Brown tide alga, Aureococcus anophagefferens, can affect growth but not survivorship of Mercenaria mercenaria larvae

Since the collapse of populations of northern quahogs (hard clam), Mercenaria mercenaria, in Long Island bays, brown tide blooms have been proposed to pose a barrier to recovery. We tested whether the brown tide alga, Aureococcus anophagefferens, affects survivorship, development or growth in the larvae of M. mercenaria. There was no effect of A. anophagefferens (clone CCMP1708) on survivorship of hard clam larvae, even at bloom concentrations. Under most experimental conditions, larvae fed a mixed diet of Isochrysis galbana (T-Iso) and A. anophagefferens or a single species diet of A. anophagefferens, developed faster than those fed a single species diet of Isochrysis. A mixed diet of I. galbana and A. anophagefferens either had no effect on larval growth, or produced enhanced growth at moderate cell densities (8 × 10⁴ cells ml⁻¹ of A. anophagefferens). Similarly, moderate cell densities of a single food diet of A. anophagefferens (1.6 × 10⁵ cells ml⁻¹) generally had no effect on the growth of larvae. When fed bloom concentrations (10⁶ cells ml⁻¹) of A. anophagefferens, larvae developed faster, but growth was reduced, compared to those fed an equal biovolume of Isochrysis. Larvae fed slow growing or near stationary phase cultures of A. anophagefferens experienced reduced growth and slowed development. These data suggest a qualitative difference between slow or stationary phase and fast growing cultures of the brown tide alga. They also suggest that impacts of A. anophagefferens, when present, are likely to be due to the nutritional quality of this alga as a food source for hard clam larvae, which could have a lasting legacy through ontogeny. Additional studies are needed to test whether our findings apply to more recently isolated strains of A. anophagefferens.     

HPLC pigment records provide evidence of past blooms of Aureococcus anophagefferens in the Coastal Bays of Maryland and Virginia, USA

Concentrations of the accessory phytoplankton pigment 19′-butanoyloxyfucoxanthin (but-fuco), derived from archived high performance liquid chromatography (HPLC) data from the Atlantic coastal bays of Maryland and Virginia (1993–1995 and 1999–2002), were used to determine the presence of Aureococcus anophagefferens at 18 stations. Paired data of direct cell counts of A. anophagefferens and but-fuco concentration data from 2000 to 2002 were linearly regressed (R² = 0.78). This regression was used to estimate historical cell densities from 1994 to 1995 and to improve the spatial resolution from 1999 to 2002. Although the HPLC method used did not permit quantification of but-fuco before 1994, the records indicate that qualitatively A. anophagefferens was present in 1993. Quantitative measurements grouped into bloom index categories showed that annually, peak densities occurred in May to July. Severe Category 3 blooms (>200,000 cells ml⁻¹) were found in 1995, 2001, and 2002. Spatially, concentrations of but-fuco were higher in the northern extent of the study region than in the lower Chincoteague Bay, and along the western shore of Chincoteague Bay than on the eastern side. On an interannual basis, it appeared that A. anophagefferens became more geographically widespread and blooms more intense throughout the study period.     

Interaction of nitrogen source and light intensity on the growth and photosynthesis of the brown tide alga Aureococcus anophagefferens

High ratios of dissolved organic nitrogen (DON) to dissolved inorganic nitrogen (DIN) have been suggested to favor the growth of the brown tide alga Aureococcus anophagefferens. DON could provide a particular advantage in low light levels, as occur when blooms induce self-shading. We examined the effects of varying DON:DIN ratios on the photosynthetic abilities of cultured Aureococcus at two light intensities, 93 and 17 μmol photons m⁻² s⁻¹. Glutamic acid and urea were used as DON sources, and the remainder of the nitrogen was added as nitrate.In experiments examining Aureococcus growth with varying ratios of DON_Glu:DIN_Nitrate at two light intensities in batch culture, higher growth rates and biomass were observed in treatments containing DIN than in those with DON only, which contrasts with the results of previous studies. In semi-continuous growth experiments with varying DON_Urea:DIN_Nitrate ratios, low light cultures with urea had higher growth rates than those without urea. Also, the effective target area for light absorption per cell and photosystem II efficiency were greater for the low light cultures of each nutrient treatment, particularly when DON:DIN mixtures (33 and 67% N_Urea) were used. The same pattern was seen in the maximum photosynthetic rates per cell in the light-saturated (P_m^cell) and in the initial slope (α^cell) of the PE (photosynthesis versus irradiance) curve, and in PON, POC and chlorophyll a cell⁻¹. This indicates that the ability of Aureococcus to acclimate to low light conditions may be enhanced by the presence of both organic and inorganic nitrogen sources. These results suggest that Aureococcus physiology and photosynthesis are different during growth on a mixture of urea-N and nitrate than when either nitrogen source is present alone. Results of this study suggest that Aureococcus may not respond to all DON substrates in the same way, and that mixtures of DON and DIN may provide for higher photosynthetic rates, especially at low light. Our results did not, however, support earlier suggestions that growth on DON alone provides the brown tide alga with a large advantage at low light levels.     

