KARENIA: The biology and ecology of a toxic genus

Table 1.

Species within the genus Karenia¹

5.1. Temperature

K. brevis has been observed in the field between 7 and 33°C, but optimal growth in laboratory cultures is between 22 and 28 °C (Magaña and Villareal, 2006; Vargo, 2009). K. mikimotoi has been found over a wide range of temperatures, 4–31°C (Gentien, 1998); however, in some instances growth was observed within a strict window within that temperature range. For example Gyrodinium aureolum isolated in 1977 from the Oslofjord by Tangen (assumed to be K. mikimotoi) did not grow at temperatures <10°C or > 25°C (Nielsen and Tǿnseth, 1991).

5.2. Salinity

K. brevis generally grows between salinities of 18 and 45 PSU, but has a maximum growth rate between 30 and 34 PSU (Magaña and Villareal, 2006; Maier Brown et al., 2006; Vargo, 2009). Because K. brevis prefers full salinity seawater and is usually not found at salinities below about 24 PSU, blooms are generally found in coastal waters but not estuaries. The only time blooms occur in estuaries is during droughts when the salinity is high in the estuary (Steidinger and Ingle, 1972; Landsberg and Steidinger, 1998). They are also found in the high salinity lagoons of Texas (Tester et al., 2004).

Contrary to this generalization of high salinity that has been widely observed, Dortch et al. (1998) found K. brevis near the mouth of the Mississippi River in waters as low as 5 PSU and numerous locations below 24 PSU. This appears to be a one-time event in which K. brevis populations from the western panhandle of Florida were transported westward towards the Mississippi Delta into low salinity water.

K. mikimotoi has been found over a wide range of salinities, from 9 to 35 PSU (Gentien, 1998), however maximum growth in some culture studies was observed at salinities > 12 PSU (Nielsen and Tǿnseth, 1991).

5.3. Light

All Karenia species have chlorophylls a and c; and have fucoxanthin, 19’-butanoyloxyfucoxanthin, 19’-hexanoyloxyfucoxanthin, and 19-hexanoyloxyparacentrone 3-acetate (gyroxanthin-diester) as accessory pigments instead of peridinin, like most other dinoflagellates (Steidinger et al., 2008a). K. brevis and K. mikimotoi also have gyroxanthin (Richardson and Pinckney, 2004).

K. brevis has a compensation point around 6–8 μmol photo m⁻² sec ⁻¹ and saturation around 35–120 μmol photon m⁻² sec ⁻¹ (Magaña and Villareal, 2006; Vargo, 2009). Schaeffer et al. (2007) show significant differences among clones of K. brevis in their photosynthetic characteristics and that they can grow well in a wide range of light intensities. This indicates they are adapted for the high light intensities they experience when aggregated at the surface as well as the low light intensities found in the bottom waters and sediment surface. Studies on changes in the pigment and biochemical composition of K. brevis under a variety of environmental conditions indicate that they are not significantly different from other species of dinoflagellates (Shanley, 1985; Higham et al., 2004; Evens and Leblond, 2004). While K. brevis appears well adapted to low light levels, it appears to use the photoprotective xanthophyll cycle pigments diadinoxanthin and diatoxanthin to tolerate high light intensity when it accumulates at the surface during the day (Evens et al., 2001).

K. mikimotoi seems to also tolerate a wide range of light intensities, from the surface to the pycnocline (Gentien, 1998). Cells exhibit photoadaptation mechanisms with cells growing in low light conditions containing more chlorophyll a, improving photosynthetic efficiency at low light intensities. Photosynthetic efficiency was also improved when dark adapted cells were returned to high irradiances (Garcia and Purdie, 1994). Saturation was observed to be approx 200 μmol photon m⁻² sec ⁻¹ (Richardson and Kullenberg,1987).

5.4. Nutrition

Karenia dinoflagellates are considered primarily autotrophic, but they do have some capability for using organic compounds and ingesting microbes. Studies with field populations of K. brevis show that it can use nitrate, ammonia, urea, glutamate, and dissolved organic matter from Trichodesmium (Bronk et al., 2004). Sinclair et al. (2009) have shown that K. brevis takes up ammonia and urea at night as well as day, which could be important in obtaining nutrients during diel vertical migration. Baden and Mende (1979) showed that K. brevis can use glycine, valine, and methionine. Shimizu et al. (1995) found that urea and glycine added to cultures of K. brevis stimulates a shift to a more heterotrophic mode, and increased biomass and brevetoxin amount 2 to 4 fold. Mulholland et al. (2004, 2006) have shown that K. brevis can utilize dissolved organic matter that has been excreted by Trichodesmium. Vargo and Shanley (1985) have shown that K. brevis uses organic phosphorus, using alkaline phosphatase. Jeong et al. (2005) and Glibert et al. (2009) have documented that cultures of K. brevis can ingest cells of the cyanobacteria Synechococcus and enhance its growth rate. It appears that K. brevis is nutritionally quite versatile, utilizing inorganic nutrients, organic nutrients, and phagotrophy on other microbes. The fact that K. brevis lives in the oligotrophic central Gulf of Mexico (Geesey and Tester, 1993) indicates that it can survive on very low levels of nutrients.

Other species of Karenia probably have similar capabilities. Mountfort et al. (2006) found that glycolate and alanine added to cultures of K selliformis doubled the biomass and gymnodimine production. Nitrogen has been identified as an important nutrient in Karenia blooms. K. mikimotoi has been observed to utilise nitrate, nitrite and ammonium as N sources however urea and uric acid were not so well utilized in laboratory studies(Yamaguchi and Itakura 1999). Urea was observed to be taken up in the East China Sea (Li et al., 2009). Glutamine and tryptophan were utilised as well as both organic and inorganic forms of P (Yamaguchi and Itakura, 1999). Gentien (1998) has suggested that K. mikimotoi is stimulated by the organics released from decaying diatom blooms. A field study on K. mikimotoi from the Ushant front in the western English Channel revealed ammonia to be the preferred nitrogen source. In addition, dark N uptake did not occur in nutrient replete cells, while it was observed in nutrient limited cells (Dixon and Holligan, 1989).

9.1. Brevetoxin

Brevetoxin is the toxin from Karenia species that affects human health and has been studied the most. Brevetoxins are produced by K. brevis, and there is some evidence that K. bicuneiformis, K. brevisulcata, K. concordia, K. cristata, K. papilionacea, and K. selliformis may also produce brevetoxins or similar molecules. The raphidophytes Chattonella antigua, C. marina, Fibrocapsa japonica, and Heterosigma akashiwo also produce brevetoxins (Landsberg, 2002; Furey et al, 2007; Ramsdell, 2008).

