Blooms Of Alexandrium Fundyense Research Articles

Insights into the loss factors of phytoplankton blooms: The role of cell mortality in the decline of two inshore Alexandrium blooms.

While considerable effort has been devoted to understanding the factors regulating the development of phytoplankton blooms, the mechanisms leading to bloom decline and termination have received less attention. Grazing and sedimentation have been invoked as the main routes for the loss of phytoplankton biomass, and more recently, viral lysis, parasitism and programmed cell death (PCD) have been recognized as additional removal factors. Despite the importance of bloom declines to phytoplankton dynamics, the incidence and significance of various loss factors in regulating phytoplankton populations have not been widely characterized in natural blooms. To understand mechanisms controlling bloom decline, we studied two independent, inshore blooms of Alexandrium fundyense, paying special attention to cell mortality as a loss pathway. We observed increases in the number of dead cells with PCD features after the peak of both blooms, demonstrating a role for cell mortality in their terminations. In both blooms, sexual cyst formation appears to have been the dominant process leading to bloom termination, as both blooms were dominated by small-sized gamete cells near their peaks. Cell death and parasitism became more significant as sources of cell loss several days after the onset of bloom decline. Our findings show two distinct phases of bloom decline, characterized by sexual fusion as the initial dominant cell removal processes followed by elimination of remaining cells by cell death and parasitism.

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 to 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=0.12–0.46d−1; Salt Pond range=−0.02 to 0.44d−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-h 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=0.27d−1 and Salt Pond=0.20d−1), which led to peak bloom concentrations on the order of 106cellsl−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-h incubation experiments did not capture, or that the experimental procedure introduced containment artifacts.

Metatranscriptome profiling reveals versatile N-nutrient utilization, CO2 limitation, oxidative stress, and active toxin production in an Alexandrium fundyense bloom

The globally increasing trend of harmful algal blooms (HAB) is often attributed to coastal eutrophication and climate change, but the physiological processes at play during a bloom are poorly understood due to lack of in situ measurements of these processes or their corresponding molecular machinery. Here we employed a dinoflagellate spliced leader-based 454-pyrosequencing technique to generate time-serial expressed sequence tags (EST) throughout a diel cycle during an Alexandrium fundyense bloom in Long Island Sound. Assembly of the reads yielded 87,273 dinoflagellate genes. To facilitate mapping of these data to species and comparing of gene expression dynamics between natural bloom and laboratory culture conditions, similar diel EST sets were sequenced for A. fundyense strain CCMP1719, which achieved 31,451 genes. The assembled metatranscriptome reveals a metabolically active A. fundyense population. Relative to the laboratory culture, the natural bloom expressed more abundantly genes related to nitrogen (N)-scavenging, CO2-concentrating and saxitoxin production. Most strikingly, the data showed a versatility to exploit various sources of N (cyanate, urea, nitrate/nitrite, and ammonium), likely conferring competitive advantages in A. fundyense for bloom formation or maintenance. The dataset also led to the first characterization of Ni-containing superoxide dismutases (NiSODs) in dinoflagellates with mitochondrial targeting signal identified, which along with other types of SOD found indicated diverse SODs being expressed in the A. fundyense bloom. Our results also demonstrate that metatranscriptomics is an effective approach to unraveling physiological processes conducive to HAB outbreaks.

Ammonium and maintenance of bloom populations of Alexandrium fundyense in the Gulf of Maine and on Georges Bank: results of laboratory culture experiments

Blooms of the toxic dinoflagellate Alexandrium fundyense, responsible for paralytic shellfish poisoning, occur annually in the Gulf of MaineGeorges Bank region of the northwest Atlantic Ocean and often reach highest cell densities in surface waters depleted of nitrate, sug- gesting a dependence on recycled ammonium. We report here the results of batch culture exper- iments with A. fundyense designed to: (1) describe the kinetics of ammonium uptake and cell growth rates over a range of ammonium concentrations encompassing those observed in the Gulf of MaineGeorges Bank region; (2) compare rates of nitrate and ammonium uptake in the pres- ence of one another; and (3) determine whether growth rates of A. fundyense on ammonium at concentrations observed in the region are sufficient to maintain established bloom populations and the degree to which continued growth of the bloom populations may be sustained by ammo- nium. The resulting half-saturation constant for growth (Ks(g)) on ammonium was 0.93 µM, and the half-saturation constant for ammonium uptake (Ks(N)) was 1.74 µM. The maximum growth rate (μmax) was 0.51 d �1 , and the maximum cell-specific uptake rate (Vmax) was 7.0 × 10 �5 µmol NH4 + -N cell �1 d �1 . Based on these results we show that observed ammonium concentrations in the Gulf of MaineGeorges Bank region during A. fundyense blooms are sufficient to sustain the blooms for extended periods (weeks) and will allow modest continued growth.