Assessment of brown tide blooms, caused by Aureococcus anophagefferens, and contributing factors in New Jersey coastal bays: 2000–2002

A 3 year study (2000–2002) in Barnegat Bay-Little Egg Harbor (BB/LEH), New Jersey (USA), was conducted by the New Jersey Department of Environmental Protection, Division of Science Research and Technology (DSRT) in cooperation with several partners to assess brown tide blooms in coastal waters in NJ. Water samples were collected by boat and helicopter at coastal stations from 2000 to 2002 along with field measurements. Aureococcus anophagefferens were enumerated and associated environmental factors were analyzed. A. anophagefferens abundances were classified using the Brown Tide Bloom Index and mapped, along with salinity and temperature parameters, to their geo-referenced location using the ArcView GIS. The highest A. anophagefferens abundances (>10⁶ cells ml⁻¹), including category 3 blooms (≥200,000 cells ml⁻¹) and category 2 blooms (≥35,000 to ≤200,000 cells ml⁻¹), recurred during each of the 3 years of sampling and covered significant geographic areas of the estuary, especially in Little Egg Harbor. While category 3 blooms were generally associated with warmer water temperatures (>16 °C) and higher salinity (>25–26 ppt), these factors were not sufficient alone to explain the timing or distribution of A. anophagefferens blooms. There was no significant relationship between brown tide abundances and dissolved organic nitrogen measured in 2002 but this was consistent with other studies. Extended drought conditions, with corresponding low freshwater inputs and elevated bay water salinities, occurring during this time were conducive to blooms. A. anophagefferens abundances were well above the reported levels that have been reported to cause negative impacts on shellfish. It was shown that over 50% of the submerged aquatic vegetation (SAV) habitat located in Barnegat Bay/Little Egg Harbor was categorized as having a high frequency of category 2 or 3 blooms for all 3 years.     

Ecology of phytoplankton communities dominated by Aureococcus anophagefferens: the role of viruses, nutrients, and microzooplankton grazing

We investigated the impact of viruses, nutrient loading, and microzooplankon grazing on phytoplankton communities in two New York estuaries that hosted blooms of the brown tide alga Aureococcus anophagefferens during 2000 and 2002. The absence of a bloom at one location during 2002 allowed for the fortuitous comparison of a bloom and non-bloom year at the same location as well as a comparison of two sites experiencing bloom and non-bloom conditions during the same year. During the study, blooms were found at locations with high levels of dissolved organic nitrogen and lower nitrate concentrations compared to a non-bloom location. Experimental additions of inorganic nitrogen and phosphorus yielded growth rates within the total phytoplankton community which significantly exceeded control treatments in 83% of experiments, while A. anophagefferens experienced significantly increased growth during only 20% of experimental inorganic nutrient additions. Consistent with prior research, these results suggest brown tides are not caused by eutrophication, but instead are more likely to occur when sources of labile DOM are readily available. Microzooplankton grazing rates on the total phytoplankton community during a bloom were lower than grazing rates at a non-bloom site, and grazing rates on A. anophagefferens were lower than grazing rates on the total community on some dates, suggesting that reduced grazing mortality may also promote brown tides. Mean densities of viruses during blooms (3 × 10⁸ ml⁻¹) were elevated compared to most estuarine environments and were twice the levels found at a non-bloom site. Experimental enrichment of the natural viral densities yielded a significant increase in A. anophagefferens growth rates relative to control treatments when background levels of viruses were low (<1.7 × 10⁸ ml⁻¹), suggesting that viruses may promote bloom occurrence by regenerating DOM or altering the composition of microbial communities.     

