Mark S. Dixon

Combined effects of a parasite, QPX, and the harmful-alga, Prorocentrum minimum on northern quahogs, Mercenaria mercenaria

Northern quahogs, Mercenaria mercenaria (L.), frequently are infected with the parasite Quahog Parasite Unknown (QPX, Labyrintohomorpha, Thraustochytriales), which can cause morbidity and mortality of the quahogs. Possible interactions between this parasitic disease and exposure to the harmful dinoflagellate Prorocentrum minimum in M. mercenaria were studied experimentally. Quahogs from Massachusetts with variable intensity of QPX infection were exposed, under controlled laboratory conditions, to cultured P. minimum added to the natural plankton at a cell density equivalent to a natural bloom. After 5 days of exposure, individual clams were diagnosed histologically to assess prevalence and intensity of parasitic infection, as well as other pathological conditions. Further, cellular defense status of clams was evaluated by analyzing hemocyte parameters (morphological and functional) using flow-cytometry. Exposure of quahogs to P. minimum resulted in: a lower percentage of phagocytic hemocytes, higher production of reactive oxygen species (ROS), larger hemocyte size, more-numerous hemocytic aggregates, and increased numbers of hemocytes in gills accompanied by vacuolation and hyperplasia of the water-tubular epithelial cells of the gills. Quahogs had a low prevalence of QPX; by chance, the parasite was present only in quahogs exposed to P. minimum. Thus, the effect of QPX alone on the hemocyte parameters of quahogs could not be assessed in this experiment, but it was possible to assess different responses of infected versus non-infected quahogs to P. minimum. QPX-infected quahogs exposed to P. minimum had repressed percentage of phagocytic hemocytes, consistent with immuno-modulating effect of P. minimum upon several molluscan species, as well as smaller hemocytes and increased hemocyte infiltration throughout the soft tissues. This experiment demonstrates the importance of considering interactive effects of different factors on the immunology and histopathology of bivalve shellfish, and highlights the importance of considering the presence of parasites when bivalves are subjected to harmful-algal blooms.

Physiological and pathological changes in the eastern oyster Crassostrea virginica infested with the trematode Bucephalus sp. and exposed to the toxic dinoflagellate Alexandrium fundyense.

Effects of experimental exposure to Alexandrium fundyense, a Paralytic Shellfish Toxin (PST) producer known to affect bivalve physiological condition, upon eastern oysters, Crassostrea virginica with a variable natural infestation of the digenetic trematode Bucephalus sp. were determined. After a three-week exposure to cultured A. fundyense or to a control algal treatment with a non-toxic dinoflagellate, adult oysters were assessed for a suite of variables: histopathological condition, hematological variables (total and differential hemocyte counts, morphology), hemocyte functions (Reactive Oxygen Species (ROS) production and mitochondrial membrane potential), and expression in gills of genes involved in immune responses and cellular protection (MnSOD, CAT, GPX, MT-IV, galectin CvGal) or suspected to be (Dominin, Segon). By comparing individual oysters infested heavily with Bucephalus sp. and uninfested individuals, we found altered gonad and digestive gland tissue and an inflammatory response (increased hemocyte concentration in circulating hemolymph and hemocyte infiltrations in tissues) associated with trematode infestation. Exposure to A. fundyense led to a higher weighted prevalence of infection by the protozoan parasite Perkinsus marinus, responsible for Dermo disease. Additionally, exposure to A. fundyense in trematode-infested oysters was associated with the highest prevalence of P. marinus infection. These observations suggest that the development of P. marinus infection was advanced by A. fundyense exposure, and that, in trematode-infested oysters, P. marinus risk of infection was higher when exposed to A. fundyense. These effects were associated with suppression of the inflammatory response to trematode infestation by A. fundyense exposure. Additionally, the combination of trematode infestation and A. fundyense exposure caused degeneration of adductor muscle fibers, suggesting alteration of valve movements and catch state, which could increase susceptibility to predation. Altogether, these results suggest that exposure of trematode-infested oysters to A. fundyense can lead to overall physiological weakness that decrease oyster defense mechanisms.

Temporal Variability in Phytoplankton Removal by a Commercial, Suspended Eastern Oyster Nursery and Effects on Local Plankton Dynamics