The brevetoxins are lipid soluble cyclic polyether compounds with molecular weights of around 900 that are tasteless, odorless, and heat stable. K. brevis produces two parent compounds, PbTx-1 and PbTx-2, which have somewhat different structures (Furey et al., 2007; Ramsdell, 2008). PbTx-1 is somewhat flexible with 10 fused polyether rings. PbTx-2 is more rigid with 11 polyether rings (Furey et al., 2007). PbTx-1 is more toxic but PbTx-2 occurs in higher concentrations (Steidinger et al., 2008a; Plakas and Dickey, 2010). Brevetoxins are polyketides synthesized by the polyketide synthase (PKS) pathway (Wright and Cembella, 1998). While there were earlier speculations that perhaps bacteria associated with K. brevis actually produce brevetoxin because laboratory cultures sometimes lose their ability to produce brevetoxin, genetic studies have now confirmed that the PKS genes exist in the K. brevis genome (Snyder et al., 2003, 2005; Monroe and Van Dolah 2008; Monroe et al., 2010). It is possible that bacteria are involved by stimulating the production of brevetoxin, especially if it serves as an allelochemical. K. brevis also produces brevisamide and brevisin, which are 4-fused cyclic ether rings and brevenals, which are 5-fused cyclic ether rings (Bourdelais et al., 2004, 2005; Ramsdell, 2008; Van Wagoner et al., 2010). These are thought to be incomplete products of the PKS biosynthetic pathway. Brevenal acts as an antagonist to brevetoxin and may also be useful as a therapeutic agent against cystic fibrosis (Potera, 2007).

In addition to PbTx-1 and PbTx-2, another 10 congeners are the result of small modifications, primarily reductions, oxidations, and hydrolysis, of these two main compounds, primarily once they are released from the cells and are modified by physical/chemical processes or microbes in the water, and metabolism by animals in the food chain. Each genotype of K. brevis produces somewhat different amounts and ratios of these two toxins, and the array changes with environmental and physiological changes (Lekan and Tomas, 2010; Errera et al., 2010). Even more changes occur as the brevetoxins enter the water, air, and food web, and are metabolized. Genetic variation was more important than environmental variation (temperature, salinity, nutrients) in determining amount of brevetoxins. Errera et al. (2010) found a 10-fold range in the amount of brevetoxin and brevenal produced by different genotypes of K. brevis. They also observed a shift to the more toxic PbTx-1 at lower salinity. Recently, Errera and Campbell (2011) have found that a rapid decrease in salinity can induce a 10-fold increase in brevetoxin production.

Brevetoxin is a long molecule that spans voltage gated sodium channels, causing them to remain open for an excessive amount of time, leading to uncontrolled sodium influx and depolarization of the membrane (Ramsdell, 2008). As a result of the persistent activation and repetitive firing of neurons, brevetoxin affects neuromuscular junctions, which can lead to respiratory distress; and affects cardiac muscle, leading to slow and arrhythmic heart beat (Ramsdell, 2008).

In several cases, Karenia species other than K. brevis have caused brevetoxin-like symptoms in humans. K. concordia in New Zealand caused respiratory distress and NSP in humans (Chang, 2011). Blooms of K. brevisulcata in New Zealand in 1998 caused mass mortality of animals and aerosols from the blooms affected the respiration of humans (Truman, 2007). The symptoms were similar to those produced by K. brevis in the Gulf of Mexico. An analysis of the lipid soluble toxins from cultures of K. brevisulcata indicated that they affected sodium channels like brevetoxin, and other characteristics were similar to brevetoxin, but not completely. K. cristata bloomed in South Africa in 1995–1996 and caused respiratory problems in humans (Botes et al., 2003a, b). It is not known if brevetoxin was involved in this case. Brevetoxin specific ELISA tests indicated the presence of brevetoxin in K. bicuneiformis, K. papilionacea, and K. selliformis (Haywood et al., 2004). To date, there has been no actual confirmation of brevetoxin in these 6 species by LC-MS however.

Brevetoxin can affect human health in three ways – by ingestion of contaminated food, by skin contact in water, and by inhalation of the aerosol.

9.2. Neurotoxic Shellfish Poisoning

Neurotoxic Shellfish Poisoning (NSP) results from humans eating filter feeding molluscs that have accumulated brevetoxin in their fatty tissues. We now know that brevetoxin can be found in the tissues of other seafood as well, such as non-filter feeding molluscs (Poli et al., 2000) and fish (Naar et al., 2007). The toxin tends to accumulate more in the fatty tissues of organs than in muscle tissue. Because humans usually eat only the muscle tissue of fish, but the entire body of shellfish, shellfish has been the primary source of NSP.

Because of a monitoring program and the banning of shellfish harvesting during red tides along the west coast of Florida, NSP cases are now extremely rare. There are no restrictions on the consumption of fish however, because it has been assumed that fish exposed to brevetoxin die and are not available for consumption. We now know that fish exposed to sublethal concentrations in fact do accumulate brevetoxin (Naar et al., 2007). While the concentrations in the muscle tissue is less than that found in the liver and other organs or in the whole bodies of shellfish, we do not know what effects these low concentrations of brevetoxin could have on human health. Interestingly, Kirkpatrick et al. (2010a) have found increased incidences of hospital admittances for gastrointestinal disorders during periods of red tide along the west coast of Florida.

NSP has occurred primarily in the Gulf of Mexico, particularly the west coast of Florida, but more recently it has also occurred in North Carolina due to an unusual transport of a K. brevis bloom from the west Florida coast to North Carolina by the Gulf Stream (Tester et al., 1989; Tester and Stumpf, 1991) and New Zealand where a new bloom of K. concordia developed (Chang, 2011). While blooms of Karenia are largest and most frequent in the Gulf of Mexico, few cases of NSP occur there because of careful monitoring. Cases of NSP occurred in North Carolina and New Zealand because new blooms occurred where they had not occurred before and were unexpected and thus not monitored for seafood safety.

After the consumption of brevetoxin contaminated food, symptoms begin within minutes to hours but diminish within a few days (Watkins et al., 2008; Plakas and Dickey, 2010). The primary gastrointestinal and neurological symptoms are abdominal pain, nausea, vomiting, diarrhea, headache, vertigo, numbness of lips, mouth and face, dilated pupils, muscle pain, loss of coordination, partial paralysis, convulsions, disorientation, tingling sensations, temperature sensation reversals, and respiratory distress (Watkins et al., 2008; Kirkpatrick et al., 2004; Fleming et al., 2011).

9.3. Skin contact

Because some brevetoxin is released into the water, primarily because of cell lysis, swimmers can experience eye and nose irritation (Kusek et al, 1999; Ramsdell, 2008). This appears rare and is not considered to be a major health hazard.

9.4. Aerosol

Because Karenia is a delicate, unarmored dinoflagellate, the cells can be ruptured relatively easily by turbulence at the surface or along the shore, releasing the brevetoxin into the air as an aerosol. Humans that breathe brevetoxin contaminated aerosols immediately experience coughing, sneezing, runny nose, watery eyes, a burning sensation in the nose and throat, chest tightness, and shortness of breath (Fleming et al., 2005; Abraham and Baden, 2006). Large aerosol particles (6–10 microns) only make it into the upper respiratory tract, causing throat and nasal irritation, while small aerosol particles (0.1–0.2 microns) make it into the lower respiratory tract, making breathing difficult (Ramsdell, 2008).