Microbial herbivory on the brown tide alga, Aureococcus anophagefferens: results from natural ecosystems, mesocosms and laboratory experiments

Experiments were conducted with natural plankton assemblages from two areas in Great South Bay (GSB) and the Peconic Bays Estuary System, NY, to compare the rates of growth and pelagic grazing mortality of Aureococcus anophagefferens with co-occurring phytoplankton. We hypothesized that A. anophagefferens would experience low mortality rates by microbial herbivores (relative to feeding pressure on other algae) thus providing it with a competitive advantage within the phytoplankton community. In fact, substantial rates of mortality were observed in nearly every experiment in our study. However, mortality rates of A. anophagefferens were less than intrinsic growth rates of the alga during late spring and early summer in Great South Bay, resulting in positive net growth rates for the alga during that period. This timing coincided with the development of a brown tide in this estuary. Similarly, growth rates of the alga also exceeded mortality rates during bloom development in natural plankton assemblages from the Peconic Bays Estuary System held in mesocosms. In contrast to the situation for A. anophagefferens, growth rates of the total phytoplankton assemblage, and another common picoplanktonic phytoplankter (Synechococcus spp.), were frequently less than their respective mortality rates. Mortality rates of A. anophagefferens in both systems were similar to growth rates of the alga during later stages of the bloom. Laboratory studies confirmed that species of phagotrophic protists that consume A. anophagefferens (at least in culture) are present during brown tides but preference for or against the alga appears to be species-specific among phagotrophic protists. We conclude that two scenarios may explain our results: (1) protistan species capable of consuming the brown tide alga were present at low abundances during bloom initiation and thus not able to respond rapidly to increases in the intrinsic growth rate of the alga, or (2) the brown tide alga produced substance(s) that inhibited or retarded protistan grazing activities during the period of bloom initiation. The latter scenario seems less likely given that significant mortality of A. anophagefferens was measured during our field study and mesocosm experiment. However, even a minor reduction in mortality rate due to feeding selectivity among herbivores might result in a mismatch between growth and grazing of A. anophagefferens that could give rise to significant net population growth of this HAB species. Either scenario infers an important role for trophic interactions within the plankton as a factor explaining the development of brown tides in natural ecosystems.     

Stimulation of the brown tide organism, Aureococcus anophagefferens, by selective nutrient additions to in situ mesocosms

The influence of nutrient additions and sediment exchange on Aureococcus anophagefferens growth was studied using 200 l mesocosms deployed in situ at the Southampton College Marine Science Center in Long Island, New York. A. anophagefferens cell density increased in mesocosms with separate additions of the following materials: urea + glucose and desiccation-stressed Enteromorpha tissue. A decrease in A. anophagefferens cell density was observed in mesocosms with either no additions (control) or with added nitrate. A treatment containing a sediment layer exhibited an increase in average cell densities, but the increase was not statistically significant (P = 0.15). In the 9 day experiment, net growth of A. anophagefferens was only observed during the last 3 days, which corresponded to a period of high solar irradiation. Total chlorophyll concentration declined in all treatments during the first 6 days, which corresponded to relatively low daily irradiance, suggesting low-light stress on the phytoplankton assemblage during the initial phase of the experiment. During the ensuing sunny period, a 4–5-fold increase in chlorophyll concentration was observed in the nitrate and urea treatments with lesser increases in the other treatments. A. anophagefferens density increased relative to total phytoplankton biomass (Chl basis) in the urea + glucose and Enteromorpha treatments. Results are consistent with a prevailing hypothesis that organic nitrogen nutrients favor the growth of A. anophagefferens. Specifically, our evidence indicates that A. anophagefferens exhibited net population growth under organic N, but not inorganic N nutrient (specifically NO₃⁻) loading.     

Temporal variations in phytoplankton, particulates, and colored dissolved organic material based on optical properties during a Long Island brown tide compared to an adjacent embayment

Since 1985, the coastal embayments of Long Island, New York, have been plagued with recurrent blooms, aptly called brown tides, of the pelagophyte Aureococcus anophagefferens. The distinct ocean color observed during these blooms suggests that optical methods can be used as a tool to study, detect, and track brown tides. Thus, the goal of our project was to compare the optical properties and pigment composition during bloom and non-bloom conditions and assess temporal variations in the phytoplankton and other constituents in the seawater associated with bloom development. From 17 May to 8 June 2000, we measured a time series of particle size distributions and concentrations as well as size-fractioned algal pigments and optical properties in two Long Island embayments where brown tides are known to occur. During our study, A. anophagefferens represented an insignificant contribution to the algal community in West Neck Bay (WNB), whereas a bloom developed in Quantuck Bay (QB). Initially, temperature and salinity were similar at the two locations; however, bulk optical properties, chlorophyll, and particle concentrations were nearly a factor of 2 greater at QB. Bulk optical properties remained constant at WNB, yet increased exponentially at QB as the bloom developed. The composition of particulates, including phytoplankton, varied little at QB, and the optical properties suggested the dominance of A. anophagefferens (confirmed by microscopy). The largest temporal variations were observed in the colored dissolved organic material (CDOM); the colloidal (0.2–0.7 μm) fraction, exhibiting a strong protein-like signal, increased dramatically at the height of the bloom. At WNB particle sizes and algal composition varied despite the invariant bulk optical properties; CDOM variations were minimal. Overall, the optical properties in the two bays demonstrated that at QB temporal variations were dominated by biomass and colloidal protein changes, whereas shifts in the algal community occurred at WNB. This study demonstrates the utility of in situ optical observations to resolve temporal changes in the ecological conditions associated with algal bloom development.     