ABSTRACT n Quantitative measurements of phytoplankton removal in a natural setting are needed to evaluate interactions between aquacultured bivalve populations and the surrounding environment. We report high-frequency (15-min) measurements of environmental variables relevant to oyster feeding and excretion at the inflow and outflow of an oyster nursery—floating upweller system (FLUPSY)—from June through September 2010 in the East Creek embayment, Peconic Estuary, NY. We demonstrated large variability in oyster particle clearance rate on short- (minutes to hours) to long-term (seasonal) timescales, including oyster responses to environmental variation, such as diurnal temperature and dissolved oxygen cycles, wind-driven turbulence, and the presence of harmful algae. A diel cycle in clearance rates calculated from whole FLUPSY measurements was apparent, with a maximum weight-specific clearance rate (CRW) of 2.21 L/h/g occurring around midnight, and a minimum CRW of 0.32 L/h/g at 0740 HR, coincident with the lowest concentration of dissolved oxygen in the water. Throughout the season, oyster growth and feeding showed constant, high values from June 12 to July 21, with a median CRW of 0.95 L/h/g. From late July to September, a toxic dinoflagellate, Cochlodinium polykrikoides, was present frequently in the water, and was coincident with depressed oyster feeding, slow/no growth, and increased mortality. Overall, the FLUPSY in East Creek did not have a large impact on the abundance of phytoplankton in the water. Future modeling efforts projecting carrying capacity and ecosystem services of shellfish aquaculture and restoration need to take into account the potential for temporal variability in feeding resulting from environmental variation, as observed in this study.

The Eastern Mudsnail, Ilyanassa obsoleta, Actively Forages For, Consumes, And Digests Cysts Of The Dinoflagellate, Scrippsiella lachrymosa

The Eastern mudsnail, Ilyanassa obsoleta, was attracted to, consumed, and digested resting cysts of the dinoflagellate Scrippsiella lachrymosa when cysts were presented in grazing experiments. Twenty snails were observed individually for one hour in petri dishes divided into four parts wherein cysts were present in one quadrant, sediment particles of the same size range were in another quadrant, and two quadrants were free of particles. Actively foraging snails were nearly twice as likely to be found in quadrants containing S. lachrymosa cysts as in the other quadrants until cysts were consumed. Microscope observations of fecal pellets from snails feeding on cysts revealed digestive destruction of the cysts. These findings indicate that deposit-feeding grazers can actively seek dinoflagellate cysts as a food item, thereby influencing distribution of cysts and subsequent germination of dinoflagellate vegetative cells.

IMPACTS OF A CYANOBACTERIUM CONTAMINATING LARGE-SCALE AQUACULTURE FEED CULTURES OF TETRASELMIS CHUI ON SURVIVAL AND GROWTH OF BAY SCALLOPS, ARGOPECTEN IRRADIANS IRRADIANS

Abstract Large-scale, open, microalgal feed cultures for hatchery and nursery production of marine invertebrates inevitably becomes contaminated with various microbes that can affect productivity and usability of the harvested biomass. In the Greenhouse for Research on Algal Mass Production Systems (GRAMPS) at the NMFS Laboratory in Milford, CT, cultures of Tetraselmis chui (PLY429) often become contaminated with a cyanobacterium; preliminary observations suggested that juvenile bay scallops, Argopecten irradians irradians showed reduced performance when the feed culture became contaminated with this cyanobacterium. We isolated a cyanobacterium from a contaminated culture of PLY429 and conducted a feeding study to determine if this isolate affects survival and growth of juvenile bay scallops, either alone or in combination with PLY429, thereby simulating feeding of a contaminated culture. Bay scallops were given a diet of either 100% PLY429, 50% PLY429 with 50% cyanobacteria, 100% cyanobacteria, or starved. There was 100% mortality of bay scallops by week 3 when they were starved, with a significant difference in survival between diets (P < 0.01). At 6 wk the scallops fed only the cyanobacterium had 63% survival, 93% survived in the mixed diet, and 98% survived when fed 100% PLY429. The net growth of bay scallops on the different diets was also significantly different (P < 0.01) with scallops fed 100% PLY429 having the highest shell-growth rate of 198-μm scallop−1 d−1, and growth rates of 82-μm scallop−1 d−1 on the mixed diet, and 65-μm scallop−1 d−1 for the cyanobacterial diet. These findings suggest that the cyanobacterium will not cause instant mortality, but it will not support sustained survival and growth over time scales of weeks.

Short communication: adaptability of the feeding behavior of intertidal ribbed mussels (Geukensia demissa) to constant submersion

The ribbed mussel (Geukensia demissa, Dillwyn 1817) is a dominant benthic filter-feeder in salt marshes along the North American Atlantic Coast. It has been proposed that the cultivation and harvest of ribbed mussels could be used to bioremediate the eutrophication of coastal waters. To accomplish this, mussels would be grown in suspension culture underwater, which is different than this species’ natural, intertidal habitat in which they are exposed to a tidal regime of submersion and emersion. To assess possible effects of constant submersion upon the feeding behavior of G. demissa, we quantified filter-feeding activities of ribbed mussels collected from either an intertidal location or a permanently submerged (2xa0months) population in the same embayment. Filtration measurements to determine clearance rates were conducted in aquaria containing ultra-filtered seawater with cultured phytoplankton. Results show that mussels taken from the intertidal population had significantly higher filtration than the submerged population initially, but after 3xa0days of submersion in the aquaria, this difference disappeared. Moreover, all experimental G. demissa had higher clearance rates during natural low tide than during natural high tide. These results indicate a potential for ribbed mussels to be grown in suspension culture for nutrient bioextraction purposes.

