« Previous | Contents | Next »
Listen
5.0 BLOOMS OF OTHER HARMFUL DINOFLAGELLATES IN SCOTTISH COASTAL WATERS
5.1 Karenia mikimotoi ( Gyrodinium aureolum)
Of the 23 HAB species recorded from Scottish coastal waters (Ayres et al., 1982), only two have been reported to have caused local fish kills: Karenia mikimotoi (= Gyrodinium aureolum, = Gymnodinium nagasakiense, = Gymnodinium mikimotoi) and Flagellate X (Gowen, 1987). [See, however, Rae et al. (1965]. The taxonomic status and toxicity of the Flagellate X complex are discussed in Section 6.2. Recurrent blooms of ichthyotoxic K. mikimotoi, identified initially as Gyrodinium aureolum and later as Gymnodinium nagasakiense, have caused mortality of wild and farmed fish and benthic invertebrates in European coastal waters. Mortality of farmed fish in Norway, south-west Ireland and Scotland, and shellfish mortality in Ireland has accompanied its blooms. In Donegal Bay, an 80% mortality of farmed clams ( Tapes semidecussata) occurred during a 1992 bloom of K. mikimotoi (<10 6 cells L -1) (O'Boyle et al., 2001). In 1995, a K. mikimotoi bloom along the French Atlantic coast caused mortality of 800-900 tonnes of Mytilus edulis (Gentien, 1998). Similarly, blooms of K. mikimotoi there caused mass mortality of post-larval stages of Pecten maximus, stopped the growth of juvenile stages and reduced both growth and reproduction of adult scallops (Erard-LeDenn et al., 1990). K. mikimotoi must be recognized as posing a major threat to aquaculture in Scotland, both to farmed salmon and, particularly, to the burgeoning shellfish cultivation despite an insignificant adverse impact to date. Its autecology and local habitat conditions, as discussed below, predispose Scottish coastal waters to harmful bloom episodes of K. mikimotoi under appropriate combinations of meteorological and hydrographic conditions. The remarkable 1990 bloom of A. tamarense discussed earlier is a useful model of this potential.
K. mikimotoi was first recorded in 1966 in European coastal waters from a southern Norwegian fjord (Braarud and Heimdal, 1970), and has become one of the commonest dinoflagellates found in northern European waters, having spread throughout the North Sea, eastern Irish Sea, Celtic Sea, western English Channel and Scottish coastal waters (Partensky and Sournia, 1986). Its origins are obscure. K. mikimotoi was initially misidentified as its look-alike species, Gyrodinium aureolum. Since the only known bloom site of G. aureolum was (and still is) a coastal salt pond located in southern New England, USA (Hulburt, 1957), its presumed bioinvasion of northern European waters was attributed to trans-Atlantic dispersion by an unknown mechanism. Recently, Hansen et al. (2000) concluded that the European populations and cultured strains identified both as K. aureolum and G. nagasakiense are conspecific with G. mikimotoi, originally described from, and found in Japanese waters. K. mikimotoi is now generally accepted to be the species previously reported as G. aureolum in European coastal waters.
Its cosmopolitan distribution notwithstanding, it is unresolved whether K. mikimotoi was introduced into the North Sea from an unknown location, as Elbrächter (1999) has concluded, or whether it was resident within this region as a member of the "hidden flora" prior to its precipitous appearance off the Norwegian coast in 1966. Should it have been indigenous, the question (still unresolved) becomes: what factors triggered its bloom and facilitated its subsequent dispersion and persistence in European waters? Irrespective of whether K. mikimotoi is an introduced species or has emerged from the "hidden flora", it had to overcome the formidable obstacles of niche pre-emption and interspecific competition to achieve bloom success and persistence in the phytoplankton community. The problems confronting successful bioinvasions of introduced species have been discussed by Smayda (2002). The bloom dynamics and ecophysiology of K. mikimotoi are reviewed by Dahl et al. (1993) and Gentien (1998).