A Quantitative Assessment of the Role of the Parasite Amoebophrya in the Termination of Alexandrium fundyense Blooms within a Small Coastal Embayment

Parasitic dinoflagellates of the genus Amoebophrya infect free-living dinoflagellates, some of which can cause harmful algal blooms (HABs). High prevalence of Amoebophrya spp. has been linked to the decline of some HABs in marine systems. The objective of this study was to evaluate the impact of Amoebophrya spp. on the dynamics of dinoflagellate blooms in Salt Pond (MA, USA), particularly the harmful species Alexandrium fundyense. The abundance of Amoebophrya life stages was estimated 3–7 days per week through the full duration of an annual A. fundyense bloom using fluorescence in situ hybridization coupled with tyramide signal amplification (FISH- TSA). More than 20 potential hosts were recorded including Dinophysis spp., Protoperidinium spp. and Gonyaulax spp., but the only dinoflagellate cells infected by Amoebophrya spp. during the sampling period were A. fundyense. Maximum A. fundyense concentration co-occurred with an increase of infected hosts, followed by a massive release of Amoebophrya dinospores in the water column. On average, Amoebophrya spp. infected and killed ∼30% of the A. fundyense population per day in the end phase of the bloom. The decline of the host A. fundyense population coincided with a dramatic life-cycle transition from vegetative division to sexual fusion. This transition occurred after maximum infected host concentrations and before peak infection percentages were observed, suggesting that most A. fundyense escaped parasite infection through sexual fusion. The results of this work highlight the importance of high frequency sampling of both parasite and host populations to accurately assess the impact of parasites on natural plankton assemblages.

Understanding interannual, decadal level variability in paralytic shellfish poisoning toxicity in the Gulf of Maine: The HAB Index

A major goal in harmful algal bloom (HAB) research has been to identify mechanisms underlying interannual variability in bloom magnitude and impact. Here the focus is on variability in Alexandrium fundyense blooms and paralytic shellfish poisoning (PSP) toxicity in Maine, USA, over 34 years (1978–2011). The Maine coastline was divided into two regions – eastern and western Maine, and within those two regions, three measures of PSP toxicity (the percent of stations showing detectable toxicity over the year, the cumulative amount of toxicity per station measured in all shellfish (mussel) samples during that year, and the duration of measurable toxicity) were examined for each year in the time series. These metrics were combined into a simple HAB Index that provides a single measure of annual toxin severity across each region. The three toxin metrics, as well as the HAB Index that integrates them, reveal significant variability in overall toxicity between individual years as well as long-term, decadal patterns or regimes. Based on different conceptual models of the system, we considered three trend formulations to characterize the long-term patterns in the Index – a three-phase (mean-shift) model, a linear two-phase model, and a pulse-decline model. The first represents a “regime shift” or multiple equilibria formulation as might occur with alternating periods of sustained high and low cyst abundance or favorable and unfavorable growth conditions, the second depicts a scenario of more gradual transitions in cyst abundance or growth conditions of vegetative cells, and the third characterizes a ”sawtooth” pattern in which upward shifts in toxicity are associated with major cyst recruitment events, followed by a gradual but continuous decline until the next pulse. The fitted models were compared using both residual sum of squares and Akaike's Information Criterion. There were some differences between model fits, but none consistently gave a better fit than the others. This statistical underpinning can guide efforts to identify physical and/or biological mechanisms underlying the patterns revealed by the HAB Index. Although A. fundyense cyst survey data (limited to 9 years) do not span the entire interval of the shellfish toxicity records, this analysis leads us to hypothesize that major changes in the abundance of A. fundyense cysts may be a primary factor contributing to the decadal trends in shellfish toxicity in this region. The HAB Index approach taken here is simple but represents a novel and potentially useful tool for resource managers in many areas of the world subject to toxic HABs.

