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Effects of two bloom-forming dinoflagellates, Prorocentrum minimum and Gyrodinium uncatenum, on the growth and survival of the eastern oyster, Crassostrea virginica (Gmelin 1791)

Authors:
  • Virginia Institute of Marine Science, College of William and Mary
... Previous research has focused on the potential effects of these HAB species on oyster wild-stock recruitment, aquaculture, and restoration (Tango et al., 2005;Glibert et al., 2007;Place et al., 2008;Stoecker et al., 2008). Little research has focused on the impacts of these HABs within the context of oyster hatcheries (Luckenbach et al., 1993). Acute exposure to these HAB species has harmful effects on many early oyster life stages (Luckenbach et al., 1993;Wikfors and Smolowitz 1995;Glibert et al., 2007;Brownlee et al., 2008;Place et al., 2008;Stoecker et al., 2008;Lin et al., 2017). ...
... Little research has focused on the impacts of these HABs within the context of oyster hatcheries (Luckenbach et al., 1993). Acute exposure to these HAB species has harmful effects on many early oyster life stages (Luckenbach et al., 1993;Wikfors and Smolowitz 1995;Glibert et al., 2007;Brownlee et al., 2008;Place et al., 2008;Stoecker et al., 2008;Lin et al., 2017). All but one of these studies (Wikfors and Smolowitz 1995) focused on acute HAB exposure within 2 days post-fertilization, or after the oysters were at least 14 days old. ...
... Unexplained larval mortality events at regional oyster hatcheries have raised concerns over the possibility of K. veneficum and P. cordatum breakthrough into hatcheries (Luckenbach et al., 1993;Tango et al., 2005). "Breakthrough," in the context of this study, is the introduction of HAB cells and/or HAB-associated toxins into hatchery water (i.e., when water treatment processes at the hatchery fail to remove or degrade HAB cells or HAB-associated toxins from the incoming source water). ...
Article
Harmful algal bloom (HAB) dinoflagellate species Karlodinium veneficum and Prorocentrum cordatum (prev. P. minimum) are commonly found in Chesapeake Bay during the late spring and early summer months, coinciding with the spawning season of the eastern oyster (Crassostrea virginica). Unexplained larval oyster mortalities at regional commercial hatcheries prompted screening of oyster hatchery water samples for these HAB species. Both HAB species were found in treated hatchery water during the oyster spawning season, sometimes exceeding bloom cell concentrations (≥ 1,000 cells/mL). To investigate the potential for these HAB species, independently or in co-exposure, to affect larval oyster mortality and activity, 96-h laboratory single and dual HAB bioassays with seven-day-old oyster larvae were performed. Treatments for the single HAB bioassay included fed and unfed controls, K. veneficum at 1,000; 5,000; 10,000; and 50,000 cells/mL, P. cordatum at 100; 5,000; 10,000; and 50,000 cells/mL. Subsequently, the 1,000 cells/mL K. veneficum and 50,000 cells/mL P. cordatum treatments were combined in a co-exposure treatment for the dual HAB bioassay. At all cell concentrations tested, K. veneficum swarmed oyster larvae and caused significant larval oyster mortality by 96 h (Karlo1,000: 21 ± 5%; Karlo5,000: 93 ± 2%; Karlo10,000: 85 ± 3%; Karlo50,000: 83 ± 5%, SE). In contrast, there was no significant difference in larval oyster mortality between the control treatments and any of the P. cordatum treatments by 96 h. By 24 h, larval oysters were significantly less active (immotile) in the presence of either HAB species as compared to control treatments (e.g., Karlo1,000: 37.8 ± 4.1%; Proro100: 47.3 ± 7.4%; Fed: 10.8 ± 3.2%; Unfed: 10.1 ± 4.9%, SE). In the dual HAB bioassay, larval oyster mortality associated with 1,000 cells/mL K. veneficum (44 ± 9%, SE) was not changed by the addition of 50,000 cells/mL P. cordatum (55 ± 7%, SE), demonstrating that K. veneficum was primarily responsible for the observed mortality. This study demonstrated that even low cell concentrations of K. veneficum and P. cordatum are harmful to larval oysters, and could contribute to reductions in oyster hatchery production through impacts on this critical life stage.
... However, substantial effects have been shown more recently. With C. virginica it has been observed experimentally, as well as anecdotally, that in the presence of P. minimum at 10 4 cells mL − 1 spawning did not occur, and at an order of magnitude higher density, oysters reduced their filtration rates and died (Luckenbach et al., 1993). Within the Rhode River, concentrations of P. minimum fell within these ranges when it occurred. ...
