Alexandrium Fundyense Cyst Research Articles

Near-bottom circulation and dispersion of sediment containing Alexandrium fundyense cysts in the Gulf of Maine during 2010–2011

The life cycle of Alexandrium fundyense in the Gulf of Maine includes a dormant cyst stage that spends the winter predominantly in the bottom sediment. Wave-current bottom stress caused by storms and tides induces resuspension of cyst-containing sediment during winter and spring. Resuspended sediment could be transported by water flow to different locations in the Gulf and the redistribution of sediment containing A. fundyense cysts could alter the spatial and temporal manifestation of its spring bloom. The present study evaluates model near-bottom flow during storms, when sediment resuspension and redistribution are most likely to occur, between October and May when A. fundyense cells are predominantly in cyst form. Simulated water column sediment (mud) concentrations from representative locations of the Gulf are used to initialize particle tracking simulations for the period October 2010–May 2011. Particles are tracked in full three-dimensional model solutions including a sinking velocity characteristic of cyst and aggregated mud settling (0.1mms−1). Although most of the material was redeposited near the source areas, small percentages of total resuspended sediment from some locations in the western (~4%) and eastern (2%) Maine shelf and the Bay of Fundy (1%) traveled distances longer than 100km before resettling. The redistribution changed seasonally and was sensitive to the prescribed sinking rate. Estimates of the amount of cysts redistributed with the sediment were small compared to the inventory of cysts in the upper few centimeters of sediment but could potentially have more relevance immediately after deposition.

Investigating the importance of sediment resuspension in Alexandrium fundyense cyst population dynamics in the Gulf of Maine

Cysts of Alexandrium fundyense, a dinoflagellate that causes toxic algal blooms in the Gulf of Maine, spend the winter as dormant cells in the upper layer of bottom sediment or the bottom nepheloid layer and germinate in spring to initiate new blooms. Erosion measurements were made on sediment cores collected at seven stations in the Gulf of Maine in the autumn of 2011 to explore if resuspension (by waves and currents) could change the distribution of over-wintering cysts from patterns observed in the previous autumn; or if resuspension could contribute cysts to the water column during spring when cysts are viable. The mass of sediment eroded from the core surface at 0.4Pa ranged from 0.05kgm−2 near Grand Manan Island, to 0.35kgm−2 in northern Wilkinson Basin. The depth of sediment eroded ranged from about 0.05mm at a station with sandy sediment at 70m water depth on the western Maine shelf, to about 1.2mm in clayey–silt sediment at 250m water depth in northern Wilkinson Basin. The sediment erodibility measurements were used in a sediment-transport model forced with modeled waves and currents for the period October 1, 2010 to May 31, 2011 to predict resuspension and bed erosion. The simulated spatial distribution and variation of bottom shear stress was controlled by the strength of the semi-diurnal tidal currents, which decrease from east to west along the Maine coast, and oscillatory wave-induced currents, which are strongest in shallow water. Simulations showed occasional sediment resuspension along the central and western Maine coast associated with storms, steady resuspension on the eastern Maine shelf and in the Bay of Fundy associated with tidal currents, no resuspension in northern Wilkinson Basin, and very small resuspension in western Jordan Basin. The sediment response in the model depended primarily on the profile of sediment erodibility, strength and time history of bottom stress, consolidation time scale, and the current in the water column. Based on analysis of wave data from offshore buoys from 1996 to 2012, the number of wave events inducing a bottom shear stress large enough to resuspend sediment at 80m ranged from 0 to 2 in spring (April and May) and 0 to 10 in winter (October through March). Wave-induced resuspension is unlikely in water greater than about 100m deep. The observations and model results suggest that a millimeter or so of sediment and associated cysts may be mobilized in both winter and spring, and that the frequency of resuspension will vary interannually. Depending on cyst concentration in the sediment and the vertical distribution in the water column, these events could result in a concentration in the water column of at least 104cystsm−3. In some years, resuspension events could episodically introduce cysts into the water column in spring, where germination is likely to be facilitated at the time of bloom formation. An assessment of the quantitative effects of cyst resuspension on bloom dynamics in any particular year requires more detailed investigation.