A comparison of N and C uptake during brown tide (Aureococcus anophagefferens) blooms from two coastal bays on the east coast of the USA

Blooms of the brown tide pelagophyte, Aureococcus anophagefferens, have been reported in coastal bays along the east coast of the USA for nearly two decades. Blooms appear to be constrained to shallow bays that have low flushing rates, little riverine input and high salinities (e.g., >28). Nutrient enrichment and coastal eutrophication has been most frequently implicated as the cause of A. anophagefferens and other blooms in coastal bays. We compare N and C dynamics during two brown tide blooms, one in Quantuck Bay, on Long Island, NY in 2000, and the other in Chincoteague Bay, at Public Landing, MD in 2002, with a physically similar site in Chincoteague Bay that did not experience a bloom. We found that the primary forms of nitrogen (N) taken up during the bloom in Quantuck Bay were ammonium and dissolved free amino acids (DFAA) while the primary form of N fueling production at both sites in Chincoteague Bay was urea. At both Chincoteague sites, amino acid carbon (C) was taken up while urea C was not. Even though A. anophagefferens has the ability to take up organic C, during the bloom at Chincoteague Bay, photosynthetic uptake of bicarbonate was the dominant pathway of C acquisition by the >1.2 μm size fraction during the day. C uptake by cells <5.0 μm was insufficient to meet cellular C demand based on the measured N uptake rates and the C:N ratio of particulate material. While cells >1.2 μm did not take up much organic C during the day, smaller cells (>0.2 μm) did. Peptide hydrolysis appeared to play an important role in mobilizing organic matter in Quantuck Bay, where amino acids contributed substantially to N and C uptake, but not in Chincoteague Bay. Dissolved organic N (DON), dissolved organic C (DOC) concentrations and the DOC/DON ratio were higher and total dissolved inorganic N (DIN) concentrations were lower at the bloom site in Chincoteague Bay than at the nonbloom site in the same bay. We conclude that A. anophagefferens is capable of using a wide variety of N and C compounds, and that nutrient inputs, biotic interactions and the dominant recycling pathways determine which compounds are available and which metabolic pathways are active at a particular site.     

Interannual variability of Aureococcus anophagefferens in Quantuck Bay, Long Island: natural test of the DON hypothesis

This study examined benthic and pelagic rate processes from the perspective of benthic dissolved organic matter (DOM) and its possible role in Aureococcus anophagefferens population dynamics. Sampling was conducted in Quantuck Bay, Long Island, New York, at three times in the summer of 2000 and two times in the summer of 2001. A. anophagefferens exhibited a large bloom between the May and July 2000 sample periods, but a smaller bloom was captured in the September 2000 sampling. Densities throughout 2001 were significantly lower than during 2000. There were few differences in most parameters measured between years, but the largest difference was the seasonal increase in both particulate (POM) and dissolved organic matter (DOM) during 2000 that was not observed during 2001. In particular, DOP accumulated the most, followed by DON and DOC, which resulted in significant seasonal decreases in the C:N:P ratios of the DOM pools. On the contrary, changes in elemental ratios of POM were not observed. The seasonal accumulation of DON appeared to be driven largely (50%) by the flux of DON from the benthos in 2000, but during 2001, all measured DON fluxes were into the sediment from the water column. This is consistent with the lack of accumulation during this year. There was little evidence for changes in microzooplankton grazing pressure between 2000 and 2001, and therefore the accumulation of DON and DOP during 2000 could have provided a competitive advantage to A. anophagefferens over other picoalgal species (e.g., Synechococcus) resulting in the significant blooms observed in 2000.     