... A 2-week delay in spawning from a single 2-week bloom alone may reduce the number of spawns, in turn reducing recruitment. When this estimate also considers the reduction in growth rates due to HABs, as is the case with P. minimum and its induction of histological damage impacting growth of oyster larvae and juveniles in laboratory studies (Luckenbach et al., 1993;Wikfors and Smolowitz, 1995), the total effect of HABs could be a substantial loss in oyster recruitment from a single HAB event of just a couple of weeks in duration (Glibert et al., 2007;Mann et al., 2014 The extent to which picocyanobacteria are taken up by oysters is a topic of considerable interest (reviewed by Rosa et al., 2018). Herein, cyanobacteria were largely discriminated against during feeding. ...
Article
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A 2-year study was undertaken to understand feeding preferences of the eastern oyster Crassostrea virginica in the eutrophic Rhode River, a tributary of Chesapeake Bay, Maryland, USA. A subset of experimentally suspended oysters was collected monthly and environmental parameters were simultaneously measured. Oysters were measured in height to determine growth, and the phytoplankton in their gut were examined both microscopically and using indicator pigments and compared with phytoplankton abundance and composition in the water column. Growth was higher in the second year of the study when flow was lower and salinity higher. Food selectivity was calculated using a modified electivity index (Ei), which relates phytoplankton composition in the gut to that in the water. Oysters appeared to preferentially graze–or at least preferentially retain in the gut–various (unidentified) flagellates, Ochrophyta (diatoms) and Myzozoa (dinoflagellates), and appeared to generally reject cyanobacteria, especially picocyanobacteria, from their diet. The Myzozoa included several common harmful algal bloom taxa, including Prorocentum minimum (=P. cordatum) and Heterocapsa rotundatum, that can detrimentally affect oyster growth. Reductions in eutrophication will likely be beneficial for oyster diets if such reductions result in fewer dinoflagellate blooms and in picocyanobacteria abundance during the critical feeding summer months.
... In Chesapeake Bay, USA, mass mortalities of commercial hard clams (Mercenaria mercenaria) (Wikfors and Smolowitz 1993) and oyster (C. virginica) larvae (Luckenbach et al. 1993) were observed in the presence of P. minimum blooms, indicating high density of P. minimum may have adverse effects on the filtering and feeding systems of bivalves. Moreover, the P. minimum blooms also caused 100% mortality of juvenile oysters within 14 days and at 33% bloom density caused 43% mortality over 22 days (Luckenbach et al. 1993). ...
... virginica) larvae (Luckenbach et al. 1993) were observed in the presence of P. minimum blooms, indicating high density of P. minimum may have adverse effects on the filtering and feeding systems of bivalves. Moreover, the P. minimum blooms also caused 100% mortality of juvenile oysters within 14 days and at 33% bloom density caused 43% mortality over 22 days (Luckenbach et al. 1993). The gill damage hypothesis had not been confirmed, and no follow-up studies of scallops in natural P. minimum blooms were conducted until the occurrence of mass mortality of wild eastern oyster, C. virginica, populations in Chesapeake Bay (Sellner et al. 1995). ...
Chapter
One of the fastest-growing global food sectors is the bivalve aquaculture industry. Bivalves particularly oysters, mussels and clams are important sources of animal protein (Tan and Ransangan 2016a, b). Bivalve aquaculture represents 14–16% of the average per capita animal protein for 1.5 billion people and supports over 200,000 livelihoods, mostly in developing countries (FAO 2018). Most of the bivalves produced around the world (89%) are from aquaculture (FAO 2016). To date, mollusc aquaculture have accounted for 21.42% (17.14 million tonnes) of the total aquaculture production, with Asia being the largest contributor (92.27%) (FAO 2018).
... In Chesapeake Bay, USA, mass mortalities of commercial hard clams (Mercenaria mercenaria) ( Wikfors and Smolowitz 1993) and oyster (C. virginica) larvae ( Luckenbach et al. 1993) were observed in the presence of P. minimum blooms, indicating high density of P. minimum may have adverse effects on the filtering and feeding systems of bivalves. Moreover, the P. minimum blooms also caused 100% mortality of juvenile oysters within 14 days and at 33% bloom density caused 43% mortality over 22 days ( Luckenbach et al. 1993). ...