Alexandrium fundyense cysts in the Gulf of Maine: Long-term time series of abundance and distribution, and linkages to past and future blooms

Here we document Alexandrium fundyense cyst abundance and distribution patterns over nine years (1997 and 2004–2011) in the coastal waters of the Gulf of Maine (GOM) and identify linkages between those patterns and several metrics of the severity or magnitude of blooms occurring before and after each autumn cyst survey. We also explore the relative utility of two measures of cyst abundance and demonstrate that GOM cyst counts can be normalized to sediment volume, revealing meaningful patterns equivalent to those determined with dry weight normalization.Cyst concentrations were highly variable spatially. Two distinct seedbeds (defined here as accumulation zones with>300cystscm−3) are evident, one in the Bay of Fundy (BOF) and one in mid-coast Maine. Overall, seedbed locations remained relatively constant through time, but their area varied 3–4 fold, and total cyst abundance more than 10 fold among years. A major expansion of the mid-coast Maine seedbed occurred in 2009 following an unusually intense A. fundyense bloom with visible red-water conditions, but that feature disappeared by late 2010. The regional system thus has only two seedbeds with the bathymetry, sediment characteristics, currents, biology, and environmental conditions necessary to persist for decades or longer. Strong positive correlations were confirmed between the abundance of cysts in both the 0–1 and the 0–3cm layers of sediments in autumn and geographic measures of the extent of the bloom that occurred the next year (i.e., cysts→blooms), such as the length of coastline closed due to shellfish toxicity or the southernmost latitude of shellfish closures. In general, these metrics of bloom geographic extent did not correlate with the number of cysts in sediments following the blooms (blooms→cysts). There are, however, significant positive correlations between 0–3cm cyst abundances and metrics of the preceding bloom that are indicative of bloom intensity or vegetative cell abundance (e.g., cumulative shellfish toxicity, duration of detectable toxicity in shellfish, and bloom termination date). These data suggest that it may be possible to use cyst abundance to empirically forecast the geographic extent of the forthcoming bloom and, conversely, to use other metrics from bloom and toxicity events to forecast the size of the subsequent cyst population as the inoculum for the next year's bloom. This is an important step towards understanding the excystment/encystment cycle in A. fundyense bloom dynamics while also augmenting our predictive capability for this HAB-forming species in the GOM.

Bioturbation, germination and deposition of Alexandrium fundyense cysts in the Gulf of Maine

Like many other dinoflagellate species, Alexandrium fundyense possesses a benthic resting cyst which enables long-term persistence and annual blooms of this species in the Gulf of Maine. The size and extent of these harmful algal blooms are associated with high cyst concentrations in the top 1cm of sediment. Despite the importance of this resting stage in the life history of A. fundyense, little work has been done on bioturbation of cysts in the deep-water cyst beds of the western Gulf of Maine. Our work intensively examined one site within a major regional “seedbed” from February 2003 until August 2005, a time span that included an extraordinarily large bloom of A. fundyense in 2005.Over the course of 2 years we collected samples for benthic infauna and cyst profiles down to a depth of 30cm. We also measured sediment porosity, organic carbon, 210Pb, and porewater dissolved oxygen. On several dates we measured depth profiles of cyst autofluorescence. Profiles of cysts revealed large subsurface maxima peaking between 10 and 15cm depth with cyst concentrations declining strongly toward the sediment surface. On one sampling date (August 2004) we observed a cyst concentration peak at the sediment surface. Using these data we constructed a mechanistic model of cyst bioturbation, mortality, germination, and deposition. Modeled bioturbation was calibrated using 210Pb and modeled cyst profiles were compared to measured profiles. Model runs with constant and interannually-varying rates of cyst deposition produced similar time-averaged cyst profiles. Results indicate that the deeper portions of cyst profiles are determined primarily by bioturbation, germination and cyst mortality and less so by interannual variation in cyst depositional history. This is due to the relatively low sedimentation rate at the study site compared to the rate of bioturbation, and the fact that the number of cysts deposited each year tends to be a small fraction of the total inventory. Seasonal and interannual variation in cyst deposition strongly influenced concentrations of cysts in the top few millimeters of the sediment, however. When cyst deposition rates are low, bioturbation and germination are sufficient to rapidly deplete cysts in this surface layer, leaving relatively few cysts within the sediment depth range that allows germination. But, bioturbation is not rapid enough to homogenize surface sediments within one year. As a result, cyst deposition results in a concentration peak at the sediment surface that persists to fuel germination the following year. Because of this phenomenon, the model predicted that years with high rates of germination follow years with large levels of cyst deposition. Over longer time scales, bioturbation transports cysts from the sediment surface to depth, which, along with germination, creates a persistent subsurface maximum in cyst concentration. Bioturbation also serves to maintain persistence of A. fundyense by transporting older cysts from these deeper layers to the sediment surface where they can germinate. Since high concentrations of cysts near the sediment surface indicate large numbers of cysts deposited during the previous year, if enhanced germination leads to large blooms of A. fundyense, these blooms are predicted to occur in years following large cyst deposition events.

