinson, 1975), the Sound of Jura, the entrance to Loch Sunart, Loch Eriboll (Dodge, 1995), the Firth of Clyde and Kyle of Tongue, with deposits ("seed banks") of resting cysts found in Loch Creran. "Seed banks" are symptomatic of a year-round presence. A cyst survey in 1992 revealed two major cyst "seed banks" in the region between Aberdeen (57°03'N) and Flamborough Head (54°05'N): in the Firth of Forth, and between Aberdeen and St. Andrew's Bay (Lewis et al.,1995). The importance of the Firth of Forth "seed bank" in seeding blooms to the south along the coast of England is debated (Brown et al., 2001; Joint et al., 1997).

Following its 1990 bloom, A. tamarense was recorded (1991-1993) in low abundance in Loch Eriboll (Dodge, 1995), and (1996-1997) at other west coast sites (Tett and Edwards, 2002). During the 1990s, PSP continued to be found regionally in west coast shellfish, from the Firth of Clyde to the Kyle of Tongue. In Loch Hourn, saxitoxin levels in May, 1997 slightly exceeded the closure threshold standard. It is not possible to evaluate the causes of these minor PSP episodes from the data available. Some aspects of the general physiology and bloom dynamics of Alexandrium spp. have been reviewed by Anderson (1998).

In summary, despite periodic major PSP outbreaks, as in 1968 and 1990, PST levels exceeding threshold levels and requiring closure of shellfishing grounds are relatively infrequent and brief in duration (Tett and Edwards, 2002; Joint et al., 1997). Unlike in western Scotland, however, in the Orkney Isles shellfishery closures are required in most years (Tett and Edwards, 2002). PSP outbreaks there, and generally in Scottish waters have been linked inferentially to A. tamarense since this species generally is believed to be the only toxic Alexandrium present in Scottish coastal waters (Wyatt and Saborido-Rey, 1993). Recent studies, however, indicate that A. minutum (= A. lusitanicum) and A. ostenfeldii, both PSP toxigenic, are widespread at the Orkney Islands where increased PSP toxicity of mussels has coincided with increasing Alexandrium abundance (Töbe et al., 2001). The occurrence of these species has been attributed to advection from oceanic sites (Hummert et al., 2001). However, since A. minutum, A. ostenfeldii and A. tamarense are common in nearshore waters, and there "seed beds" of Alexandrium cysts (species unstated) in Orkney coastal waters (Töbe et al., 2001), these species are probably indigenous there. While A. tamarense is undoubtedly the primary PSP-producing species in the contiguous waters of Scotland, England and Northern Ireland, A. minutum and A. ostenfeldii have some unique ecophysiological features that warrant comment.

4.2.2 Alexandrium minutum

Alexandrium minutum had been conspicuously absent among the harmful dinoflagellate species reported for Scottish coastal waters until a recent, ambiguous report that it occurs in Orkney Isle waters (Töbe et al., 2001). The life cycle stage in which it was found is not clearly stated by Tobe et al. Those investigators appear to have found motile, vegetative cells; they mention having examined sediment deposits of resting cysts produced by unidentified Alexandrium spp. The stage(s) in the life cycle in which A. minutum was present is significant, given this first report of its occurrence in Scottish waters. If resting stages were found, a locally established population is probable. If found in its motile vegetative stage only, the population may be either of local origin or advected into local waters as a visiting species. While Töbe et al. puzzled over the source of A. minutum, Hummert et al. (2001) attributed its occurrence to advection " from oceanic waters", an unlikely source since A. minutum is a coastal species. Alexandrium minutum has been reported in the ballast of ships visiting Scottish ports, from which inoculation into local waters might occur (Macdonald and Davidson, 1998). This is discussed in greater detail in the section dealing with ballast water introductions [Section 11.2].

Although it is an open question whether an A. minutum population is established in Orkney waters, such an expansion into Scottish waters , if not already achieved, is not unrealistic. The following summary of A. minutum autecology is presented based on the assumption that either it is, or shall become present in these waters.

Alexandrium minutum, originally described from eutrophicated Alexandria Harbor, Egypt (Halim, 1960), and conspecific with Alexandrium lusitanicum, appears to be expanding its range within European waters (Nehring, 1998), and perhaps globally (see deSalas et al., 2001). Since 1985, it has produced persistent blooms along the north-west coast of Brittany, especially in small bays and shallow estuaries, causing severe losses to aquaculture and producing "red tides" reaching 3 million cells L ^-1 (see Erard-LeDenn, 1991). Alexandrium minutum has also been found off the coasts of Norway, Spain (1985-1987) and The Netherlands (1992) (see Erard-Le Denn, 1991). In 1987, it produced a toxic bloom in Irish coastal waters (Cork Harbor) (Gross, 1989). Between 1956 to 1994, after which it disappeared, A. minutum was a recurrent summer bloom species in the eutrophicated waters of Alexandria Harbor, sometimes accompanied by massive fish kills during its prodigious blooms (up to 24 x 10 ⁶ cells L ^-1) (Ismael and Halim, 2001).