Nutrients and water masses in the Gulf of Maine–Georges Bank region: Variability and importance to blooms of the toxic dinoflagellate Alexandrium fundyense

We report here the results of ten oceanographic survey cruises carried out in the Gulf of Maine–Georges Bank region of the Northwest Atlantic during the late spring to summer period in 2007, 2008 and 2010, for which we examine and characterize relationships among dissolved inorganic nutrient fields, water mass dynamics and cell densities of the toxic dinoflagellate Alexandrium fundyense. Nutrients are supplied to continental shelf waters of the Gulf of Maine–Georges Bank region by inflows of deep offshore water masses; once in the Gulf they are transported with the residual circulation and mix with surface waters, both in the Gulf and on the Bank. Those fluxes of offshore water masses and their nutrient loads are the major source of nutrients for phytoplankton production in the region, including annual blooms of A. fundyense in the Gulf and on Georges Bank. This much is already known. We suggest here that the locations and magnitude of A. fundyense blooms are controlled in part by variable nutrient fluxes to the interior Gulf of Maine from offshore, and, those interior Gulf of Maine waters are, in turn, the main nutrient source to Georges Bank, which are brought onto the Bank by tidal pumping on the Northern Flank. We present evidence that nitrate is the initial form of nitrogenous nutrient for A. fundyense blooms, but it is quickly depleted to limiting concentrations of less than 0.5µM, at which time continued growth and maintenance of the population is likely fueled by recycled ammonium. We also show that phosphate may be the limiting nutrient over much of Georges Bank in summer, allowing recycled ammonium concentrations to increase. Our temperature–salinity analyses reveal spatial and temporal (seasonal and interannual) variability in the relative proportions of two deep source waters that enter the Gulf of Maine at depth through the Northeast Channel: Warm Slope Water (WSW) and Labrador Slope Water (LSW). Those two source waters are known to vary in their nutrient loads, with nitrate concentrations about 50% higher in WSW than LSW, for example, and as such the proportions of these two water masses to one another are important determinants of the overall nutrient loads in the interior Gulf. In addition to these deep slope water fluxes, we show evidence here of episodic fluxes of relatively fresh and low-nutrient shelf waters from the Nova Scotian Shelf, which enter the Gulf in pulses at depths between the surface and approximately 150m, displacing deep slope waters, and consequently they significantly dilute the Gulf's interior waters, reducing nutrient concentrations and, in turn, affect the magnitude of A. fundyense blooms.

Alexandrium fundyense cyst viability and germling survival in light vs. dark at a constant low temperature

Both observations and models suggest that large-scale coastal blooms of Alexandrium fundyense in the Gulf of Maine are seeded by deep-bottom cyst accumulation zones (“seed beds”) where cysts germinate from the sediment surface or the overlying near-bottom nepheloid layers at water depths exceeding 100m. The germling cells and their vegetative progeny are assumed to be subject to mortality while in complete darkness, as they swim to illuminated surface waters. To test the validity of this assumption we conducted laboratory investigations of cyst viability and the survival of the germling cells and their vegetative progeny during prolonged exposure to darkness at a temperature of 6°C, simulating the conditions in deep Gulf of Maine waters. We isolated cysts from bottom sediments collected in the Gulf of Maine under low red light and incubated them in 96-well tissue culture-plates in culture medium under a 10:14h light:dark cycle and under complete darkness. Cyst viability was high, with excystment frequency reaching 90% in the illuminated treatment after 30 days and in the dark treatment after 50 days. Average germination rates were 0.062 and 0.038d−1 for light and dark treatments, respectively. The dark treatment showed an approximately 2-week time lag in maximum germination rates compared to the light treatment. Survival of germlings was considerably lower in the dark treatment. In the light treatments, 47% of germinated cysts produced germlings that were able to survive for 7 days and produce vegetative progeny, i.e., there were live cells in the well along with an empty cyst at least once during the experiment. In the dark treatments 12% of the cysts produced germlings that were able to survive for the same length of time. When dark treatments are scaled to take into account non-darkness related mortality, approximately 28% of the cysts produced germlings that were able to survive for at least 7 days. Even though cysts are able to germinate in darkness, the lack of illumination considerably reduces survival rate of germling cells. In addition to viability of cysts in surface sediments and the near-bottom nepheloid layer, survivability of germling cells and their vegetative progeny at aphotic depths is an important consideration in assessing the quantitative role of deep-coastal cyst seed beds in bloom formation.