Thirty years – Alexandrium fundyense cyst, bloom dynamics and shellfish toxicity in the Bay of Fundy, eastern Canada

Sediment and water samples were collected for Alexandrium fundyense spatial and temporal distribution and abundance at more than 120 locations throughout the Bay of Fundy during the summers and winters of 1980–1984. These broad surveys have been repeated at various times through the past 30 years, with more regular sampling since 2004. In addition, A. fundyense abundance has been monitored at several locations within the Bay of Fundy at weekly intervals from April to November and monthly during the remaining months since 1988. Paralytic Shellfish Poisoning (PSP) toxins in shellfish (notably Mya arenaria) have also been monitored at multiple locations in the Bay of Fundy since 1943. The datasets were examined to determine relationships and roles between overwintering resting cysts, bloom initiation, bloom decline, motile cell dispersal and A. fundyense motile populations and resulting shellfish toxicity since 1980. Cysts are widely dispersed throughout the Bay of Fundy in the offshore, inshore and intertidal zones with the largest deposits located in the offshore in silt/clay sediments to the east and north of Grand Manan Island at depths of 60–180m. Results show that there is a constant stable source of cysts in the Bay of Fundy with highest concentrations of cysts (9780cystscm−3) observed in 2010 and highest concentrations of A. fundyense motile cells (18×106cellsL−1) observed in 1980. Interannual changes in abundance in A. fundyense populations, resting cysts and the temporal trends in M. arenaria toxicity are discussed. Results show that there was no relationship between the abundance of overwintering cysts and the magnitude of A. fundyense blooms. The offshore seed beds appear to be relatively constant in cyst density among most years and serve as an important source for the motile cells that lead to initiation of major blooms and resulting shellfish toxicity throughout the Bay of Fundy.

Benthic nepheloid layers in the Gulf of Maine and Alexandrium cyst inventories

Cysts residing in benthic nepheloid layers (BNLs) documented in the Gulf of Maine have been proposed as a possible source of inoculum for annual blooms of a toxic dinoflagellate in the region. Herein we present a spatially extensive data set of the distribution and thickness of benthic nepheloid layers in the Gulf of Maine and the abundance and inventories of suspended Alexandrium fundyense cysts within these near-bottom layers. BNLs are pervasive throughout the gulf and adjacent Bay of Fundy with maximum layer thicknesses of 50–60m observed. Mean BNL thickness is 30m in the eastern gulf and Bay of Fundy, and 20m in the western gulf. Cyst densities in the near-bottom particle resuspension layers varied by three orders of magnitude across the gulf with maxima of 105cystsm−3. An important interconnection of elevated BNL cyst densities is observed between the Bay of Fundy, the Maine Coastal Current and the south-central region of the gulf. BNL cyst inventories estimated for the eastern and western gulf are each on the order of 1015 cysts, whereas the BNL inventory in the Bay of Fundy is on the order of 1016. Although BNL cyst inventories in the eastern and western gulf are 1–2 orders of magnitude smaller than the abundance of cysts in the upper 1cm of sediment in those regions, BNL and sediment-bound cyst inventories are comparable in the Bay of Fundy. The existence of widespread BNLs containing substantial cyst inventories indicates that these near-bottom layers represent an important source of germinating A. fundyense cysts in the region.