Recognizing biotic breakage of the hard clam, Mercenaria mercenaria caused by the stone crab, Menippe mercenaria: An experimental taphonomic approach

The ability to assign lethal traces left on prey to particular durophagous predators enhances our understanding of predation pressure in the fossil record. To determine whether stone crabs (Menippe mercenaria Say 1818) leave diagnostic traces in the act of feeding on hard clams (Mercenaria mercenaria Linnaeus 1758), live clams were offered to crabs in laboratory aquaria over several months and the fragments produced during predation were examined for diagnostic breakage patterns. These fragments were then compared both macroscopically and using scanning electron microscopy to the fracture patterns produced by tumbling clams in a rock tumbler which simulated breakage during transport in the surf zone, and crushing clams using an Instron which simulated breakage resulting from sediment compaction. Fossil specimens of Mercenaria mercenaria were also examined to determine whether the criteria for recognizing predation traces generated experimentally could be recognized. While not all acts of predation produce diagnostic traces, when larger fragments (greater than 50% shell remaining) are produced during feeding, predatory-diagnostic breakage ranges from 70 to 80%. Macroscopic breakage patterns generated during the predation experiments were also present in fossil specimens. Damage caused by abiotic mechanisms (tumbling and crushing) is highly unlikely to be confused with damage produced by this predator.     

The influence of plankton composition and water quality on hard clam (Mercenaria mercenaria L.) populations across Long Island's south shore lagoon estuaries (New York, USA)

We conducted a two-year study to assess how plankton composition and water quality impacts the distribution, densities, condition, growth, biochemical composition and reproductive success of juvenile and adult Mercenaria mercenaria (L.) in Long Island's south shore estuaries (LISSE). Juvenile and adult hard clams were placed in suspended cages at 10 locations ranging from the ocean inlets to locations furthest from inlets in Shinnecock Bay (SB), the eastern-most barrier island estuary of LISSE, and Great South Bay (GSB), the western-most barrier island estuary of LISSE. Phytoplankton community composition, temperature, salinity, dissolved oxygen, and clam growth and condition were monitored bi-weekly. A benthic survey of M. mercenaria densities in both estuaries was also conducted. In both 2004 and 2005, juveniles in central bay locations had significantly faster growth rates, lower mortality rates, and higher lipid content relative to sites closest to the inlets. Adult hard clams closest to the Fire Island inlet also had significantly lower condition indexes compared to mid-bay stations and densities of wild M. mercenaria populations in both estuaries were lower near inlets compared to locations further from inlets. In addition to substantial spatial differences within each estuary, differences were also observed between the embayments as juvenile clams in SB grew approximately twice as fast as those in GSB and adults in SB had significantly greater condition indexes than clams in GSB. Instantaneous juvenile growth rates were highly correlated to temperatures below 24 °C (p < 0.0001) and were also significantly correlated with several indicators of suspended food quantity and food quality (centric diatoms, phytoplankton cells > 5 μm, and dinoflagellates (inverse correlation)) which co-varied independently of temperature. In sum, these results suggest tidal exchange in LISSE promotes a water quality regime (cold water, with low food concentration) which would reduce the growth of juvenile clams and the overall reproductive success of adult hard clams located near newly-formed ocean inlets. However, increased exchange for regions furthest from inlets could enhance juvenile clam growth rates by reducing summer peak temperatures (> 24 °C) and densities of poor food sources (dinoflagellates).     

Physiological responses of Aureoumbra lagunensis and Synechococcus sp. to nitrogen addition in a mesocosm experiment

Aureoumbra lagunensis is the causative organism of the Texas brown tide and is notable because it dominated the Laguna Madre ecosystem from 1990 to 1997. This species is unusual because it has the highest known critical nitrogen to phosphorus ratio (N:P) for any microalgae ranging from 115 to 260, far higher than the 16N:1P Redfield ratio. Because of its high N:P ratio, Aureoumbra should be expected to respond to N additions that would not stimulate the growth of competitors having the Redfield ratio. To evaluate this prediction, a mesocosm experiment was performed in the Laguna Madre, a South Texas coastal lagoon, in which a mixed Aureoumbra–Synechococcus (a cyanobacterium) community was enclosed in 12 mesocosms and subjected to nitrogen addition (6 controls, 6 added ammonium) for 16 days. After day 4, added nitrogen did not significantly increase Aureoumbra specific growth rate but the alga retained dominance throughout the experiment (64–75% of total cell biovolume). In control mesocosms, Aureoumbra became less abundant during the first 4 days of the experiment but rebounded by the end of the experiment and was dominant over Synechococcus. Despite the lack of a strong positive growth response, Aureoumbra did respond physiologically to N addition. By the end of the experiment, the average N:P ratio of the Aureoumbra-dominated community was 86 in the N+ treatment and 41 in the control, indicating that the alga became less N-limited in the N+ treatment. The average C:N ratio was 6.6 in the N+ treatment (8.6 in the control) and suggests that the alga was not N-limited, however, C:N ratio may not be a good indicator of nitrogen limitation since this alga can produce significant quantities of carbon-containing extracellular polysaccharides, depending on growth conditions. Both Aureoumbra cellular chlorophyll fluorescence and cell size increased in response to added N, indicating a reduction in N limitation. It appeared that the N additions were not large and/or frequent enough to stimulate Aureoumbra growth. The main competitor, the unicellular cyanobacterium Synechococcus, responded positively to the nitrogen addition by increased specific growth rate. Unlike Aureoumbra, no significant effect on Synechococcus cellular pigment fluorescence or cell size was noted. Literature data suggest that Synechococcus, like Aureoumbra, may have a critical N:P ratio much higher than 16:1, which could explain its response.     

