The effect of the toxic dinoflagellate Alexandrium fundyense on the fitness of the calanoid copepod Calanus finmarchicus.

Inshore and offshore waters of the Gulf of Maine (USA) have spring/summer harmful algal blooms (HABs) of the toxic dinoflagellate Alexandrium fundyense, which is responsible for paralytic shellfish poisoning (PSP) in humans. The calanoid copepod Calanus finmarchicus co-occurs with A. fundyense during the seasonal blooms. At that time, C. finmarchicus population abundances are high, dominated by immature copepods preparing for diapause, and by actively-reproducing adults. High survival has been reported for copepods exposed to toxic A. fundyense, but little is known about possible sublethal effects. In this study, C. finmarchicus adult females were fed either a control diet of non-toxic Rhodomonas spp. or one of two diets containing either low dose (LD) or high dose (HD) levels (50 and 200 cells mL-1, respectively) of toxic A. fundyense for a total of 7 days in two independent experiments. As expected, ingestion of the dinoflagellate had no effect on copepod survival and grazing activity. However, significant reductions of egg production and egg viability were observed in C. finmarchicus females fed on either experimental diet. After the 7-day experiment, total nauplius production by females on the LD and HD diets was reduced by 35% to 75% compared to the control females. These results suggest that blooms of A. fundyense in the Gulf of Maine may be an environmental challenge for C. finmarchicus populations, with a potential negative effect on copepod recruitment.

Zooplankton Community Grazing Impact on a Toxic Bloom of Alexandrium fundyense in the Nauset Marsh System, Cape Cod, Massachusetts, USA.

Embayments and salt ponds along the coast of Massachusetts can host localized blooms of the toxic dinoflagellate Alexandrium fundyense. One such system, exhibiting a long history of toxicity and annual closures of shellfish beds, is the Nauset Marsh System (NMS) on Cape Cod. In order measure net growth rates of natural A. fundyense populations in the NMS during spring 2012, incubation experiments were conducted on seawater samples from two salt ponds within the NMS (Salt Pond and Mill Pond). Seawater samples containing natural populations of grazers and A. fundyense were incubated at ambient temperatures. Concentrations of A. fundyense after incubations were compared to initial abundances to determine net increases from population growth, or decreases presumed to be primarily due to grazing losses. Abundances of both microzooplankton (ciliates, rotifers, copepod nauplii and heterotrophic dinoflagellates) and mesozooplankton (copepodites and adult copepods, marine cladocerans, and meroplankton) grazers were also determined. This study documented net growth rates that were highly variable throughout the bloom, calculated from weekly bloom cell counts from the start of sampling to bloom peak in both ponds (Mill Pond range = 0.12 - 0.46 d-1; Salt Pond range = -0.02 - 0.44 d-1). Microzooplankton grazers that were observed with ingested A. fundyense cells included polychaete larvae, rotifers, tintinnids, and heterotrophic dinoflagellates of the genera Polykrikos and Gymnodinium. Significant A. fundyense net growth was observed in two incubation experiments, and only a single experiment exhibited significant population losses. For the majority of experiments, due to high variability in data, net changes in A. fundyense abundance were not significant after the 24-hr incubations. However, experimental net growth rates through bloom peak were not statistically distinguishable from estimated long-term average net growth rates of natural populations in each pond (Mill Pond = 0.27 d-1 and Salt Pond = 0.20 d-1), which led to peak bloom concentrations on the order of 106 cells l-1 in both ponds. Experimental net growth rates from the incubations underestimated the observed natural net growth rates at several time intervals prior to bloom peak, which may indicate that natural populations experienced additional sources of vegetative cells or periods of reduced losses that the 24-hr incubation experiments did not capture, or that the experimental procedure introduced containment artifacts.

PSP toxin levels and plankton community composition and abundance in size-fractionated vertical profiles during spring/summer blooms of the toxic dinoflagellate Alexandrium fundyense in the Gulf of Maine and on Georges Bank, 2007, 2008, and 2010: 1. Toxin levels.

As part of the NOAA ECOHAB funded Gulf of Maine Toxicity (GOMTOX) project, we determined Alexandrium fundyense abundance, paralytic shellfish poisoning (PSP) toxin composition, and concentration in quantitatively-sampled size-fractionated (20-64, 64-100, 100-200, 200-500, and > 500 µm) particulate water samples, and the community composition of potential grazers of A. fundyense in these size fractions, at multiple depths (typically 1, 10, 20 m, and near-bottom) during 10 large-scale sampling cruises during the A. fundyense bloom season (May-August) in the coastal Gulf of Maine and on Georges Bank in 2007, 2008, and 2010. Our findings were as follows: (1) when all sampling stations and all depths were summed by year, the majority (94% ± 4%) of total PSP toxicity was contained in the 20-64 µm size fraction; (2) when further analyzed by depth, the 20-64 µm size fraction was the primary source of toxin for 97% of the stations and depths samples over three years; (3) overall PSP toxin profiles were fairly consistent during the three seasons of sampling with gonyautoxins (1, 2, 3, and 4) dominating (90.7% ± 5.5%), followed by the carbamate toxins saxitoxin (STX) and neosaxitoxin (NEO) (7.7% ± 4.5%), followed by n-sulfocarbamoyl toxins (C1 and 2, GTX5) (1.3% ± 0.6%), followed by all decarbamoyl toxins (dcSTX, dcNEO, dcGTX2&3) (< 1%), although differences were noted between PSP toxin compositions for nearshore coastal Gulf of Maine sampling stations compared to offshore Georges Bank sampling stations for 2 out of 3 years; (4) surface cell counts of A. fundyense were a fairly reliable predictor of the presence of toxins throughout the water column; and (5) nearshore surface cell counts of A. fundyense in the coastal Gulf of Maine were not a reliable predictor of A. fundyense populations offshore on Georges Bank for 2 out of the 3 years sampled.

PSP toxin levels and plankton community composition and abundance in size-fractionated vertical profiles during spring/summer blooms of the toxic dinoflagellate Alexandrium fundyense in the Gulf of Maine and on Georges Bank, 2007, 2008, and 2010: 2. Plankton community composition and abundance.

As part of the Gulf of Maine Toxicity (GOMTOX) project, we determined Alexandrium fundyense abundance, paralytic shellfish poisoning (PSP) toxin levels in various plankton size fractions, and the community composition of potential grazers of A. fundyense in plankton size fractions during blooms of this toxic dinoflagellate in the coastal Gulf of Maine and on Georges Bank in spring and summer of 2007, 2008, and 2010. PSP toxins and A. fundyense cells were found throughout the sampled water column (down to 50 m) in the 20-64 µm size fractions. While PSP toxins were widespread throughout all size classes of the zooplankton grazing community, the majority of the toxin was measured in the 20-64 µm size fraction. A. fundyense cellular toxin content estimated from field samples was significantly higher in the coastal Gulf of Maine than on Georges Bank. Most samples containing PSP toxins in the present study had diverse assemblages of grazers. However, some samples clearly suggested PSP toxin accumulation in several different grazer taxa including tintinnids, heterotrophic dinoflagellates of the genus Protoperidinium, barnacle nauplii, the harpacticoid copepod Microsetella norvegica, the calanoid copepods Calanus finmarchicus and Pseudocalanus spp., the marine cladoceran Evadne nordmanni, and hydroids of the genus Clytia. Thus, a diverse assemblage of zooplankton grazers accumulated PSP toxins through food-web interactions. This raises the question of whether PSP toxins pose a potential human health risk not only from nearshore bivalve shellfish, but also potentially from fish and other upper-level consumers in zooplankton-based pelagic food webs.