Kirkpatrick et al. (2006) found pneumonia, bronchitis, asthma and respiratory distress to increase 31%, 56%, 44% and 64% respectively during a red tide up to 1.6 km inshore along the west coast of Florida. Humans with asthma are particularly sensitive to brevetoxin aerosols and often end up in the hospital with severe symptoms (Kirkpatrick et al., 2004, 2011a; Abraham and Baden, 2006; Fleming et al. 2007, 2011)

Humans have experienced respiratory distress from blooms of other species of Karenia in New Zealand (Truman, 2007; Chang, 2011), South Africa (Botes et al., 2003a, b), and New Jersey, USA (Mahoney et al., 1990).

9.5. Other effects

Some studies have indicated that brevetoxin may affect the immune system (Bossart et al., 1998; Benson et al., 2005; Fleming et al., 2011). Radwan and Ramsdell (2008) showed that brevetoxin forms covalent DNA adducts and is thus potentially mutagenic.

12.1. Blooms

While blooms of K. brevis and K. mikimotoi have been known to occur for many hundreds of years and are part of their natural population dynamics, it is not clear if the other, newly discovered species of Karenia have always bloomed on occasion and are only now being discovered, or if these recent blooms are a new phenomenon, perhaps a result of a changing environment.

In terms of species composition, one can find a whole range of examples. Some blooms are essentially monospecific (Steidinger and Vargo, 1988). In other cases, other species of algae are mixed in with Karenia. It has been recently discovered that many of these Karenia blooms actually include several species of Karenia. That several species of Karenia would bloom at the same time and place suggests that their basic biology and ecological requirements are similar, but that also brings up the question of the competitive exclusion principle, and how these different Karenia species coexist if they occupy similar niches.

A fundamental question to be addressed is how Karenia species can develop such a large biomass in a bloom. This is a very complex question, and in most instances the involved in the development of high biomass blooms are not known but are probably a combination of biological and physical factors. Karenia, like most dinoflagellates, replicate very slowly, less than once a day. Dinoflagellates are basically the slowest of all the algal taxa. How can they outcompete fast growing competitors such as diatoms? How are dinoflagellates different from diatoms and other algae in a way that allows them to compete?

While dinoflagellates are among the slowest growing algae, they are the fastest swimmers. This allows them to undergo diel vertical migration. This allows them access to higher concentrations of nutrients below the pycnocline in stratified waters not available to most competing species of algae (Heil, 1986; Kamykowski et al., 1998). In the case of at least K. brevis, it can also swim into the sediment pore waters to obtain the even higher nutrient concentrations there (Sinclair and Kamykowski, 2008).

Dinoflagellates in general appear to have a greater ability to utilize organic nutrients in addition to inorganic nutrients (Smayda, 1997; Glibert and Legrand, 2006; Burkholder et al., 2008). Most coastal waters contain much more organic nutrients than inorganic nutrients, so this could allow Karenia to ultimately develop a much higher biomass than algae than can only use inorganic nutrients.

Karenia species appear to produce a number of allelochemicals that could help them outcompete faster growing algae and resist attacks from microbial predators. Allelochemicals are generally not effective against large grazers on a microscopic scale at low concentrations, but once a bloom has developed, the high concentration of allelochemicals may reduce large grazers as well and help maintain or prolong the bloom. There is some evidence to support this with K. mikimotoi and diatoms (Gentien et al., 2007).

Diel vertical migration, ability to use organic nutrients, and the production of allelochemicals may allow Karenia to outcompete other species, but these factors alone do not explain the sporadic distribution in time and space of blooms or predict any specific bloom.

Physical factors play an important role for two reasons. First, dilution rate as a result of turbulent mixing must be lower than the growth rate of the algae, which is slow in the case of Karenia and dinoflagellates in general. This is necessary for both the early growth and maintenance of a bloom. Some of the Karenia species bloom in embayments where advection out of the water body is low. Examples include Wellington Harbor, New Zealand for K. concordia, the high salinity lagoons of Texas (Tester et al., 2004) for K. brevis, and Tampa Bay, Florida under high salinity conditions during a drought (Steidinger and Ingle, 1972) for K. brevis.

In general however, Karenia species tend to bloom in open coastal waters where advection and turbulent mixing is stronger. Olascoaga et al. (2006) and Beron-Vera and Olascoaga (2009) have argued that persistent Lagrangian Coherent Structures may provide the low mixing parcels of water that can act as incubators that allow a bloom to get started without excessive mixing dilution. These Lagrangian Coherent Structures can persist for approximately two months on the West Florida Shelf, enough time for K. brevis to increase its biomass approximately 100,000-fold by cell division alone (assuming no grazing loss). Olascoaga (2010) found that the three areas in the Gulf of Mexico with the lowest mixing activity in her analysis to be off the coast of Florida, Texas, and Mexico, precisely where K. brevis forms the most blooms. In general, it appears that many Karenia blooms occur in stratified waters where turbulent mixing is low.

A second factor that is quite likely to be important is a physical concentrating mechanism. In many if not most cases, blooms appear to increase in size faster than the dinoflagellates can grow. This implies a physical concentrating mechanism. As a result of diel vertical migration, K. brevis tends to aggregate at the surface during the day. This can concentrate cells by only about one order of magnitude however (cells in a 10 m water column swimming to the surface and becoming concentrated in the upper 1 m, for example). Langmuir circulation cells can also aggregate cells in convergence zones on a small scale. These mechanisms might concentrate Karenia enough for their allelochemicals to become more effective. Other mechanisms are needed for the much greater concentrations observed over larger scales. The most obvious case is downwelling, in which cells at the surface from a large area are transported to the downwelling site and accumulate there as they swim upward to counteract the downward movement of the water. Over time, this mechanism can generate very high concentrations of organisms (Hetland and Campbell, 2007).

12.2. Nutrients for blooms

While a large amount of nutrients are needed to generate a large bloom biomass, high concentrations of nutrients are not necessary, and nutrients may not necessarily play a major role in initiating a bloom. Low concentrations of nutrients can generate low concentrations of Karenia over a large area. A physical concentrating mechanism can then aggregate these cells into a bloom that contains far more nutrients than would be in the water parcel they occupy.

While nutrients are clearly a factor in generating many algae blooms in certain areas around the world, they may be less important in the initiation of a Karenia bloom. A sudden pulse of inorganic nutrients is more likely to give diatoms a competitive advantage over Karenia. Nutrient sources that could give Karenia an advantage over diatoms and other algae are those below the pycnocline or in the sediments that they can migrate to, or organic nutrients that they can more easily assimilate than other algae. In addition to the large pool of organic nutrients in seawater and freshwater runoff, dieoff of diatom blooms, benthic biota, fish, or excretion by organisms such as Trichodesmium could provide a source of nutrients.

It is important to distinguish new and old nutrients, as new nutrients will generate more plant biomass, while old nutrients will not. For an individual species, such as Karenia, this distinction needs to be modified. For example, if upwelled inorganic (new) nutrients generate a diatom bloom which subsequently dies and release nutrients to Karenia, those recycled nutrients are technically old nutrients, but act as new nutrients to generate new biomass of Karenia. The same would be true for new nutrients taken up by macroalgae or seagrasses that subsequently die and release their nutrients to Karenia.

It is also important to distinguish nutrient sources that help initiate a bloom and those that are important in increasing its biomass and sustaining it over time. Many nutrient sources are potentially available to increase the Karenia biomass. It is more difficult to identify a nutrient source that can explain when and where blooms have first developed. Most nutrient sources appear to be more widespread than the blooms.