The emergence of Dinophysis acuminata blooms and DSP toxins in shellfish in New York waters

The dynamics of Dinophysis acuminata and its associated diarrhetic shellfish poisoning (DSP) toxins, okadaic acid (OA) and dinophysistoxin-1 (DTX1) as well as pectenotoxins (PTXs), were investigated within plankton and shellfish in Northport Bay, NY, USA, over a four year period (2008–2011). Over the course of the study, Dinophysis bloom densities ranged from ~104 to 106cellsL−1 and exceeded 106L−1 in 2011 when levels of total OA, total DTX1, and PTX in the water column were 188, 86, and 2900pgmL−1, respectively, with the majority of the DSP toxins present as esters. These cell densities exceed – by two orders of magnitude – those previously reported within thousands of samples collected from NY waters from 1971 to 1986. The bloom species was positively identified as D. acuminata via scanning electron microscopy and genetic sequencing (cox1 gene). The cox1 gene sequence from the D. acuminata populations in Northport Bay was 100% identical to D. acuminata from Narragansett Bay, RI, USA and formed a strongly supported phylogenetic cluster (posterior probability=1) that included D. acuminata and Dinophysis ovum from systems along the North Atlantic Ocean. Shellfish collected from Northport Bay during the 2011 bloom had DSP toxin levels (1245ngg−1 total OA congeners) far exceeding the USFDA action level (160ngg−1 total OA of shellfish tissue) representing the first such occurrence on the East Coast of the U.S. D. acuminata blooms co-occurred with paralytic shellfish poisoning (PSP) causing blooms of Alexandrium fundyense during late spring each year of the study. D. acuminata cell abundances were significantly correlated with levels of total phytoplankton biomass and Mesodinium spp., suggesting food web interactions may influence the dynamics of these blooms. Given that little is known regarding the combined effects of DSP and PSP toxins on human health and the concurrent accumulation and depuration of these toxins in shellfish, these blooms represent a novel managerial challenge.

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)11Gulf of Maine TOXicity (GOMTOX) http://www.whoi.edu/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 >500μm) particulate water samples, and the community composition of potential grazers of A. fundyense in these size fractions, at multiple depths (typically 1, 10, 20m, 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 20–64μm size fraction; (2) when further analyzed by depth, the 20–64μm 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 (GOMTOX11Gulf of Maine TOXicity (GOMTOX) http://www.whoi.edu/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 50m) in the 20–64µm 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 20–64µm 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.

Seasonal and interannual variability in Gulf of Maine hydrodynamics: 2002–2011

In situ observations including long-term moored meteorological and oceanographic measurements and multi-year gulf-wide ship survey data are used to quantify interannual variability of surface wind, river runoff, and hydrographic conditions in the Gulf of Maine during summers 2002–2011. The cumulative upwelling index shows that upwelling (downwelling)-favorable wind conditions were most persistent in 2010 (2005) over the 10-year study period. River discharge was highest in 2005; peak runoff occurred in early April in 2010 as opposed to late April to middle May in other years. Moored time series show that coastal water temperature was 0.5–2°C warmer than average in summer 2010, and about 2°C colder than average in 2004. Coastal salinity in April 2010 was the lowest in the 10-year study period. Both moored Acoustic Doppler Current Profiler (ADCP) current measurements and dynamic height/geostrophic velocity calculations based on gulf-wide ship survey data show May–June 2010 had one of the weakest alongshore transports in the western Gulf of Maine during the 10-year study period, likely associated with intrusions of warm slope water and fresher-than-usual Scotian Shelf water. Comparisons of coastal currents to the Paralytic Shellfish Poisoning (PSP) closure maps resulting from Alexandrium fundyense blooms suggest a linkage between alongshore transport and the downstream extent of toxicity.

Suppression of the 2010 Alexandrium fundyense bloom by changes in physical, biological, and chemical properties of the Gulf of Maine.