Scottish and UK waters have not escaped harmful blooms of K. mikimotoi. Its blooms have caused significant mortality of Atlantic salmon and rainbow trout in Scottish, Irish and Norwegian fish farms, and mortality of wild fish and benthic invertebrates, including shellfish and crustaceans (Boalch, 1987; Dahl and Tangen, 1993; Partensky and Sournia, 1986; Potts and Edwards, 1987). A 1987 bloom along the Cornish Coast was accompanied by fish kills, benthic dieoffs and physiological impairment (Forster, 1979; Griffiths et al., 1979; Widdows et al., 1979). Among invertebrates, mortality of lugworms, starfish and mussels, e.g. different functional groups, occurred along with mortality of eels, gadoids and cage culture salmonids. K. mikimotoi blooms have plagued Irish coastal waters and aquaculture, causing mortality of farmed salmon and clams ( Tapes semidecussata) (O'Boyle et al., 2001; Helm et al., 1974; McMahon et al., 1998; Ottway et al., 1979; Pybus, 1980; Raine et al., 1990). The impact of K. mikimotoi and its blooms on shellfish cultivation is further considered in Section 10.5.
The first reported fish kill in west Scotland waters attributed to a K. mikimotoi bloom occurred in Loch Fyne in September 1980. This red tide also occurred in Loch Striven, East Loch Tarbert and Loch Ewe (Jones et al., 1982). Sea water unintentionally pumped from Loch Fyne into a shore-based salmon farm during the bloom caused the death of adult salmon and smolts (Jones et al., 1982). Tett and Edwards (2002) state that this to have been the "largest bloom recorded in Scottish waters" [biomass levels reached 2,000 mg chl m -3], and that it probably was the result of unusual physical and biological processes.
Hypoxia is often the cause of mortality during K. mikimotoi blooms (Helm et al., 1974; Tangen, 1977, 1979). Farmed fish died from night-time hypoxia, the depletion of oxygen caused by the combined, high respiration rates of the salmon and bloom populations (Tangen, 1979). During the day, the waters are well oxygenated because of K. mikimotoi photosynthesis. Hypoxia is not the only mortality mode - haemolytic cytotoxins produced by K. mikimotoi also cause fish kills (Tangen, 1977; Yasumoto et al., 1990). The gill lesions of farmed salmon ( Salmo salar) that develop during K. mikimotoi blooms were reproducible in experimental cultures, consistent with a haemolytic effect (Turner et al., 1987). Mortality of rainbow trout also occurred when exposed to cultures K. mikimotoi (Roberts et al., 1983). K. mikimotoi has been shown to secrete anti-algal substances that inhibit competing phytoplankton species (Gentien and Arzul, 1990). This capacity may be a factor in the very dense blooms that K. mikimotoi achieves in European waters .
K. mikimotoi is common in open coastal waters, where it is often associated with shelf fronts, and advected from there into onshore embayments and fjordic systems (Holligan, 1979; Lindahl, 1986; McMahon et al., 1998; Raine et al., 1990; Richardson and Kullenberg, 1987). Holligan and co-workers (Holligan, 1979; Holligan et al., 1984a,b) provide important insights into bloom development and regulation of K. mikimotoi in UK waters. Smayda and Reynolds (2001) have classified it as a Type IV life-form - a species adapted for growth in frontal zones and during advection. It has two distinct types of blooms: offshore blooms in response to local hydrographic influences, including frontal zone delivery of nutrients, and sea loch blooms in waters conditioned by runoff and fish farm activity. It is also capable of producing blooms in relatively nutrient poor, inshore waters (Kristiansen et al., 1995). Sea loch blooms of K. mikimotoi require advective seeding from offshore populations. The basic ecophysiological requirements of the open coastal water and sea loch populations K. mikimotoi remain the same, but the combination of factors regulating the two bloom modes may differ significantly. A key distinction is that farmed fish are caged while cultured shellfish are sessile and filter feed on the natural phytoplankton communites. Thus, neither are capable of avoidance responses to antagonistic blooms of K. mikimotoi. Of the dinoflagellates present in Scottish coastal waters, blooms of K. mikimotoi are probably the most threatening to aquaculture.