12.3. K. brevis in the Gulf of Mexico

The species that has the largest impact on human health and has been investigated in more detail is K. brevis. It appears to live in the oligotrophic waters of the oceanic regions of the Gulf of Mexico in low concentrations, at somewhat higher concentrations on the continental shelves, and occasionally bloom to extremely high concentrations closer to the coast (Geesey and Tester, 1993). Further evidence that it is adapted to relatively oligotrophic conditions is the fact that it can survive being transported by the Gulf Stream out of the Gulf of Mexico and up the east coast of North America (Murphy et al., 1975; Tester et al, 1989; Tester and Stumpf, 1991; Tester and Steidinger, 1997).

Blooms of K. brevis are most frequent along the west coast of Florida, between Tampa Bay and Sanibel Island (Brand and Compton, 2007). This is where tidal mixing is at a minimum (He and Weisberg, 2002) and a transport barrier reduces mixing between inshore and offshore waters (Yang et al, 1999; Olascoaga et al. 2006; Olascoaga, 2010). In Florida, Texas, and Mexico, K. brevis is most likely to form blooms in the fall months (Tester and Steidinger, 1997; Steidinger et al, 1998; Brand and Compton, 2007; Hetland and Campbell, 2007). Hetland and Campbell (2007) have shown that downwelling during the fall months along the Texas coast can lead to a 1000-fold concentration of K. brevis cells, making it a likely factor in the development of blooms there. On the west coast of Florida however, winds in the fall tend to favor upwelling (Stumpf et al., 1998, 2008; Yang and Weisberg, 1999; He and Weisberg, 2003; Walsh et al., 2006; Weisberg et al., 2009). This has led to many studies hypothesizing that K. brevis in bottom waters is carried inshore to frontal boundaries (He and Weisberg, 2003; Walsh et al., 2006; Stumpf et al., 2008; Milroy et al., 2008; Weisberg et al., 2009; Schaeffer et al., 2009). But upwelling alone will not concentrate the cells, only bring deep dwelling cells closer to the coastline. Once they upwell to the surface, surface currents will carry them back offshore. Some studies (Vargo et al., 2004; Stumpf et al., 2008; Weisberg et al., 2009) indicate that the upwelling occurs in frontal regions, where some unknown mechanism will concentrate the cells rather than let them be transported back offshore. This mechanism has not been identified. One scenario could be a low salinity plume overlaying the upwelling region, with the Karenia cells advecting under the plume then migrating up into it, generating a bloom along the salinity front. Such a mechanism has been described for dinoflagellate blooms in the Gulf of Maine (Hetland et al., 2002). Alternatively, Lanerolle, et al. (2006) suggest that a complex sequence of both upwelling and downwelling may be responsible for concentrating the cells.

Another problem with the upwelling hypothesis is that few data have shown significant amounts of K. brevis in bottom water on the West Florida Shelf. Most data show higher concentrations in surface waters than deep water. In this situation, the upwelling circulation will lead to a net flux of cells offshore. A mechanism is needed to trap and concentrate the cells inshore. The very broad West Florida Shelf could provide a large seed population even if sporadic and in low concentrations, but the source has not been identified (Walsh et al., 2002). It is not clear if the seed population is planktonic or benthic, from the inner or outer shelf, or throughout the shelf.

During the fall months when K. brevis blooms are most likely, other factors interact with this general upwelling circulation pattern (deep waters moving inshore and surface waters moving offshore). It is at this time that vertical stratification weakens and breaks down (Weisberg et al., 2001). Winds increase and upwelling increases in the fall (Stumpf et al., 1998). This is the time that alongshore currents shift from northward to southward (Yang and Weisberg, 1999; Carlson and Clarke, 2009). This is also the time that shallow waters in the north cool down and send plumes of cold water southward along the coast, generating thermal fronts (He and Weisberg, 2003). This is also the peak of the wet season and land runoff in South Florida (Brand and Compton, 2007), when salinity fronts are generated along the coastline. It is suspected that the interaction of the shoreward movement of the bottom waters containing low concentrations of K. brevis with these thermal and salinity fronts at a time of weakening vertical stratification may provide a mechanism (still not understood) for concentrating K. brevis.

Almost certainly, physical factors are very important in the development of Karenia blooms, but so far we have no models that can predict exactly when or where a bloom will develop.

12.4. Nutrient sources on the west coast of Florida

To generate the large biomass in a Karenia bloom, large amount of nutrients are needed. There are many potential sources of nutrients available to the Karenia blooms along the west Florida coastline, but it is not clear if any of them can be the major source and/or explain the early development of the blooms and their eventual size.

Surface waters of the West Florida Shelf have low concentrations of nutrients, particularly nitrogen (Vargo, 2009). This may be why K. brevis, which appears to be adapted for surviving the oligotrophic waters of the central Gulf of Mexico, survives on the West Florida Shelf as well. These low nutrient concentrations do not necessarily indicate low nutrient inputs however. Because the wide West Florida Shelf is rather shallow, much of it is within the photic zone, so much of the nutrient inputs are probably rapidly taken up by the benthic plant community (macroalgae, seagrasses, sedimentary microalgae). Benthic chlorophyll on the West Florida Shelf is much higher than in the water column above (Walsh and Steidinger, 2001).

A number of researchers have noted a rough correlation between land runoff and K. brevis blooms (Gunter et al., 1947; Slobodkin, 1953; Odum et al., 1955; Finucane, 1964; Steidinger and Joyce, 1973; Dixon and Steidinger, 2004). Some have even suggested an iron index as an indicator of land runoff (Ingle and Martin, 1971). One also observes a general correlation on a seasonal basis, with K. brevis blooms most likely during the fall months when land runoff is at its peak (Brand and Compton, 2007). Rounsefell and Nelson (1966) summarized much of the earlier research on this topic. In all cases, these are only general correlations, and there are many exceptions, e.g., blooms during droughts and no blooms during large runoff events. Though rare, blooms have developed during the spring dry season, and some years have no obvious blooms during the wet season.

A perusal of the 50 year monitoring data collected by the State of Florida shows a number of cases in which blooms of K. brevis first appear near the mouth of rivers. Olascoaga et al. (2008) document a bloom in 2004 that appears to originate near the mouth of the Caloosahatchee River, and Yentsch et al. (2008) do the same for a bloom in 2005 near the mouth of the Caloosahatchee River. Vargo et al. (2004) observed elevated concentrations of silica in all four blooms he examined, indicating the blooms were in water masses with land runoff influences.

Brand and Compton (2007) argued that land runoff nutrients were significant in increasing K. brevis biomass because the biomass is larger inshore in lower salinity water than offshore in higher salinity water. They also argued that K. brevis biomass has increased significantly over the past 50 years, during a time that land runoff nutrients have increased significantly but offshore nutrients have not.

It should be noted that even if there is a strong correlation between blooms and land runoff, it would not necessarily be the result of nutrients. The increased salinity fronts generated during land runoff might help set up concentrating mechanisms for generating high concentrations of the slow growing Karenia.