For the period 2005-2009, the abundance of resting cysts in bottom sediments from the preceding fall was a first-order predictor of the overall severity of spring-summer blooms of Alexandrium fundyense in the western Gulf of Maine and southern New England. Cyst abundance off mid-coast Maine was significantly higher in fall 2009 than it was preceding a major regional bloom in 2005. A seasonal ensemble forecast was computed using a range of forcing conditions for the period 2004-2009, suggesting that a large bloom was likely in the western Gulf of Maine in 2010. This did not materialize, perhaps because environmental conditions in spring-summer 2010 were not favorable for growth of A.fundyense. Water mass anomalies indicate a regional-scale change in circulation with direct influence on A. fundyense's niche. Specifically, near-surface waters were warmer, fresher, more stratified, and had lower nutrients than during the period of observations used to construct the ensemble forecast. Moreover, a weaker-than-normal coastal current lessened A. fundyense transport into the western Gulf of Maine and Massachusetts Bay. Satellite ocean color observations indicate the 2010 spring phytoplankton bloom was more intense than usual. Early-season nutrient depletion may have caused a temporal mismatch with A. fundyense's endogenous clock that regulates the timing of cyst germination. These findings highlight the difficulties of ecological forecasting in a changing oceanographic environment, and underscore the need for a sustained observational network to drive such forecasts.

Dynamics of a mesoscale eddy off Cape Ann, Massachusetts in May 2005

Observations and numerical modeling indicate that a mesoscale anti-cyclonic eddy formed south of Cape Ann at the northern entrance of Massachusetts Bay (MB) during May 2005, when large river discharges in the western Gulf of Maine and two strong Nor'easters passing through the regions led to an unprecedented toxic Alexandrium fundyense bloom (red tide). Both model results and field measurements suggest that the western Maine Coastal Current separated from Cape Ann around May 7–8, and the eddy formed on around May 10. The eddy was trapped at the formation location for about a week before detaching from the coastline and moving slowly southward on May 17. Both model results and theoretical analysis suggest that the separation of the coastal current from the coast and subsequent eddy formation were initiated at the subsurface by an adverse pressure gradient between Cape Ann and MB due to the higher sea level set up by onshore Ekman transport and higher density in downstream MB. After the formation, the eddy was maintained by the input of vorticity transported by the coastal current from the north, and local vorticity generation around the cape by the horizontal gradients of wind-driven currents, bottom stress, and water density induced by the Merrimack River plume. Observations and model results indicate that the anti-cyclonic eddy significantly changed the pathway of nutrient and biota transport into the coastal areas and enhanced phytoplankton including Alexandrium abundances around the perimeter of the eddy and in the western coast of MB.

Dynamics of Alexandrium fundyense blooms and shellfish toxicity in the Nauset Marsh System of Cape Cod (Massachusetts, USA)

Paralytic Shellfish Poisoning (PSP) toxins are annually recurrent along the Massachusetts coastline (USA), which includes many small embayments and salt ponds. Among these is the Nauset Marsh System (NMS), which has a long history of PSP toxicity. Little is known, however, about the bloom dynamics of the causative organism Alexandrium fundyense within that economically and socially important system. The overall goal of this work was to characterize the distribution and dynamics of A. fundyense blooms within the NMS and adjacent coastal waters by documenting the distribution and abundance of resting cysts and vegetative cells. Cysts were found predominantly in three drowned kettle holes or salt ponds at the distal ends of the NMS – Salt Pond, Mill Pond, and Town Cove. The central region of the NMS had a much lower concentration of cysts. Two types of A. fundyense blooms were observed. One originated entirely within the estuary, seeded by cysts in the three seedbeds. These blooms developed independently of each other and of the A. fundyense population observed in adjacent coastal waters outside the NMS. The temporal development of the blooms was different in the three salt ponds, with initiation differing by as much as 30 days. These differences do not appear to reflect the initial cyst abundances in these locations, and may simply result from higher cell retention and higher nutrient concentrations in Mill Pond, the first site to bloom. Germination of cysts accounted for a small percentage of the peak cell densities in the ponds, so population size was influenced more by the factors affecting growth than by cyst abundance. Subsurface cell aggregation (surface avoidance) limited advection of the vegetative A. fundyense cells out of the salt ponds through the shallow inlet channels. Thus, the upper reaches of the NMS are at the greatest risk for PSP since the highest cyst abundances and cell concentrations were found there. After these localized blooms in the salt ponds peaked and declined, a second, late season bloom occurred within the central portions of the NMS. The timing of this second bloom relative to those within the salt ponds and the coastal circulation patterns at that time strongly suggest that those cells originated from a regional A. fundyense bloom in the Gulf of Maine, delivered to the central marsh from coastal waters outside the NMS through Nauset Inlet. These results will guide policy decisions about water quality as well as shellfish monitoring and utilization within the NMS and highlight the potential for “surgical” closures of shellfish during PSP events, leaving some areas open for harvesting while others are closed.

Diversity and dynamics of a widespread bloom of the toxic dinoflagellate Alexandrium fundyense.