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.

Categorizing the severity of paralytic shellfish poisoning outbreaks in the Gulf of Maine for forecasting and management

Development of forecasting systems for harmful algal blooms (HABs) has been a long-standing research and management goal. Significant progress has been made in the Gulf of Maine, where seasonal bloom forecasts are now being issued annually using Alexandrium fundyense cyst abundance maps and a population dynamics model developed for that organism. Thus far, these forecasts have used terms such as “significant”, “moderately large” or “moderate” to convey the extent of forecasted paralytic shellfish poisoning (PSP) outbreaks. In this study, historical shellfish harvesting closure data along the coast of the Gulf of Maine were used to derive a series of bloom severity levels that are analogous to those used to define major storms like hurricanes or tornados. Thirty-four years of PSP-related shellfish closure data for Maine, Massachusetts and New Hampshire were collected and mapped to depict the extent of coastline closure in each year. Due to fractal considerations, different methods were explored for measuring length of coastline closed. Ultimately, a simple procedure was developed using arbitrary straight-line segments to represent specific sections of the coastline. This method was consistently applied to each year’s PSP toxicity closure map to calculate the total length of coastline closed. Maps were then clustered together statistically to yield distinct groups of years with similar characteristics. A series of categories or levels was defined (“Level 1: Limited”, “Level 2: Moderate”, and “Level 3: Extensive”) each with an associated range of expected coastline closed, which can now be used instead of vague descriptors in future forecasts. This will provide scientifically consistent and simply defined information to the public as well as resource managers who make decisions on the basis of the forecasts.

Spatial and temporal variability of Alexandrium cyst fluxes in the Gulf of Maine: Relationship to seasonal particle export and resuspension

Quantification of Alexandrium cyst fluxes through the Gulf of Maine water column is central to understanding the linkage between the source and fate of annual Alexandrium blooms in the offshore waters. These blooms often lead to paralytic shellfish poisoning (PSP) and extensive closures of shellfish beds. We report here on time-series sediment trap deployments completed at four offshore locations in the gulf between 2005 and 2010 as components of two ECOHAB–GOM field programs. Data presented documents the substantial spatial and temporal fluctuations in Alexandrium fundyense cyst fluxes in the gulf. Cyst delivery out of the euphotic zone peaked primarily between July and August following annual spring–summer Alexandrium blooms and was greatest in the western gulf. At all sites, cyst flux maxima to the subsurface waters were rarely coincident with seasonal peaks in the total mass export of particulate material indicating that cyst delivery was primarily via individually sinking cysts. Where persistent benthic nepheloid layers (BNLs) exist, significant sediment resuspension input of cysts to the near-bottom water column was evidenced by deep cyst fluxes that were up to several orders of magnitude greater than that measured above the BNL. The largest cyst fluxes in the BNL were observed in the eastern gulf, suggesting greater resuspension energy and BNL cyst inventories in this region. Temporal similarities between peak cyst export out of the upper ocean and peak cyst fluxes in the BNL were observed and document the contribution of seasonal, newly formed cysts to the BNL. The data however also suggest that many Alexandrium cells comprising the massive, short-lived blooms do not transition into cysts. Time-series flow measurements and a simple 1D model demonstrate that the BNL cyst fluxes reflect the combined effects of tidal energy-maintained resuspension, deposition, and input of cysts from the overlying water column.