Bottom-up controls on a mixed-species HAB assemblage: A comparison of sympatric Chattonella subsalsa and Heterosigma akashiwo (Raphidophyceae) isolates from the Delaware Inland Bays, USA

Recent novel mixed blooms of several species of toxic raphidophytes have caused fish kills and raised health concerns in the highly eutrophic Inland Bays of Delaware, USA. The factors that control their growth and dominance are not clear, including how these multi-species HAB events can persist without competitive exclusion occurring. We compared and contrasted the relative environmental niches of sympatric Chattonella subsalsa and Heterosigma akashiwo isolates from the bays using classic Monod-type experiments. C. subsalsa grew over a temperature range from 10 to 30 °C and a salinity range of 5–30 psu, with optimal growth occurring from 20 to 30 °C and 15 to 25 psu. H. akashiwo had similar upper temperature and salinity tolerances but also lower limits, with growth occurring from 4 to 30 °C and 5 to 30 psu and optimal growth between 16 and 30 °C and 10 and 30 psu. These culture results were confirmed by field observations of bloom occurrences in the Inland Bays. Maximum nutrient-saturated growth rates (μ_max) for C. subsalsa were 0.6 d⁻¹ and half-saturation concentrations for growth (K_s) were 9 μM for nitrate, 1.5 μM for ammonium, and 0.8 μM for phosphate. μ_max of H. akashiwo (0.7 d⁻¹) was slightly higher than C. subsalsa, but K_s values were nearly an order of magnitude lower at 0.3 μM for nitrate, 0.3 μM for ammonium, and 0.2 μM for phosphate. H. akashiwo is able to grow on urea but C. subsalsa cannot, while both can use glutamic acid. Cell yield experiments at environmentally relevant levels suggested an apparent preference by C. subsalsa for ammonium as a nitrogen source, while H. akashiwo produced more biomass on nitrate. Light intensity affected both species similarly, with the same growth responses for each over a range from 100 to 600 μmol photons m⁻² s⁻¹. Factors not examined here may allow C. subsalsa to persist during multi-species blooms in the bays, despite being competitively inferior to H. akashiwo under most conditions of nutrient availability, temperature, and salinity.     

The effects of a harmful alga on bivalve larval lipid stores

Marine invertebrates often have complex life histories that include a swimming planktivorous larval stage, at which time they are vulnerable to a variety of stressors, including those associated with nutritional stress and harmful algal blooms. Lipid stores have been shown to be especially important for post-metamorphic survivorship and growth in a variety of marine invertebrates. We investigated the effects of the harmful brown tide alga Aureococcus anophagefferens on the lipid stores and growth of larvae of the hard clam (northern quahog, Mercenaria mercenaria), a dominant bivalve in many western Atlantic bays and estuaries. M. mercenaria was the dominant bivalve in Great South Bay, Long Island, until the mid-1970s, but very few larvae are presently found in these waters. Recent brown tide blooms have been hypothesized to pose a barrier to recovery of M. mercenaria populations and hinder recent restoration efforts by negatively affecting clam larvae. To test whether a diet of the brown tide alga affects the accumulation of beneficial lipid stores, we fed larvae one of three diets representing equal biovolumes of Isochrysis galbana, a nutritious control alga; A. anophagefferens, the brown tide alga for which nutritional quality is not presently known; or a mixture of the two. Larvae fed only brown tide had significantly less lipid stores than those in the other dietary treatments. In addition, brown tide negatively affected larval size. We also tested for evidence of tradeoffs between larval growth and lipid stores, predicting that when the diet was less nutritious as in the brown tide treatments, larval size and lipids would be negatively correlated. In contrast, we found that larvae fed a mixed algal diet or only A. anophagefferens showed a significant positive correlation between lipid stores and size, suggesting that some larvae were simply better at obtaining food and associated nutrients. Larval success likely depends on a complex interplay between genetic and environmental factors. Our study suggests that poor nutrition associated with a harmful alga can have negative effects on larval size and lipids stores, which in turn are mediated by the inter-individual variability in the ability to grow and accumulate necessary lipid stores. Phytoplankton quality is likely to be important for the sustainability of bivalve populations even when it primarily impacts the larval phase; and a diet of brown tide algae may have lasting legacies for juveniles and adults.     