... virginica) larvae ( Luckenbach et al. 1993) were observed in the presence of P. minimum blooms, indicating high density of P. minimum may have adverse effects on the filtering and feeding systems of bivalves. Moreover, the P. minimum blooms also caused 100% mortality of juvenile oysters within 14 days and at 33% bloom density caused 43% mortality over 22 days ( Luckenbach et al. 1993). The gill damage hypothesis had not been confirmed, and no follow-up studies of scallops in natural P. minimum blooms were conducted until the occurrence of mass mortality of wild eastern oyster, C. virginica, populations in Chesapeake Bay ( Sellner et al. 1995). ...
Article
Polycyclic aromatic hydrocarbons (PAHs) are a class of hazardous organic contaminants that are widely distributed in nature, and many of them are potentially toxic to humans and other living organisms. Biodegradation is the major route of detoxification and removal of PAHs from the environment. Aerobic biodegradation of PAHs has been the subject of extensive research; however, reports on anaerobic biodegradation of PAHs are so far limited. Microbial degradation of PAHs under anaerobic conditions is difficult because of the slow growth rate of anaerobes and low energy yield in the metabolic processes. Despite the limitations, some anaerobic bacteria degrade PAHs under nitrate-reducing, sulfate-reducing, iron-reducing, and methanogenic conditions. Anaerobic biodegradation, though relatively slow, is a significant process of natural attenuation of PAHs from the impacted anoxic environments such as sediments, subsurface soils, and aquifers. This review is intended to provide comprehensive details on microbial degradation of PAHs under various reducing conditions, to describe the degradation mechanisms, and to identify the areas that should receive due attention in further investigations.
... NEC=0.5 µg ST X100g −1 ). Different studies reported declines in bivalve growth rates during an exposure to PST-producing algae (Erard-Le Denn et al., 1990;Nielsen and Strømgren, 1991;Bricelj et al., 1993;Luckenbach et al., 1993;Hermabessiere et al., 2016). Based on these observations, we assumed that PST affected maintenance costs and calibrated this effect on growth experiments. ...
Thesis
Full-text available
L’huître creuse Crassostrea gigas est l’un des mollusques les plus commercialisé au monde. Cette espèce cosmopolite doit faire face à de nombreux agents pathogènes (bactéries, virus), parasites, xénobiotiques, et/ou micro-algues toxiques. En tant que bivalve filtreur, elle peut accumuler de fortes charges de phycotoxines, dont les toxines paralysantes (PST), lorsqu’elle est exposée à des blooms de microalgues toxiques (HAB). Pour protéger la santé humaine, des interdictions de vente de coquillages sont déclarées lorsque ceux-ci sont contaminés en PST, impactant ainsi le secteur ostréicole. Ce travail de thèse a pour but de développer un modèle basé sur la théorie des Budgets d’Energie Dynamiques (DEB) décrivant la cinétique d’intoxication et de détoxication des PST chez C. gigas. Le couplage d’un modèle de bioaccumulation avec un modèle DEB permet de prendre en compte certaines variables physiologiques de l’huître et les conditions environnementales pour simuler avec précision la dynamique d’accumulation des PST. Deux expériences consistant à exposer C. gigas au dinoflagellé toxique Alexandrium minutum ont été réalisées. La consommation de toxines a été calibrée dans une première expérience à court terme où le taux de filtration et l’efficacité d’assimilation ont été mesurés individuellement durant une phase d’exposition à des micro-algues non-toxiques puis toxiques. Les taux de respiration et le rythme cardiaque ont également été mesurés. En identifiant trois phénotypes distincts ayant des potentiels d’accumulation différents, cette étude amène de nouvelles connaissances concernant l’importante variabilité inter-individuelle dans l’accumulation de PST observée chez C. gigas. Ensuite, une expérience à moyen terme a été menée où des naissains ont été exposés à un mélange de micro-algues toxiques et non-toxiques. Différentes conditions ont été mises en place pour calibrer (1) le processus d’élimination de toxines, (2) les effets des PST sur la bioénergétique de l’huître, et (3) valider une fonction permettant de traiter de la sélection alimentaire. Un modèle DEB simulant l’évolution de la concentration en PST basé sur deux compartiments (toxines non assimilées et assimilées) a ainsi été proposé et validé en utilisant des jeux de données obtenus en laboratoire et sur le terrain. Dans une dernière partie, le modèle a été utilisé pour étudier les différences d’accumulation entre les huîtres diploïdes et triploïdes selon leur masse, leur âge et leur stade de gamétogenèse. Les résultats obtenus tendent à montrer que les triploïdes accumulent plus que les diploïdes, excepté après la ponte de ces dernières.