Alexandrium fundyense cyst dynamics in the Gulf of Maine

Abstract The flux of cells from germinated cysts is critical in the population dynamics of many dinoflagellates. Here, data from a large-scale cyst survey are combined with surveys in other years to yield an Alexandrium fundyense cyst distribution map for the Gulf of Maine that is massive in geographic extent and cyst abundance. The benthic cyst population extends nearly 500 km alongshore. Embedded within it are several distinct accumulation zones or “seedbeds,” each 3000–5000 km 2 in area. Maximal cyst abundances range from 2–20×10 6 cysts m −2 . Cysts are equally or more abundant in deeper sediment layers; nearshore, cysts are fewer by a factor of 10 or more. This cyst distribution reflects sedimentary dynamics and the location of blooms in overlying surface waters. The flux of germinated cells from sediments was estimated using a combination of laboratory measurements of cyst germination and autofluorescence and observations of cyst autofluorescence in the field. These measurements constrained a germination function that, when applied to the cyst distribution map, provided an estimate of the germination inoculum for a physical/biological numerical model. In the laboratory studies, virtually all cysts incubated at different temperatures and light regimes became autofluorescent, but the rate of development was slower at lower temperatures, with no difference between light and dark incubations. Germination rates were highest at elevated temperatures, and were 2-fold greater in the light than in the dark. Laboratory and field fluorescence measurements suggest that>70% of the cysts in the top cm of sediment would germinate over a 60–90 day period in offshore waters. The combination of laboratory germination experiments and numerical modeling predicts nearly 100% germination of cysts in the top cm of sediment and resulting early season cell concentrations that are comparable in magnitude to observed cell distributions. It cannot account for late-season peaks in cell abundance that are heavily influenced by vegetative growth. Cyst germination flux from deep-water (>50 m) cyst seedbeds is 14X the flux in shallow waters. A conceptual model is proposed that is consistent with observed and modeled A. fundyense cyst and motile cell distributions and dynamics in the Gulf of Maine. Cysts germinate within the Bay of Fundy seedbed, causing localized, recurrent blooms that are self-seeding and “propagatory” in nature, supplying cells that populate the eastern segment of the Maine Coastal Current (MCC) and eventually deposit cysts offshore of Penobscot and Casco Bays. These cysts serve as a seed population for western Maine blooms that are transported to the west by the western segment of the MCC, where cells are removed either by mortality or advection from the region. Without the localized, “incubator” characteristic of the Bay of Fundy bloom zone, A. fundyense populations in the Gulf of Maine should diminish through time. Their persistence over many decades highlights the effectiveness of the mechanisms described here.

Does uptake of Alexandrium fundyense cysts contribute to the levels of PSP toxin found in the sea scallop, Placopecten magellanicus?

Atlantic sea scallops, Placopecten magellanicus, in most areas of the Bay of Fundy, New Brunswick, Canada, have year-round concentrations of paralytic shellfish posioning (PSP) toxins greater than the regulatory concentration of 80 μg STX eq. 100 g −1 wet weight. Scallops (mean shell height of 10.7 cm, age 3–5 years) were collected by SCUBA and individually tagged near Parker Island, Bay of Fundy. Half were hung 2 m below the low tide water level and the remainder were placed on the bottom (11 m depth at low tide) under the scallops held at 2 m. Scallop, water and sediment samples were collected monthly for determination of concentrations of PSP toxins and Alexandrium fundyense. In October, 1993, mean concentrations of PSP toxins in digestive gland, and mantle were 3205 and 1018 μg STX eq. 100 g −1 wet weight, respectively. Eight months later (June 1994), PSP concentrations in digestive glands from the surface and bottom had declined to 504 and 682 μg STX eq. 100 g −1 wet weight, respectively, whereas those in the mantle had declined to 802 and 681 μg STX eq. 100 g −1 wet weight. During July 1994, A. fundyense concentrations observed at Parker Island and offshore were 320 cells l −1 and 14,200 cells l −1, respectively. Subsequently, toxin concentrations in surface and bottom scallop digestive glands increased to 12,720 and 11,408 μg STX eq. 100 g −1 wet weight, whereas concentrations in mantles increased to 2126 and 1748 μg STX eq. 100 g −1 wet weight, respectively. Concentrations of PSP toxins in these tissues in October 1994 were similar to those measured in October 1993. Concentrations of PSP toxin were less than the regulatory concentration in the gonads and non-detectable in adductor muscles of all scallops sampled. There were no statistically significant differences in profiles for uptake and depuration of PSP toxins in scallops held at the surface compared to those from bottom, suggesting that A. fundyense cysts at the concentrations found in the sediment (45 cysts cm −3) did not contribute significantly to the year-round presence of PSP toxins within scallop tissues. The year-round occurrence of PSP toxin is probably due to accumulation during summer blooms followed by a very slow rate of depuration.