Mediation of benthic–pelagic coupling by microphytobenthos: an energy- and material-based model for initiation of blooms of Aureococcus anophagefferens

We present a conceptual model for initiation of blooms of the estuarine brown-tide pelagophyte Aureococcus anophagefferens. The model is based on the observation that in addition to its well-documented stimulation by organic nutrients, Aureococcus is pre-adapted to low light levels. Its relatively low maximum (light-saturated) growth rate makes it a poor competitor with other estuarine species at high light under acclimated conditions. Its large photosynthetic antenna and relatively low quota of photoprotective pigments make it more susceptible to photoinhibition than other species to which it is compared. These same characteristics give it a competitive advantage at low light levels. In its shallow habitat, both the light level and the rate of nutrient supply from groundwater and benthic porewater are determined by the degree of benthic coupling. Experimental manipulations in a microcosm and a survey of the literature demonstrate the ability of the sediment-associated microphytobenthos (MPB) to regulate both the light- and nutrient-environment in the overlying water column. The model predicts that the growth dynamics of the MPB are such that the benthic/water column interactions tend towards one of two stable states. In one, a well-developed population of MPB restricts resuspension of particulate material and efflux of dissolved nutrients, resulting in clear and nutrient-poor overlying waters. This condition does not favor growth of Aureococcus. In the alternative state, erosion of the MPB results in turbid, nutrient-rich waters that do favor bloom initiation. Alternation between the states is caused by external physical forcing, through wind-driven mixing of the water column. Field data from Quantuck Bay, New York (USA), failed to document the transition from non-bloom to bloom conditions. Even so, they are consistent with the model’s predictions.     

Flocculation and removal of the brown tide organism, Aureococcus anophagefferens (Chrysophyceae), using clays

Previous attempts to remove the brown tideorganism, Aureococcusanophagefferens, through flocculation withclays have been unsuccessful, in spite ofadopting concentrations and dispersalprotocols that yielded excellent cellremoval efficiency (RE >90%) with otherspecies, so a study was planned to improvecell removal. Four modifications in claypreparation and dispersal were explored: 1)varying the salinity of the claysuspension; 2) mixing of the clay-cellsuspension after clay addition; 3) varyingof concentration of the initial clay stock;4) pulsed loading of the clay slurry. Theeffect of salinity was dependent on theclay mineral type: phosphatic clay (IMC-P2)had a higher RE than kaolinite (H-DP) whenseawater was used to disperse the clay, butH-DP removed cells more efficiently whensuspended in distilled water prior toapplication. Mixing after dispersalapproximately doubled RE for both clayscompared to when the slurry was layeredover the culture surface. Lowering theconcentration of clay stock and pulsing theclay loading increased RE, regardless ofmineral type. However, this increase wasmore apparent for clays dispersed inseawater than in distilled water. Ingeneral, application procedures thatdecrease the rate of self-aggregation amongthe clay particles and increase thecollision frequency between clay particlesand A. anophagefferens achieve highercell removal efficiency. These empiricalstudies demonstrated that clays might be animportant control option for the brown tideorganism, given the proper attention topreparation, dispersal methods,environmental impacts, and the hydrodynamicproperties of the system being treated. Implications for the treatment of browntides in the field are discussed.     

