Effects of Karenia brevis exposure on adult Mercenaria mercenaria: Histopathological and cellular responses in adults and effects on gamete and larval quality

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Neurotoxic shellfish poisoning

Blooms of K. brevis may cause neurotoxic shellfish poisoning (NSP) in humans, a rare and so far non-fatal condition typically caused by ingestion of brevetoxic filter feeding bivalve molluscs. The neurological and gastrointestinal symptoms of this poisoning include; reversal of hot and cold sensations, nausea, vomiting, diarrhoea, paraesthesia, cramps, bronchoconstriction, paralysis, seizures and coma (Poli et al., 2000; Watkins et al., 2008). NSP is not restricted to the GoM region, cases have also been recorded along the south east coast of the U.S. and even in New Zealand (in
New Zealand the causative organism was thought to be a similar Karenia species, K. concordia) (Chang et al., 2006; Haywood et al 2004; Steidinger et al., 2008; Tester et al., 1989). Non-filter feeding molluscs, such as whelks, and fish can also accumulate levels of PbTx toxic to humans, highlighting that NSP can also be caused by ingestion of species other than filter feeding bivalves (Poli et al., 2000; Naar et al., 2007).

Mortalities

Perhaps the most well-known and well reported impacts of K. brevis blooms are the significant mortalities of marine mammals, birds, fish and invertebrates, caused by exposure to toxic material through ingestion or as an aerosol (Flewelling et al., 2005; Gunter et al., 1948; Landsberg, 2002; Plakas and Dickey, 2010; Quick and Henderson, 1974; Shen et al., 2010; Steidinger and Ingle, 1972). The primary route of exposure for marine mammals and sea birds is thought to be via ingestion of toxic fish and shellfish that have been washed up on the shore or are floating in the sea (Forrester et al., 1977; Geraci, 1989; van Deventer et al., 2012). Lysing of the fragile K. brevis cells as they reach near-shore areas and are broken open by wave action also releases brevetoxin as an aerosol (Pierce et al., 1990, 2001). Breathing this toxic aerosol can cause respiratory irritation in humans and air breathing marine animals such as the Florida manatee, Trichechus manatus latirostris (Bossart et al., 1998; Pierce et al., 1986, 1990; Music et al., 1973).
Fish kills may occur when brevetoxin is absorbed across gill membranes (following lysis of the fragile K. brevis cell and release of the intracellular toxin), or from ingestion of toxic organisms (Abbott et al., 1975; Baden and Mende, 1982; Landsberg 2002; Naar et al., 2007; Shi et al., 2012; Steidinger et al., 1973; Quick and Henderson, 1974; Tester et al., 2000). Bloom concentrations as low as 100 cells mL-1 have been linked to fish kills (Finucane, 1964; Morton and Burklew, 1969; Starr, 1958; Steidinger and Ingle 1972; Steidinger 2009).
Severe invertebrate mortalities have also been reported and linked to K. brevis blooms (Gunter et al., 1947, 1948; Jefferson et al., 1879; Simon and Dauer, 1972; Summerson and Peterson, 1990; Taylor, 1917; Tiffany and Heyl, 1978). There have been mixed reports of the effects of K. brevis exposure on the same bivalve species. For example; Jefferson et al. (1879) and Gunter et al. (1947, 1948) reported mortalities in the eastern oyster, yet; Taylor (1917) and Steidinger and Ingle (1972) reported no effect on eastern oysters during historic K. brevis blooms which caused severe mortalities of other organisms such as fish, marine birds and mammals. These observations highlight the importance of reporting cell concentrations and other environmental data to differentiate between effects from K. brevis/ associated toxins and those attributable to other negative environmental factors which may be associated with blooms. For example; at least 5 other Karenia species have been found to co-occur in blooms of K. brevis, including K. mikimotoi and K. selliformis (Heil and Steidinger 2009; Steidinger et al., 1998, 2008b). These two algal species are known to produce other biotoxins. Gymnodimine (GYM), produced by K. selliformis, has been linked with fish kills (Table 1, Arzul et al., 1995; Gentien and Arzul, 1990; Seki et al., 1995; Steidinger et al., 2008a). In addition, the high biomass that sometimes accompanies blooms, may add mucilage and anoxia to the unfavorable environmental conditions (Brand et al., 2012).

Community structure

Blooms which result in these simultaneous lethal effects on marine organisms are only one aspect of K. brevis exposure. They also directly and indirectly alter the structure of the entire community. Declines in the recruitment of fish and bivalve species following blooms of K. brevis were observed by Flaherty and Landsberg (2011) and Summerson and Peterson (1990) respectively. Heil et al. (2004) and Meyer et al. (2014) observed changes in the microbial community structure during a bloom of K. brevis due to nutrient cycling by bacteria and mixotrophic grazing of K. brevis on bacteria. Finally, a long lasting (> 1 year) bloom altered the entire nekton community structure (Flaherty and Landsberg, 2011), highlighting that long-lasting blooms, even at low concentrations can cause a cascade of lethal and sublethal changes (Landsberg, 2002).