In addition to surface water runoff from land, groundwater inputs to coastal waters must also be considered. Miller et al. (1990) showed the importance of groundwater in Charlotte Harbor and Hu et al. (2006) argued that groundwater could be a major source of nutrients to the West Florida Shelf. As a result of various human activities on land, groundwater nutrient concentrations have increase dramatically in recent decades (Scott et al., 2006). Related to this is the possibility that K. brevis could migrate down into the sediments to take advantage of higher nutrient concentrations in the porewaters (Sinclair and Kamykowski, 2008). The higher nutrient concentrations there are reflected in the fact that chlorophyll concentrations are higher in the sediments than the water column above (Walsh and Steidinger, 2001).

Other early studies focused on upwelling of nutrient rich deep water onto the shelf and its transport across the shelf to the coastal region (Steidinger and Haddad, 1981; Tester and Steidinger, 1997; Lanerolle et al., 2006; Janowitz and Kamykowski, 2006; Weisberg et al., 2009). The overall estuarine circulation of the shelf with bottom water flowing inshore more than offshore (Weisberg et al., 2001), certainly will tend to generate a net flux of nutrients inshore, allowing the shelf to act as a nutrient trap to some degree. While this certainly supplies some nutrients to the blooms, Walsh et al. (2003) concluded that the amount of nutrients transported by this mechanism is insufficient to support the blooms observed.

A somewhat unique characteristic of the West Florida Shelf is the presence of large phosphate deposits along the west coast of Florida and presumably on out onto the shelf (Compton, 1997; Brand 2002; Walsh et al., 2006). This generates low N/P ratios and an ecosystem that is nitrogen limited (Brand, 2002; Walsh et al., 2006; Brand and Compton, 2007). As a result, inorganic nitrogen concentrations are usually very low on much of the West Florida Shelf, even inshore. Any input of nitrogen is quickly taken up by phytoplankton that have sufficient phosphorus and are starved for nitrogen. This situation provides a selective advantage to nitrogen-fixing cyanobacteria.

Some researchers have noted an apparent correlation between blooms of the nitrogen –fixing Trichodesmium and K. brevis (Gunter et al., 1948; Geesey and Tester, 1993). It has been shown that Trichodesmium excretes organic nitrogen that can then be taken up by K. brevis (Havens et al., 2004; Mulholland et al., 2004, 2006). Cyanobacteria , especially nitrogen-fixers, need more iron than eukaryotic algae (Rueter et al., 1990; Brand, 1991; Paerl et al., 1994). Lenes et al. (2001), Walsh and Steidinger (2001), and Walsh et al. (2006) have hypothesized that iron limits the growth of Trichodesmium on the West Florida Shelf, and iron-rich dust from Africa is a major source of iron and may serve as a stimulant for blooms of Trichodesmium, which could then lead to blooms of K. brevis. Biegalski and Villareal (2005) observed higher input of atmospheric iron during a bloom of K. brevis along the Texas coast.

While inshore waters probably get more iron from land runoff, atmospheric dust is probably the major source of iron offshore. It seems quite plausible that this iron is enhancing the growth of Trichodesmium and augmenting the nitrogen pool of the West Florida Shelf that is available to K. brevis. Whether or not atmospheric dust input is the major factor stimulating blooms of K. brevis is less clear. An examination of the timing of atmospheric dust input, Trichodesmium, and K. brevis blooms shown in Walsh and Steidinger (2001) and Berg et al. (2004) shows only partial correlation, as also noted by Stumpf et al. (2008). Furthermore, atmospheric dust will tend to cover large areas of the West Florida Shelf, but the blooms generally start in relatively small areas. Atmospheric iron probably increases the biomass of Trichodesmium and K. brevis, but it is not clear if it can explain when or where K. brevis blooms will occur.

The dieoff of other organisms and the release of their nutrients is another potential source of nutrients. Some have considered decomposition of dead fish (Vargo et al., 2008; Walsh et al., 2009). Once a bloom is dense enough to kill fish, nutrients from decomposing fish could certainly help sustain a bloom of K. brevis, especially if it dominates the community. It is less clear if fish kills from some other cause could be an important factor in initiation of the sporadic blooms of K. brevis. Another possibility is the dieback of benthic plants on the shelf, particularly in the deeper water where the plants are near their compensation point. The fall months are when benthic plants are under the greatest energy balance stress – when temperatures are still high (keeping respiration rates high) but light intensity and daylength are declining. This is typically the time of year that dieoffs of seagrass and macroalgae are observed. Bottom temperature and water clarity above vary spatially and temporally due to hydrography and other factors. They would be factors in determining the extent to which benthic plants might die and release nutrients slowly to K. brevis. If a benthic population of K. brevis exists, it would also be under energy balance stress, perhaps stimulating it to migrate to the surface. For example, bottom temperatures could actually increase in the fall when the advection of cold bottom water from offshore stops and stratification breaks down. This increase in temperature at a time of reduced light could either stimulate a benthic population of K. brevis to migrate up into the surface waters and/or lead to the death of macroalgae and seagrasses and subsequent release of nutrients to K. brevis.

Dying diatom blooms are another potential source of nutrients. Many seasonal sequences throughout the world start with diatom blooms utilizing upwelled inorganic nutrients. As the diatom blooms die, they release nutrients and dinoflagellates become more dominant. It seems likely that K. brevis may get most of its nutrients only after recycling through diatoms and other parts of the food web; and inorganic nutrients from bottom water or land runoff simply enhances that food web.

Whatever the initial source of nutrients, the blooms are typically much larger inshore than offshore (Brand and Compton, 2007). This suggests that even if land runoff is not an important factor in initiating blooms, it is probably important for the eventual buildup of larger biomass. Upwelling of offshore nutrients, atmospheric iron, and dead fish as nutrient sources cannot explain this inshore-offshore gradient.

12.5. K. concordia in New Zealand

Beyond the Gulf of Mexico, another location that has experienced significant human health problems (along with animal mortalities) from Karenia is New Zealand (Chang, 1995). The first significant blooms of Karenia were in January (summer) 1993 along the northeast coast (Bay of Plenty) of the North Island of New Zealand. The newly identified species was K. concordia and it apparently produces toxins similar to K. brevis (Chang et al., 1998). Hundreds of people ended up with NSP and respiratory distress (Chang, 1995; Trusewich et al., 1996; Chang et al., 1998), as there was no monitoring program in place because there had been no problems previously. Another bloom of K. concordia developed along the northeast coast (Hauraki Gulf) of the North Island in October (spring) 2002 (Chang and Ryan, 2004; Chang et al., 2008). In this case, no human effects were observed, but widespread mortality of fish and abalone occurred. Although one bloom occurred in the summer and the other in the spring, both were in years of El Nino, in which upwelling favorable winds were stronger than normal. The 2002 bloom occurred after the winds died down and a warm tongue of offshore water was transported inshore over the cold upwelled water (Chang and Ryan, 2004; Chang et al., 2008). It is known that low concentrations of K. brevisulcata, K. concordia , and K. mikimotoi occur in the warm offshore waters (Chang and Ryan, 2004). It is thought that the transport of the warm water over the upwelled water brought K. concordia into Hauraki Gulf and its diel vertical migration behavior allowed it to take advantage of the nutrient rich water below. There is less information on the 1993 bloom, but Chang et al. (1996) noted that the temperature was lower and the salinity was higher than normal when the bloom developed in the Bay of Plenty, suggesting a similar set of circumstances.