Distribution of Pfiesteria piscicida cyst populations in sediments of the Delaware Inland Bays, USA

The toxic dinoflagellate, Pfiesteria piscicida, is a common constituent of the phytoplankton community in the Delaware Inland Bays, USA. In this study, molecular methods were used to investigate the distributions of benthic stages (cysts) of P. piscicida in sediment cores from the Delaware Inland Bays. Cores from 35 sites were partitioned into nephloid and anoxic layers and analyzed for P. piscicida by nested amplification of the 18S rDNA gene using P. piscicida-specific primers. The presence of inhibitory substances in the PCR reaction was evaluated by inclusion of an exogenous control DNA in the extraction buffer, thus eliminating samples that may yield false-negative results. Our results indicate a patchy distribution of P. piscicida in sediments of the Delaware Inland Bays, with distinct differences between each of the three bays. Overall, P. piscicida was found more frequently in sediments from Rehoboth Bay compared to Indian River and Little Assawoman Bays. These differences suggest (i) that populations of P. piscicida may be more widely distributed in Rehoboth Bay, (ii) that populations of P. piscicida may have been introduced to Rehoboth Bay at an earlier time, (iii) that past blooms of P. piscicida in Rehoboth Bay estuaries may have seeded the sediments with higher numbers of cysts, and/or (iv) that Rehoboth Bay sediments may be more resistant to clearing due to storm turbulence.     

Red tide blooms of Cochlodinium polykrikoides in a coastal cove

Successive blooms of the dinoflagellate Cochlodinium polykrikoides occurred in Pettaquamscutt Cove, RI, persisting from September through December 1980 and again from April through October 1981. Cell densities varied from <100 cells L⁻¹ at the onset of the bloom and reached a maximum density exceeding 3.4 × 10⁶ cells L⁻¹ during the summer of 1981. The bloom was mainly restricted to the mid to inner region of this shallow cove with greatest concentrations localized in surface waters of the southwestern region during summer/fall periods of both years. Highly motile cells consisting of single, double and multiple cell zooids were found as chains of 4 and 8 cells restricted to the late August/September periods. The highest cell densities occurred during periods when annual temperatures were between 19 and 28 °C and salinities between 25 and 30. A major nutrient source for the cove was Crying Brook, located at the innermost region at the head of the cove. Inorganic nitrogen (NH₃ and NO₂ + NO₃) from the brook was continually detectable throughout the study with maximum values of 57.5 and 82.5 μmol L⁻¹, respectively. Phosphate (PO₄-P) was always present in the source waters and rarely <0.5 μmol L⁻¹; silicate always exceeded 30 μmol L⁻¹ with maximum concentrations reaching 226 μmol L⁻¹. Chlorophyll a and ATP concentrations during the blooms varied directly with cell densities. Maximum Chl a levels were 218 mg m⁻³ and ATP-carbon was >20 g C m⁻³. Primary production by the dinoflagellate-dominated community during the bloom varied between 4.3 and 0.07 g C m⁻³ d⁻¹. Percent carbon turnover calculated from primary production values and ATP-carbon varied from 6 to 129% d⁻¹. The dinoflagellates dominated the entire summer period; other flagellates and diatoms were present in lesser amounts. A combination of low washout rate due to the cove dynamics, active growth, and life cycles involving cysts allowed C. polykrikoides to maintain recurrent bloom populations in this area.     

Control of the harmful alga Cochlodinium polykrikoides by the naked ciliate Strombidinopsis jeokjo in mesocosm enclosures

Red tides dominated by the harmful dinoflagellate Cochlodinium polykrikoides have caused annual losses of USD $5–60 million to the Korean aquaculture industry annually since 1995 and a loss of USD $3 million during a 1999 net-pen fish mortality event in Canada. In order to evaluate the potential to control C. polykrikoides red tides dominated by using mass-cultured heterotrophic protistan grazers, we monitored the abundance of Strombidinopsis jeokjo (a naked ciliate) and C. polykrikoides after mass-cultured S. jeokjo was introduced into mesocosms (ca. 60 l) deployed in situ and containing natural red tide waters dominated by C. polykrikoides. Water temperature, salinity, and pH, as well as the abundance of co-occurring other protists and metazooplankton were measured concurrently. To compare the growth and ingestion rates of S. jeokjo feeding on cultured versus natural populations of C. polykrikoides, we also monitored the abundance of cultured C. polykrikoides and S. jeokjo in bottles during laboratory grazing experiments. S. jeokjo introduced into the mesocosms grew well, effectively reducing natural populations of C. polykrikoides from approximately 1000 cells ml⁻¹ to below 10 cells ml⁻¹ within 2 days. The growth and ingestion rates of cultured S. jeokjo on natural populations of C. polykrikoides in the mesocosms for the first 30 h (0.72 day⁻¹ and 51 ng C grazer⁻¹ day⁻¹) were 84% and 44%, respectively, of those measured in the laboratory during bottle incubations with similar initial prey concentrations. The calculated grazing impact of S. jeokjo on natural populations of C. polykrikoides suggests that large-scale cultures of this ciliate could be used for controlling red tides by C. polykrikoides in small areas.