Sublethal effects and trophic transfer

Sublethal impacts may lead to an overall reduction in the fitness of an individual. Sublethal effects such as reduced feeding (Leverone et al., 2007), reproduction (Kubanek et al., 2007), development (Leverone et al., 2006) and physiological changes (Leverone, 2007) and; increased pathologies and impaired immune function (Bossart et al., 1998), have also been recorded in response to K. brevis exposure (Landsberg, 2002).
In addition, brevetoxin is fairly stable in the environment and can be accumulated and/ or transferred by organisms at many trophic levels, thus even in the absence of a bloom, negative effects may continue (Bricelj et al., 2012; Fire et al., 2007; Flewelling et al., 2005, 2010; Landsberg et al., 2009; Naar et al., 2007; Steidinger et al., 2008; Tester et al., 2000). For example, a lag time between K. brevis blooms and manatee mortalities was attributed to the consumption of still brevetoxic filter feeding organisms living on seagrass and PbTx associated directly with seagrass on which manatees feed (Flewelling et al., 2005; Landsberg and Steidinger, 1998). Poli et al. (2000) and Pierce et al. (2004) reported trophic transfer of PbTx from the filter-feeding bivalve, Mercenaria mercenaria, firstly to the whelk, Busycon contrarium, and then to humans (resulting in NSP).
The possible lethal and sublethal effects of exposure of bivalves to K. brevis and its associated toxins has been studied very little. Along the south west Florida (SW FL) coast, where K. brevis blooms are especially common, environmentally and economically important, bivalve species such as the eastern oyster (Crassostrea virginica) and the hard clam (= northern quahog, Mercenaria mercenaria) may be affected more than is currently realized. Several aspects of C. virginica and M. mercenaria physiology and life history mean encounters with K. brevis blooms are frequent. For these reasons they were chosen as study organisms in the current project.

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Bivalves and Karenia brevis

Importance

Bivalve molluscs filter large amounts of algae and other particles from the water column and so provide vital ecosystem services such as clearing the water of particles (allowing increased light penetration for aquatic vegetation), nutrient cycling and, provision of secondary habitat in shallow estuaries (sensu Burkholder and Shumway, 2012; Dame, 1993; Newell, 2004; Wells,1961). Bivalves also have important economic value. For example; eastern oyster (Crassostrea virginica) fisheries and hard clam (Mercenaria mercenaria) production contribute markedly to the economies of states bordering the GoM; notably in Florida. In 2012, landings of market size oysters on the Gulf coast of Florida alone were estimated at 1.5 x 103 tonnes, worth over $9.9 million (NMFS, 2012). In 2005, 4 x 104 tonnes of food size hard clams worth over $60 million were produced in the U.S., primarily in Virginia, Florida and Connecticut (United States Department of Agriculture (US DOA), 2005).

Distribution

The native ranges of C. virginica and M. mercenaria covers the temperate and sub-tropical eastern seaboard of north America; from the Gulf of St Lawrence, Canada, to the Gulf of Mexico (Palmer, 1927; Andrews, 1971; Abbott, 1974; Carlton and Mann, 1996; Yonge, 1960), although intentional and accidental introduction has expanded the range of these species throughout north America, Europe and Asia (Hanna, 1966; Heppell, 1961; Ruesink et al., 2005; Zhang et al., 2003). Both species live in near-shore and shallow estuary areas, plentiful along the Gulf coast of Florida.

Filter-feeding

The process of filter feeding is similar for both species. Water containing algal cells and other particles is pumped over the gills and cells are passed to the labial palps (Figure 4). Particle selection may occur at the palps, where algae (and other particles including dissolved organic matter, sediment and bacteria, Newell and Jordan, 1983) are either ingested through the mouth as slurry, or are rejected (Figure 4, Ward et al., 1994). Both bivalve species exhibit particle selection based on factors such as the size, shape, structure and compounds associated with the algal cell and, concentration of the particles in the water (including algae and sediment) (Tammes and Dral, 1955; Newell et al., 1989; Shumway and Cucci, 1987; Ward and Shumway, 2004). Bivalves may reject particles either without incorporation in pseudofeces, or more often as pseudofeces (Bricelj et al., 1998; Hégaret et al., 2007; Shumway et al., 1985; Shumway and Cucci 1987, Ward et al., 1997, Ward and Shumway, 2004).

Table of contents :

Part 1: Introduction to Karenia brevis and its effects:
1.1 Harmful algal blooms
1.2 Life cycle and growth of Karenia brevis
1.3 Toxins
1.4 Blooms
1.5.1 Effects: Neurotoxic shellfish poisoning
1.5.2 Mortalities
1.5.3 Community structure
1.5.4 Sublethal effects and trophic transfer
Part 2: Bivalves and Karenia brevis
2.1 Importance
2.2. Distribution
2.3 Filter feeding
2.4 Life cycle
2.5 Reproduction
2.6 Encounters with Karenia brevis
2.7 Brevetoxin accumulation
2.8 Sensitivity
2.9 Lethal and sublethal effects
2.10 Summary
Part 3: Objectives and Rationale
3.1 Objectives
3.2 Rationale
References
Chapter 1: Short and long-term effects of Karenia brevis exposure on Crassostrea virginica: Toxin accumulation and histopathological responses in adults and effects on gametogenesis, gamete and larval quality
Chapter 2: Effects of Karenia brevis exposure on adult Mercenaria mercenaria: Histopathological and cellular responses in adults and effects on gamete and larval quality
Chapter 3: Transfer of brevetoxin to the gametes of eastern oysters (Crassostrea virginica) and northern quahogs (= hard clam, Mercenaria mercenaria) following field exposure to Karenia brevis
Chapter 4: Effects of the red tide dinoflagellate, Karenia brevis, on early development of the eastern oyster Crassostrea virginica and northern quahog Mercenaria mercenaria
Chapter 5: Susceptibility of gametes and embryos of the eastern oyster, Crassostrea virginica, to Karenia brevis and its toxins

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