12.6. K. brevisulcata in New Zealand

A different species, K. brevisulcata, bloomed January to March (summer) 1998 along the south coast of the North Island of New Zealand and in Wellington Harbor on the north coast of the South Island (Chang, 1999; Wear and Gardner, 2001; Truman et al., 2005). Humans experienced respiratory distress and skin irritations. Animal mortality was extremely widespread, including zooplankton, benthic invertebrates, and both benthic and pelagic fish (Wear and Gardner, 2001). It was noted that the water was unusually warm and stratified at the time of the bloom.

12.7. K. cristata and K. bicuneiformis in South Africa

Along the southwest coast of South Africa, blooms of Karenia have developed in the fall months of numerous years (Botes et al., 2003a, b). K. cristata has bloomed in 1988, 1989, 1995, and 1996. Humans experienced respiratory effects and skin irritation during those blooms. Mortality of abalone has also been observed. Blooms of K. bicuneiformis have occurred in 1995 and 1997. No human effects or animal mortalities were observed associated with this species. It appeared that these blooms in the fall were associated with periods of calm weather followed by winds generating surface movements to the shoreline and downwelling (Botes et al., 2003a, b).

12.8. K. mikimotoi

Blooms of K. mikimotoi have occurred in many parts of the world, causing major fish kills, particularly since the 1960s. In Europe anecdotal evidence suggest that this species was blooming off the south west coast of Ireland as early as the late 1800s (http://ioc-unesco.org/hab/index.php?option=com_oe&task=viewDocumentRecord&docID=4605). In Europe, the first major bloom of K. mikimotoi occurred in the fall 1966 along the Norwegian coast (Braarud and Heimdal, 1970). Blooms usually occur during the summer or fall when the water is stratified. In Europe, blooms are observed in coastal waters, but are believed to develop in more offshore areas between fronts of different water masses (Pingree et al., 1975, Tangen 1977, Lindahl 1986, Gentian 1998, Gentian et al., 2005, Davidson et al., 2009). Pingree et al. (1978) has argued that surface blooms occur where pycnocline populations in stratified waters meet frontal boundaries where the water is mixed or at times when stratified waters become mixed. Gentien (1998) has suggested that K. mikimotoi tends to reside in the pycnocline if it is strong and undergo diel vertical migration if the pycnocline is relatively weak. Blooms may be enhanced by anoxia in the bottom waters. At the present time, there is no mechanistic model that can fully explain or predict when and where blooms of K. mikimotoi occur.

Pingree et al. (1975) documented a bloom at a front at the western entrance to the English Channel in 1975. He argues that K. mikimotoi resides in the pycnocline of the stratified waters of the Atlantic Ocean and form a surface bloom at the front where the stratified water meets the mixed waters of the English Channel (Pingree et al., 1978). Similar blooms occurred in July in 1977 and 1978, and in September in 1980 and 1981 at fronts between inshore mixed waters and offshore stratified waters along the coast of Scotland (Gowen, 1987). The blooms in 1980 and 1981 killed large numbers of fish (Jones et al, 1982; Davidson et al., 2009). Davidson et al. (2009) have also documented blooms of K. mikimotoi in the Orkney Islands in 1999 and 2003, the Shetland Islands in 2003 and a large bloom in northern Scotland that started on the west coast in July 2006 and moved along the coastline to the east coast. This bloom killed large numbers of benthic invertebrates and some fish. K. mikimotoi blooms have also been observed in Ireland, sometimes with devasting impacts on farmed fish (Raine et al., 2001, Silke et al., 2005). In this area, thermal jets are believed to play a role transporting the bloom along the Irish coast (Raine et al., 2010). Blooms have occurred in the summer at fronts along the Atlantic coast of France in 1984 and 1987 (Gentian et al., 1998). In July 1995, a similar bloom expanded to the entire coastline of western France.

In Scandinavian waters blooms of K. mikimotoi have been associated with offshore inflow into the Skaggerak (Lindahl, 1986). The relationship between land run off and K. mikimotoi blooms is complex. Blooms have been observed along the southern coast of Norway after heavy freshwater input (Dahl et al., 1987), however in some instances the amount of nitrogen needed to sustain a K. mikimoti in coastal areas is not associated with land run off but with nutrients from more offshore areas or physical processes (Lindahl, 1986). This was also observed in Scottish waters in 2006 where the number of K. mikimotoi cells in Scapa Bay in the Orkney islands could not be supported by the nitrogen entering the system from land based sources (Davidson et al., 2009). In September 1982, blooms developed along a front between the higher salinity North Sea and lower salinity Skagerrak (Lindahl, 1983, 1993; Richardson and Kullenberg, 1987). A similar bloom developed in the late summer and fall 1987 as a pycnocline residing population of K. mikimotoi surfaced at a front in the Skagerrat (Richardson and Kullenberg, 1987).

The other major area that gets frequent blooms of K. mikimotoi is Japan (primarily the Seto Inland Sea), Hong Kong, and Korea. Although some blooms of K. mikimotoi occurred earlier in Japan (Oda, 1935; Honjo, 1994; Okaichi, 2004), major blooms leading to mortality of fish and pearl oysters began in 1965 and have continued with great frequency since then (Partensky et al., 1988; Okaichi, 1989; Honjo, 1994; Dahl and Tangen, 1993; Kimura et al., 1999). Most of these blooms occur in the Seto Inland Sea, but also occur elsewhere along the coasts of Japan (Matsuoka et al., 1989). They occur primarily in the summer when the water is stratified (Kimura et al., 1999). The increase in blooms after 1965 has been attributed to anthropogenic eutrophication, and a decline in these blooms in the 1980s and 1990s has been attributed to environmental regulation reducing that eutrophication (Prakesh, 1987; Kimura et al., 1999). The blooms appear to be associated with high rainfall and land runoff (Yanagi et al., 1992, 1995; Kimura et al., 1999). Imai et al. (2006) have argued that blooms of K. mikimotoi in the Seto Inland Sea occurred prior to the period of eutrophication in the 60s and 70s and thus it is considered an ‘inherent red tide species from ancient times’. Honjo et al. (1990) and Kimura et al. (1999) argued that the blooms are more prevalent where the bottom waters have gone anaerobic and it is shallow enough that the dinoflagellates can migrate to the bottom on a diel basis.

Lam and Ho (1989) document the large increase in HABs in Tolo Harbor, Hong Kong, some of which are K. mikimotoi. Blooms of K. mikimotoi typically occur around September to December (Wong, 1989). Interestingly, K. mikimotoi tends to bloom in the winter or spring in Port Shelter, Hong Kong (Wong, 1989), which suggests an effect of the interaction of seasonal changes in the wind direction and the orientation of the water bodies. The best documented bloom occurred in March and April 1998, killing large number of fish (Hodgkiss and Yang, 2001; Hodgkiss et al., 2001). The bloom included some K. digitata mixed in with the dominant K. mikimotoi (Lu and Hodgkiss, 2004). The bloom produced very thick mucus, which interfered with fish respiration (Dickman, 2001). It was associated with heavy rainfall (Yang and Hodgkiss, 2001). Wong (1989) suggested that the blooms were stimulated by organic compounds produced by fish cages in the area.