Transplant experiment to evaluate the feeding behaviour of the Atlantic ribbed mussel, Geukensia demissa, moved to a high inorganic seston area

In 2011–12, a field study demonstrated that ribbed mussels from two locations in the north-east Atlantic Coast of the USA used different feeding strategies to adapt to widely differing seston characteristics and achieve the same absorption efficiency. To investigate whether there was local, genetic adaptation of mussels in the two contrasting sites, we conducted a transplant experiment in 2012 in which mussels were moved from the high-plankton, low-inorganic waters of Milford Harbor, CT, to the high-inorganic, low-plankton waters of Hunts Point, Bronx, NY. Results showed that mussels from Milford adapted to the new, poorer-quality seston within 6 days of submersion in Hunts Point waters, which indicates that phenotypic plasticity in the species is sufficient to account for adaptability of the ribbed mussel to Hunts Point conditions. This adaptability makes the ribbed mussel a good candidate for environmental remediation technologies, such as nutrient bioextraction.

Design and Use of an Apparatus for Quantifying Bivalve Suspension Feeding at Sea

As shellfish aquaculture moves from coastal embayments and estuaries to offshore locations, the need to quantify ecosystem interactions of farmed bivalves (i.e., mussels, oysters, and clams) presents new challenges. Quantitative data on the feeding behavior of suspension-feeding mollusks is necessary to determine important ecosystem interactions of offshore shellfish farms, including their carrying capacity, the competition with the zooplankton community, the availability of trophic resources at different depths, and the deposition to the benthos. The biodeposition method is used to quantify feeding variables in suspension-feeding bivalves in a natural setting and represents a more realistic proxy than laboratory experiments. This method, however, relies upon a stable platform to satisfy the requirements that water flow rates supplied to the shellfish remain constant and the bivalves are undisturbed. A flow-through device and process for using the biodeposition method to quantify the feeding of bivalve mollusks were modified from a land-based format for shipboard use by building a two-dimensional gimbal table around the device. Planimeter data reveal a minimal pitch and yaw of the chambers containing the test shellfish despite boat motion, the flow rates within the chambers remain constant, and operators are able to collect the biodeposits (feces and pseudofeces) with sufficient consistency to obtain accurate measurements of the bivalve clearance, filtration, selection, ingestion, rejection, and absorption at offshore shellfish aquaculture sites.

The East River tidal strait, New York City, New York, a high-nutrient, low-chlorophyll coastal system

The East River tidal strait, located between New York Harbor and Western Long Island Sound, is characterized by high suspended silt concentrations with low organic content kept in suspension by intense tidal currents. Inorganic nutrients, including nitrate, nitrite, ammonia, and phosphate, were high even during the summer. Dissolved inorganic nitrogen (DIN) concentrations generally were above 20xa0µM and did not likely limit phytoplankton growth. Despite high nutrient concentrations, median chlorophyll a concentration was only 1.53xa0µgxa0l−1, making the East River tidal strait a high-nutrient, low-chlorophyll (HNLC) area, likely a result of suspended silt blocking light penetration into the surface water. There were times at which the ratio of mixed layer to depth of the euphotic zone was generally greater than what has been suggested for phytoplankton to produce net primary production. The high-nutrient East River tidal strait is likely one of the sources of nutrients fueling summer phytoplankton production and consequent hypoxia in the Western Long Island Sound as silt settles from surface water in the lower turbulence conditions of the western narrows of Long Island Sound, thereby allowing light penetration and subsequent consumption of dissolved nutrients by phytoplankton.

Characterizing seston in the Penobscot River Estuary

The Penobscot River Estuary is an important system for diadromous fish in the Northeast United States of American (USA), in part because it is home to the largest remnant population of Atlantic salmon, Salmo salar, in the country. Little is known about the chemical and biological characteristics of seston in the Penobscot River Estuary. This study used estuarine transects to characterize the seston during the spring when river discharge is high and diadromous fish migration peaks in the Penobscot River Estuary. To characterize the seston, samples were taken in spring 2015 for phytoplankton identification, total suspended matter (TSM), percent organic TSM, chlorophyll a, particle size (2xa0μm-180xa0μm), particulate carbon and nitrogen concentrations, and stable carbon and nitrogen isotopes. The estuarine profiles indicate that TSM behaved non-conservatively with a net gain in the estuary. As phytoplankton constituted only 1/1000 of the particles, the non-conservative behavior of TSM observed in the estuary was most likely not attributable to phytoplankton. Particulate carbon and nitrogen ratios and stable isotope signals indicate a strong terrestrial, allochthonous signal. The seston in the Penobscot River Estuary was dominated by non-detrital particles. During a short, two-week time period, Heterosigma akashiwo, a phytoplankton species toxic to finfish, also was detected in the estuary. A limited number of fish samples, taken after the 2015 Penobscot River Estuary bloom of H.xa0akashiwo, indicated frequent pathological gill damage. The composition of seston, along with ichthyotoxic algae, suggest the need for further research into possible effects upon resident and migratory fish in the Penobscot River Estuary.