Historically, cosmopolitan phytoplankton species were presumed to represent largely unstructured populations. However, the recent development of molecular tools to examine genetic diversity have revealed differences in phytoplankton taxa across geographic scales and provided insight into the physiology and ecology of blooms. Here we describe the genetic analysis of an extensive bloom of the toxic dinoflagellate Alexandrium fundyense that occurred in the Gulf of Maine in 2005. This bloom was notable for its intensity and duration, covering hundreds of kilometers and persisting for almost two months. Genotypic analyses based on microsatellite marker data indicate that the open waters of the northeastern U.S. harbor a single regional population of A. fundyense comprising two genetically distinct sub-populations. These subpopulations were characteristic of early- and late-bloom samples and were derived from the northern and southern areas of the bloom, respectively. The temporal changes observed during this study provide clear evidence of succession during a continuous bloom and show that selection can act on the timescale of weeks to significantly alter the representation of genotypes within a population. The effects of selection on population composition and turnover would be magnified if sexual reproduction were likewise influenced by environmental conditions. We hypothesize that the combined effects of differential growth and reproduction rates serves to reduce gene flow between the sub-populations, reinforcing population structure while maintaining the diversity of the overall regional population.

Zooplankton community grazing impact on a bloom of Alexandrium fundyense in the Gulf of Maine

Shipboard grazing experiments were conducted in the Gulf of Maine and on Georges Bank during of June 2006 to estimate zooplankton community grazing impact on a natural bloom of the toxic dinoflagellate Alexandrium fundyense. Surface seawater samples containing natural populations of grazers and A. fundyense from 23 stations were incubated at ambient temperatures. Concentrations of A. fundyense after incubations were compared to those at the start of each experiment to determine net increases due to population growth, or decreases presumed to be primarily due to grazing losses. Abundances of both microzooplankton (tintinnids, oligotrich ciliates, rotifers, copepod nauplii and heterotrophic dinoflagellates) and mesozooplankton (copepod nauplii, copepodites and adult copepods, rotifers, marine cladocerans, and meroplankton) grazers in experimental aliquots were also determined. The total zooplankton community had minimal grazing impact on natural populations of A. fundyense at most stations. At 70% of the stations where grazing experiments were performed, there were no significant differences in initial and final concentrations of A. fundyense. This indicated that growth of, and grazing on A. fundyense were in approximate balance. At 2 stations, which had the highest A. fundyense abundances of the cruise (>10 4 cells l −1), % of the A. fundyense population grazed per day was significantly negative, indicating that net population growth of A. fundyense exceeded grazing losses. At 5 stations, which had low concentrations of A. fundyense (10 2–10 3 cells l −1), % of the A. fundyense population grazed per day was significantly positive, indicating that losses of A. fundyense due to grazing exceeded net population growth. For stations with significant differences between Initial and Grazed concentrations of A. fundyense, grazing had the greatest impact at lower concentrations of A. fundyense, and grazing impact by the larger mesozooplankton was inversely related to zooplankton abundance. There was no relationship between microzooplankton abundance and grazing impact on A. fundyense. Grazing exceeded growth only where A. fundyense abundance was low, and growth exceeded grazing only where A. fundyense abundance was high. The inverse relationship between grazing impact and A. fundyense abundance implies that grazing may be capable of retarding bloom development at low concentrations typical of the early stages of a bloom, but at higher concentrations once a bloom becomes established, either grazing maintains a balance with A. fundyense growth, or growth exceeds grazing losses at highest concentrations.

The influence of anthropogenic nitrogen loading and meteorological conditions on the dynamics and toxicity of Alexandrium fundyense blooms in a New York (USA) estuary