5.2 Lingulodinium polyedrum
Blooms of Lingulodinium polyedrum (= Gonyaulax polyedra; = Lingulodinium machaerophorum) can lead to intense red tides. Otherwise, this enigmatic dinoflagellate is characterized by prolonged (decadal) gaps between its blooms (if not regional extinctions that require reseeding to bloom again). It appears to have markedly different ecotypes, and its purported toxicity is controversial. Eppley and Harrison (1975) have reviewed its bloom behavior in Californian waters and some aspects of its ecophysiology. Lewis and Hallett (1997) provide a more detailed, general review from a paleontological perspective. Lingulodinium polyedrum, given its putative toxicity, is considered here because it achieves high population densities during summer blooms in Loch Creran where, similar to West Loch Tarbert, rich deposits of resting cysts are also found (Lewis, 1988; Lewis et al., 1985). The ability of L. polyedrum to complete its life cycle of motile and cyst stages indicates that it is indigenous to these waters and, probably, in contiguous areas. This occurrence is consistent with its geographic distribution in European coastal waters, which extends from the Iberian peninsula to western Norway, Ireland and the U.K. (see Figure 29 in Lewis and Hallett, 1997). The cyst stage of L. polyedrum, recorded as L. machaerophorum by paleooceanographers, is restricted to waters with summer temperatures just above 10°C, with a biogeographical boundary just north of Trondheim on the Norwegian coast (see Dale et al., 1999).
The erratic bloom behavior of L. polyedrum was captured in Allen's (1943) summary of his daily observations during a 26-year time series in California: L. polyedrum " reached conspicuous ... red water abundance ... in only 3 years out of nearly 30". This pattern of long periods of virtual disappearance between blooms has continued in those waters (Eppley and Harrison, 1975). Similar bloom gaps have been recorded along the Iberian peninsula. In Portugal, where L. polyedrum is common in coastal waters, after a 1944 "red tide" bloom it did not bloom again for two decades (1967), followed thereafter by a three decade gap before its next bloom in 1996 (Amorim et al., 2001; Sampayo, 1989). In Spanish Galician rías that have become important shellfish cultivation sites, L. polyedrum "red tides" were recorded in 1916-1917 and in 1966, and have since become rare (Fraga and Bakun, 1993). The investigators state that L. polyedrum has been replaced by PSP toxic Gymnodinium catenatum.
Lingulodinium polyedrum had been known to bloom primarily in upwelling regions during periods of upwelling relaxation (Blasco, 1977). A bloom of L. polyedrum persisted for 20 days off Baja California in upwelled watermasses under turbulent conditions and elevated NO 3 concentrations (Eppley and Harrison 1975). It can also produce significant blooms at frontal zones, such as the 300 km bloom patch reported off Baja California (Lasker and Zweifel, 1978). The "red tides" of L. polyedrum along the Iberian peninsula, and specifically those in Portuguese and Spanish coastal waters (commented on in the previous paragraph), are in a region also well known for its upwelling. This apparent habitat preference led Smayda and Reynolds (2001) to classify L. polyedrum as a Type V dinoflagellate life-form - species which bloom in upwelling regions during upwelling relaxations. Interestingly, the apparent disappearance of L. polyedrum in Galician rîas was accompanied by emergence of Gymnodinium catenatum as a major bloom species (Fraga and Bakun, 1993), also a Type V dinoflagellate life-form.
The salient ecotypic feature of L. polyedrum allowing it to bloom in these physically dynamic upwelling and frontal regions in offshore coastal waters is its tolerance of "mixing-drift" conditions. There is increasing evidence that another ecotype of L. polyedrum occurs distinguished by its blooms in highly eutrophicated, nearshore habitats when vertical turbulence is seasonally (summer) dampened. Kastela Bay, Croatia, for example, has become one of the most eutrophicated systems in the Mediterranean (Marasovic et al., 1995,1998). Beginning in 1980, L. polyedrum blooms have recurred annually, its blooms progressively increasing in duration, from two weeks to the entire summer. This stimulation by high nutrient levels is consistent with the evidence presented by Dale et al. (1999). Their analyses of dinoflagellate cysts in sediment cores collected in the inner Oslofjord revealed the abundance of L. polyedrum resting cysts increased proportionately with cultural eutropication beginning in the mid-1800s. Dale and co-workers concluded that this species prefers regions of high nutrients, in agreement with Eppley and Harrison (1975), and that the level of its cyst abundance in "seed banks" serves as a eutrophication signal.
Lewis and Hallett (1997) discuss the contradictory evidence that L. polyedrum produces a toxin. Much of the evidence, both for and against toxicity, comes from culture experiments that have yet to resolve whether experimental techniques, strain differences or growth conditions are factors contributing to the variable results obtained. It is noteworthy that during the intense "red tides" that L. polyedrum produces human illness associated with phycotoxin production have not been reported, and faunal deaths are rare. Benthic mortality has been reported to occur during a L. polyedrum bloom (Stohler, 1959) and a post-bloom hypoxic event (Legovic et al., 1991).
« Previous | Contents | Next »