The emergence of toxic A. minutum as an important HAB species in European coastal waters, and elsewhere, has focused interest in the mechanisms of its regional expansion, and the habitat features that favor its blooms. In Kastela Bay, Croatia, one of the most heavily eutrophicated areas within the Mediterranean Sea, A. minutum first appeared in 1989 and then bloomed in 1992 (Marasovic et al., 1995). In the Adriatic Sea, A. minutum was first reported from the nutrient-enriched, Po river plume (Honsell, 1993). Among Alexandrium species, therefore, A. minutum shows a preference for nutrient enriched habitats where it can achieve great abundance. Nonetheless, very high nutrient levels do not appear to be a bloom prerequisite given its blooms elsewhere during upwelling events (Chang et al., 1996) and in habitats of low nutrient concentration (Hallegraeff et al., 1988). A. minutum appears to have a very wide niche.

Hallegraeff et al. (1988) believed that the putative regional and global expansions of A. minutum have resulted from bio-invasions facilitated by ballast water conveyance, and specifically into Australian waters. More recent molecular evidence suggests that the Australian and New Zealand populations (ribotypes) are indigenous, although partial genetic and toxicological similarities with European strains of A. minutum keep open the possibility that one or more introductions of A. minutum into Australian waters from Europe [Mediterranean] may have also occurred and introduced another ribotype (de Salas et al., 2001).

Based on the limited, available evidence, A. minutum does not appear to pose a significant threat to cultured and natural fish and shellfish stocks in Scottish coastal waters. It is recommended that surveys of Orkney coastal waters in search of this species to confirm its presence should be undertaken.

4.2.3 Alexandrium ostenfeldii and the toxin spirolide

Alexandrium ostenfeldii is widely distributed in European waters, including Iceland, Faroe Islands, Norway, Denmark and Spain (see MacKenzie et al., 1996). Its cysts are often abundant in "seed banks" (MacKenzie et al., 1996), but its pelagic stage is rare. The latter suggests that A. ostenfeldii is a member of the "hidden flora" capable of precipitous, aperiodic blooms in response to unknown environmental stimulation. In Nova Scotian waters, A. ostenfeldii occurs cryptically in sub-surface aggregations at relatively low abundance (<4,000 cells L ^-1) Cembella et al., 2001). Its low pelagic population levels are enigmatic given the abundant "seed bank" deposits of its resting cysts that are available for germination and bloom initiations.

Alexandrium ostenfeldii is also unique among Alexandrium spp. in its toxin composition. In addition to producing PSP toxins (Jensen and Moestrup, 1997), A. ostenfeldii produces toxic spirolides, first reported in the early 1990s. Spirolides are " fast acting toxins" present in lipophilic extracts of scallop and mussel viscera harvested from aquacultural sites in Nova Scotia (Cembella et al., 2000, 2001). Spirolides are pharmacologically active macrocyclic imines having many derivatives; their chemical structure is given in Cembella et al. (2001). Biosynthesis of these polyketide-derived metabolites is governed by light dependent events during the cell division cycle (John et al., 2001).

In coastal Nova Scotian waters, spirolides and PSP toxins and the respective sources of these toxins, A. ostenfeldii and the closely related species, A. tamarense, can co-occur, an overlap considered coincidental rather than successional (Cembella et al., 2001). Both species have occurred regularly in Danish fjords since the mid-1980s, sometimes causing closure of shellfish harvesting areas (Jensen and Moestrup, 1997). Of the two species, A. tamarense is ecophysiologically more robust, more abundant, may have less fastidious growth requirements, and has a faster growth rate: µ = ca. 1.0 d ^-1 vs. 0<0.35 d ^-1 for A. ostenfeldii (John et al., 2001; Jensen and Moestrup, 1997). Given this, when both species co-occur during a toxic PSP event the contribution of A. ostenfeldii may be difficult to establish (see John et al., 2003). Where A. ostenfeldii occurs alone, its low abundance and associated spirolide toxicity may be overlooked.

In Scotland, A. ostenfeldii is presently known only from Orkney (Töbe et al., 2001; John et al., 2003), but is expected to be more widely distributed in Scottish waters. It may have been routinely overlooked because of its low planktonic population densities and cryptic occurrence as a "hidden flora" species. Habitat conditions in Scottish waters are similar to those at its known bloom sites in Nova Scotia and in Spanish rîas (Fraga and Sanchez, 1985). Shellfish aquaculture at those sites possibly contributes to its blooms. The occurrence of A. ostenfeldii in Icelandic and Faroese waters also makes it likely that it is much more widely distributed in Scottish waters than currently documented. This expectation has been strengthened by the recent discovery of high spirolide concentrations in the surface waters off the east coast of Scotland (Figure 8; Rühl et al., 2001; John et al., 2003). Spirolides were also commonly detected during a survey in May, 2000 conducted along 12 onshore - offshore transects extending from Orkney to south of the Firth of Forth. Alexandrium ostenfeldii was the most probable source of the spirolides, since it is the only proven producer of this metabolite based on laboratory studies on A. ostenfeldii strains isolated from Limfjord, Denmark (Cembella et al., 2000) and Nova Scotia (John et al., 2001). The extent to which spirolides adversely effect the natural biota, particularly shellfish, and fish farming in Scotland is unknown. Further evaluation of spirolide presence and A. ostenfeldii occurrence in Scottish waters is recommended, an inquiry having added significance since A. ostenfeldii is also a PST producer.

« Previous | Contents | Next »