The goal of this two-year study was to explore the role of nutrients and climatic conditions in promoting reoccurring Alexandrium fundyense blooms in the Northport-Huntington Bay complex, NY, USA. A bloom in 2007 was short and small (3 weeks, 10 3 cells L −1 maximal density) compared to 2008 when the A. fundyense bloom, which persisted for 6 weeks, achieved cell densities >10 6 cells L −1 and water column saxitoxin concentrations >2.4 × 10 4 pmol STX eq. L −1. During the 2008 bloom, both deployed mussels (used as indicator species) and wild soft shell clams became highly toxic (1400 and 600 μg STX eq./100 g shellfish tissue, respectively) resulting in the closure of shellfish beds. The densities of benthic A. fundyense cysts at the onset of this bloom were four orders of magnitude lower than levels needed to account for observed cell densities, indicating in situ growth of vegetative cells was responsible for elevated bloom densities. Experimental enrichment of bloom water with nitrogenous compounds, particularly ammonium, significantly increased A. fundyense densities and particulate saxitoxin concentrations relative to unamended control treatments. The δ 15N signatures (12–23‰) of particulate organic matter (POM) during blooms were similar to those of sewage (10–30‰) and both toxin and A. fundyense densities were significantly correlated with POM δ 15N ( p < 0.001). These findings suggest A. fundyense growth was supported by a source of wastewater such as the sewage treatment plant which discharges into Northport Harbor. Warmer than average atmospheric temperatures in the late winter and spring of 2008 and a cooler May contributed to an extended period of water column temperatures optimal for A. fundyense growth (12–20 °C), and thus may have also contributed toward the larger and longer bloom in 2008. Together this evidence suggests sewage-derived N loading and above average spring temperatures can promote intense and toxic A. fundyense blooms in estuaries.

Investigation of the 2006 Alexandrium fundyense bloom in the Gulf of Maine: In-situ observations and numerical modeling

In-situ observations and a coupled bio-physical model were used to study the germination, initiation, and development of the Gulf of Maine (GOM) Alexandrium fundyense bloom in 2006. Hydrographic measurements and comparisons with GOM climatology indicate that 2006 was a year with normal coastal water temperature, salinity, current and river runoff conditions. A. fundyense cyst abundance in bottom sediments preceding the 2006 bloom was at a moderate level compared to other recent annual cyst survey data. We used the coupled bio-physical model to hindcast coastal circulation and A. fundyense cell concentrations. Field data including water temperature, salinity, velocity time series and surface A. fundyense cell concentration maps were applied to gauge the model's fidelity. The coupled model is capable of reproducing the hydrodynamics and the temporal and spatial distributions of A. fundyense cell concentration reasonably well. Model hindcast solutions were further used to diagnose physical and biological factors controlling the bloom dynamics. Surface wind fields modulated the bloom's horizontal and vertical distribution. The initial cyst distribution was found to be the dominant factor affecting the severity and the interannual variability of the A. fundyense bloom. Initial cyst abundance for the 2006 bloom was about 50% of that prior to the 2005 bloom. As the result, the time-averaged gulf-wide cell concentration in 2006 was also only about 60% of that in 2005. In addition, weaker alongshore currents and episodic upwelling-favorable winds in 2006 reduced the spatial extent of the bloom as compared with 2005.

Gulf of Maine Harmful Algal Bloom in summer 2005 - Part 2: Coupled Bio-physical Numerical Modeling.

A coupled physical/biological modeling system was used to hindcast the 2005 Alexandrium fundyense bloom in the Gulf of Maine and investigate the relative importance of factors governing the bloom's initiation and development. The coupled system consists of a state-of-the-art, free-surface primitive equation Regional Ocean Modeling System (ROMS) tailored for the Gulf of Maine (GOM) using a multi-nested configuration, and a population dynamics model for A. fundyense. The system was forced by realistic momentum and buoyancy fluxes, tides, river runoff, observed A. fundyense benthic cyst abundance, and climatological nutrient fields. Extensive comparisons were made between simulated (both physical and biological) fields and in-situ observations, revealing that the hindcast model is capable of reproducing the temporal evolution and spatial distribution of the 2005 bloom. Sensitivity experiments were then performed to distinguish the roles of three major factors hypothesized to contribute to the bloom: 1) the high abundance of cysts in western GOM sediments; 2) strong northeaster storms with prevailing downwelling-favorable winds; and 3) a large amount of fresh water input due to abundant rainfall and heavy snowmelt. Results suggested that the high abundance of cysts in western GOM was the primary factor of the 2005 bloom. Wind forcing was an important regulator, as episodic bursts of northeast winds caused onshore advection of offshore populations. These downwelling favorable winds accelerated the alongshore flow, resulting in transport of high cell concentrations into Massachusetts Bay. A large regional bloom would still have happened, however, even with normal or typical winds for that period. Anomalously high river runoff in 2005 resulted in stronger buoyant plumes/currents, which facilitated the transport of cell population to the western GOM. While affecting nearshore cell abundance in Massachusetts Bay, the buoyant plumes were confined near to the coast, and had limited impact on the gulf-wide bloom distribution.