K. mikimotoi bloomed for the first time in Korea in the summer and fall of 1981 and killed a large amount of shellfish (Park et al., 1989; Kim et al., 1995). This bloom was composed of several algal species, of which K. mikimotoi was one. In 1984, another bloom of K. mikimotoi occurred in Korea (Partensky et al., 1988).

While the most blooms of K. mikimotoi appear to occur in Europe, Japan, and Hong Kong, sporadic blooms have occurred elsewhere. Mahoney et al. (1990) blooms that developed along the coast of New Jersey, USA in the late summer of both 1984 and 1985 when the weather was calm and water was stratified. Invertebrates were killed and humans experienced nausea, throat and eye irritation, and lung congestions. The blooms were densest at the coastline but extended offshore two to eight kilometers at lower concentrations.

A K. mikimotoi bloom was observed in the pycnocline in October (spring) 1988 off the coast of Argentina south of the Plata River (Negri, 1992), but no animal mortalities were observed.

12.9. K. selliformis in New Zealand, Chile and Kuwait

In 1994, and bloom of K. selliformis developed along the south coast of the South Island of New Zealand, leading to the death of many fish and shellfish (de Salas et al., 2005). K. selliformis formed monospecific blooms in the coastal waters of southern Chile around the Chiloe Archipelago in March and April (fall) 1999, killing large numbers of fish and shellfish (Clement et al., 2001; Carreto et al., 2001; Uribe and Ruiz, 2001). It was thought that this bloom started with low concentrations offshore that then greatly increased in abundance as the population was carried inshore. It was noted that temperatures were unusually high and rainfall was greatly reduced from normal at the time of the bloom. Blooms of K. selliformis killed large numbers of fish in Kuwait Bay in August and September 2001 (Heil et al., 2001). This developed only a few weeks after similar blooms developed upstream in the coastal waters of Iran. A large increase in nutrients was observed right before the bloom developed.

12.10. K. umbella and K. asterichroma in Tasmania

Along the southeast coast of Tasmania, a bloom composed of a mixture of K. umbella, K. asterichroma, and three unidentified species of Karenia developed in May (late fall) 2003, killing large number of fish (de Salas et al., 2004a, b).

12.11. K. digitata and K. longicanalis in Hong Kong and Japan

Blooms of K. digitata developed in the coastal waters of Hong Kong and western Japan in the summers of 1995 and 1996, causing large fish kills (Yang et al., 2000). In May 1998, a bloom of K. digitata developed in Hong Kong and it was followed two weeks later by a bloom of K. longicanalis (Yang et al., 2001). Both species were associated with large fish kills.

K. brevis blooms frequently in the Gulf of Mexico and K. mikimotoi blooms frequently in Europe, Japan, and Hong Kong. Blooms of the other species of Karenia appear to be very infrequent. This suggests that these species normally exist at very low concentrations, and form blooms only under very unusual circumstances. Blooms of all the Karenia species except K. brevis and K. mikimotoi have first appeared only in the past few decades. Were all these Karenia species simply overlooked in the past or have environmental conditions changed to support their occasional blooming?

12.13. Increase of Karenia blooms?

On a global scale, there is widespread agreement that Harmful Algal Blooms in general are increasing (Smayda, 1990, 2008; Hallegraeff, 1993; Glibert et al., 2005a, b; Anderson et al., 2002, 2008; Glibert and Burkholder, 2006; Heisler et al, 2008) and that anthropogenic nutrients are a major cause in many cases. Is this the case for Karenia?

Brand and Compton (2007) examined the monitoring data collected by the State of Florida (Florida Fish and Wildlife Research Institute, 2002) on K. brevis and concluded that its abundance had increased dramatically over the past 50 years. They argued that the only plausible source of the increased nutrients needed for this increased biomass was land runoff from anthropogenic sources. This increase parallels the increase in groundwater nutrients (Scott et al., 2006), coastal nutrients (Turner et al., 2006) and macroalgae (Lapointe and Bedford, 2007) observed along the west coast of Florida in recent decades. Kuhar et al. (2009) concluded that both scientists and the public believe that K. brevis blooms are increasing in frequency, geographic distribution, and persistence over time. Magaña et al. (2003) stated that there is a perception that K. brevis blooms along the Texas coast have increased as well.

Prakesh (1987) and Kimura et al. (1999) have argued that there has been a substantial increase in blooms of K. mikimotoi in the Seto Inland Sea of Japan that is related to eutrophication.

In the past two decades, a number of new species have been discovered, primarily as a result of mass mortality events and improved identification and molecular techniques. As a result, more species are likely to be described as a result of improving molecular techniques. Botes et al. (2003a) showed that K. cristata first bloomed in South Africa in 1988, killing large amounts of shellfish. De Salas et al. (2004a) describes new blooms of K. umbella in Tasmania, and other species of Karenia in Norway, Japan, New Zealand, Chile, and Hong Kong. Zingone et al. (2006) have documented the recent appearance of numerous toxic species of algae, including 5 species of Karenia that were not seen decades ago in the Mediterranean Sea. Heil et al. (2001) described a fish kill by a new Karenia species in Kuwait Bay. While many of these species may have lived in those ecosystems at low concentrations unnoticed, large blooms and fish kills are less likely to go unnoticed. In some cases, the spread of aquaculture and high concentrations of fish in cages might be a factor. In other cases, it seems plausible that anthropogenic eutrophication could be a factor leading to higher concentrations of these species that now cause problems and get noticed. As aquaculture expands and eutrophication increases, it is possible that Karenia blooms and associated fish kills could increase.

The development of Karenia blooms is obviously complex and poorly understood at this time. Because of their sporadic nature, it is difficult to determine if blooms have in fact increased over time, either in frequency or magnitude. Nutrients are only one of many factors that may be involved. Eutrophication may be involved in the increase of some Karenia blooms, but certainly not all.

13.1. Cell abundance and species-specific detection

The federal regulatory standard in the US for the closure of shellfish harvesting during Karenia brevis blooms is set at 5 × 10³ cells L⁻¹. Direct counts of water samples by light microscopy has been the primary method for detection and enumeration of K. brevis. This standard approach, however, is now complicated by observations that blooms may consist of multiple species, along with the inherent highly variable morphology of an individual species, which makes positive identifications by light microscopy difficult (Heil & Steidinger, 2009)

New technologies for Karenia detection include pigment based, optical, molecular, and imaging methods. Monitoring using pigment analysis by high performance liquid chromatography (HPLC) has been proposed based on the biomarker pigment gyroxanthin-diester (Richardson & Pickney, 2004). This pigment is found in other closely related gymnodinoid species of Karenia, as well as Karlodinium and Takayama (de Salas et al., 2003; 2005), so does not provide species-specific detection.

The Optical Plankton Detector (OPD, BreveBuster), developed for K. brevis, also relies on the unique absorption of spectrum of K. brevis to detect its presence in a mixed phytoplankton community (Kirkpatrick et al., 2000). Using stepwise discriminant analysis based on 4^th – derivative normalized absorption spectra, the OPD has been deployed on an automated underwater vehicle to provide greater spatial resolution for early detection of blooms (Robbins et al., 2006).

To improve taxonomic specificity and limit of detection, molecular techniques have proven to be invaluable. For example, nucleic acid sequence-based amplification (NASBA) approaches have been developed for K. brevis (Casper et al., 2004; 2007) and K. mikimotoi (Ulrich et al., 2010). Cell-based fluorescent in situ hybridization (FISH) assays have been developed for K. brevis (e.g. Mikulski et al., 2005) and cell-free hybridization assays for K. brevis, K. mikimotoi, K. selliformis, and K. papilionacea (Goodwin et al., 2005; Haywood et al., 2007). A multiplexed flow cytometric approach was carried on using the Luminex 100 platform and XMap technology to detect simultaneously 14 different species of dinoflagellates. This bead array method is based on color coded microspheres, which are conjugated to probes designed for each single species (Scorzetti et al., 2009). Recently the same technology was used with locked-nuclei acid modified capture probes for the detection of K. brevis and K. mikimotoi (Diaz et al., 2010). This flow cytometry-based technology has the potential for detection and quantification of multiple (up to 100) RNA targets simultaneously (Scorzetti et al., 2009; Diaz et al., 2010).

In addition, microsatellite markers have been developed for K. brevis (Henrichs et al., 2008; Renshaw et al. 2006) and K. mikimotoi (Nishitani et al., 2009). These hypervariable molecular markers are used to assess genetic diversity within and among bloom populations and to infer the relationship between populations.

One of the most promising new technologies for early warning of HABs is imaging-in-flow cytometry. This approach, using the Imaging Flow Cytobot (Olson & Sosik, 2007; Sosik & Olson, 2007) has provided valuable early warning capabilities for HABS, such as Dinophysis ovum (Campbell et al. 2010a) and K. brevis in the Gulf of Mexico (Campbell et al., 2010b). Although automated image classification is possible at the species-specific level in some cases, currently identification of Karenia is at the genus level. The variation in morphology, as discussed above, has limited the ability of the automated classifier (Sosik and Olson, 2007) to reliably distinguish among species of Karenia; however, the continuous and automated approach has permitted timely and successful early warning.

13.2. Satellite imagery of blooms

To assess the extent of Karenia blooms, data are needed at spatial and temporal scales not attainable by routine monitoring of cell counts. Satellite imagery was an obvious choice for HAB detection and has been used to detect blooms of Karenia worldwide for a number of years. Beginning in the 1970s, the Coastal Zone Color Scanner (CZCS) provided data for the Gulf of Mexico (Steidinger and Haddad, 1981). Subsequently the Sea-Viewing Wide Field-of-View Sensor/OrbView-2 (SeaWiFS), and most recently fluorescence data from Moderate Resolution Imaging Spectroradiometer (MODIS) on the Aqua satellite have been used (Hu et al., 2005; Vanhoutte-Brunier et al., 2008; Carvalho et al., 2010).

Satellite imagery for detection is limited, however, to surface (1 optical depth) and is obscured if clouds are present. More importantly, detection of chl a is not specific, as all phytoplankton contain chl a, and in coastal waters the signal can be influenced by resuspended sediments, colored dissolved organic material (CDOM) and bottom reflectance (Cannizzaro et al., 2008). Based on laboratory experiments, estimated detection for Karenia is limited to concentrations above 5 × 10⁴ Karenia cells l⁻¹ (Tester et al., 1998), so is not capable of early detection of bloom initiation. With the availability of SeaWIFS ocean color measurements, Stumpf proposed the chlorophyll anomaly method, which detects increases between a single image and the mean for the previous two months, as an index of K. brevis blooms (Stumpf et al., 2003; Tomlinson et al. 2004). Corrections for false positive predictions due to resuspension of benthic algae were developed by Wynne et al. (2005). Based on field observations of bio-optical properties, Cannizzaro et al. (2008) found the backscatter (b_b(λ)): chl a ratio was significantly lower for K. brevis, so proposed a classification scheme based on high chlorophyll and low backscatter to detect K. brevis. They also introduced the use of fluorescence line height (FLH) parameter from MODIS data. The combination of these approaches together with ancillary data from field observations (time series of abundance, winds, current and sea surface temperature) have been shown to improve ocean color forecasting (Hu et al., 2008). NOAA’s Harmful Algal Bloom Operational Forecast System (HAB-OFS) provides a weekly HAB Bulletin http://tidesandcurrents.noaa.gov/hab/bulletins.html) that uses daily ocean color satellite imagery together with field observations of cell counts and optical properties, buoy data, forecasted wind and current data to predict the location, development and extent of blooms. Evaluation of remote sensing techniques (Tomlinson et al., 2009), use of several satellite ocean color algorithms (Carvalho et al., 2011) and the capabilities of the HAB operational forecast system (Stumpf et al., 2009) have been reviewed recently.

Earth observation data have been used with some success in a study of a K. mikimotoi bloom in Scottish waters during 2006 (Davidson et al., 2009, Shutler et al., 2011) and provided complimentary information to support field measurements and cell counts about the origins and progress of the bloom. The data showed some potential to classify the bloom as K. mikimotoi and more work is needed to refine this tool so it can be implemented as a monitoring tool (Davidson et al., 2009, Shutler et al., 2011).

13.3. Toxins

To re-open commercial shellfish harvesting affected by K. brevis blooms, toxicity testing is required to verify toxin levels have returned to acceptable levels. The traditional method, the mouse bioassay (MBA) was first used by McFarren et al. (1965) to estimate risk to humans from consuming oysters contaminated with brevetoxin. A number of limitations of the MBA, including lack of specificity and sensitivity, as well as on ethical grounds (Plakas and Dickey 2010) have led to the search for a replacement.

Alternative methods for quantification of brevetoxin include both pharmacological and structural approaches (Baden and Adams, 2000; Poli, 2008). In shellfish, brevetoxins are extensively metabolized, so identification and determination of the toxicity of metabolites is also essential (Abraham et al., 2008; Plakas and Dickey, 2010). Pharmacological based assays include cytotoxicity, based on the activity of voltage gated sodium channel (e.g. Plakas et al., 2002; David et al., 2003; Wang et al., 2004), and receptor binding assays, based on the affinity of brevetoxin for sodium channels (Trainer and Poli, 2000; Van Dolah et al., 1994). Toxin detection based on structure of the compounds includes both immunological, such as the competitive ELISA to detect brevetoxins in K. brevis (Naar et al., 2002), or electrochemiluminescence (Poli et al., 2007), and LCMS (Poli et al., 2000; Errera et al., 2010). The advantages and disadvantages of these methods are reviewed by Plakas and Dickey (2010, and references therein).

Over the last decade, structural methods using LCMS have become essential for confirmation and increasingly for quantification (e.g. Errera et al., 2010). Although instrumentation was too expensive and of limited sensitivity just a decade ago (Baden and Adams, 2000), current instruments have increased sensitivity by orders of magnitude. As additional toxins are discovered and identified in new Karenia species, the importance of standards will continue to be an important concern.

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