... Ichthyotoxic; Toxic to marine mammals; Neurotoxic; Toxic to phytoplankton [88,107,109] Heterocapsa circularisquama ROS; Hemolysin Toxic to mollusks; Antialgal; Antiprotozoal; Toxic to zooplankton [110][111][112][113][114][115] Akashiwo sanguineum (=Gymnodinium sanguineum) ROS Ichthyotoxic; Toxic to mollusks; Antimycotic; Toxic to mice [55,98,116,117] Karlodinium veneficum ROS Ichthyotoxic; Toxic to zooplankton [55,118,119] Alexandrium catenella Saxitoxin; Neosaxitoxin; Gonyautoxin; N-sulfocarbomoyl toxins; Hemolysin; ROS Neurotoxic; Paralytic shellfish poisoning; Toxic to marine organisms [73,82,[120][121][122][123][124][125][126] Prorocentrum minimum Venerupin; Prorocentrin; ß-diketone; ROS Venerupin shellfish poisoning; Toxic to marine organism; Neurotoxic [127][128][129][130][131][132][133][134][135][136][137][138][139] Prymnesium parvum Prymnesin 1 and 2; Hemolysin ...
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Most marine phytoplankton with relatively high ROS generation rates are categorized as harmful algal bloom (HAB)-forming species, among which Chattonella genera is the highest ROS-producing phytoplankton. In this review, we examined marine microalgae with ROS-producing activities, with focus on Chattonella genera. Several studies suggest that Chattonella produces superoxide via the activities of an enzyme similar to NADPH oxidase located on glycocalyx, a cell surface structure, while hydrogen peroxide is generated inside the cell by different pathways. Additionally, hydroxyl radical has been detected in Chattonella cell suspension. By the physical stimulation, such as passing through between the gill lamellas of fish, the glycocalyx is easily discharged from the flagellate cells and attached on the gill surface, where ROS are continuously produced, which might cause gill tissue damage and fish death. Comparative studies using several strains of Chattonella showed that ROS production rate and ichthyotoxicity of Chattonella is well correlated. Furthermore, significant levels of ROS have been reported in other raphidophytes and dinoflagellates, such as Cochlodinium polykrikoides and Karenia mikimotoi. Chattonella is the most extensively studied phytoplankton in terms of ROS production and its biological functions. Therefore, this review examined the potential ecophysiological roles of extracellular ROS production by marine microalgae in aquatic environment.
... Flood-associated abiotic stressors can negatively impact larval survival and development in the water column (Baker and Mann, 1992;Clark and Gobler, 2016;Davis, 1958), as well as reduce growth rates and increase mortality in postmetamorphosis juveniles on the benthos (Dickinson et al., 2012;Loosanoff, 1952;Stevens and Gobler, 2018). Multiple marine HAB-forming species also have negative effects on early oyster life stages (Griffith et al., 2019;Luckenbach et al., 1993;Rolton et al., 2015), but the impacts of freshwater cyanobacteria blooms are unknown. Although larvae and post-settlement juveniles are known to be more sensitive to environmental stressors than adult oysters, the tolerance ranges of early life stages are not as well studied as in adults (His et al., 1999;Shumway, 1996). ...
Article
Oyster reefs provide essential ecosystem services but are severely degraded worldwide. Extreme flooding events, which can be intensified by water management decisions, reduce water quality in estuaries and further threaten oyster populations. Restoration and conservation of oysters is dependent on the success of early oyster life stages. This study examined the effect of water quality stressors associated with flooding events on the growth and survival of larval and juvenile oysters (Crassostrea virginica). In 96-h assays, we exposed D-stage larvae to a range of dissolved oxygen, microcystin-LR, pH, and salinity concentrations. These conditions were selected based on water quality data from the Mississippi Sound during a 2019 freshwater flooding event caused by the Bonnet Carré Spillway opening. There was no negative effect of microcystin-LR or pH on early veligers at the concentrations tested, but low salinity significantly reduced shell growth, and hypoxia (< 2 mg L⁻¹ O2) decreased both larval growth and survival. Post-metamorphosis juvenile oysters were exposed to the same water quality stressors for 24 days in the lab. Low DO, pH, and salinity treatments reduced juvenile change in wet weight and shell growth rates, but had no effects on survival. These laboratory-exposed juveniles were subsequently deployed into the field to assess the ability of juveniles to recover from short-term exposure to simulated flooding-associated stressors. After deployment to natural conditions in the Mississippi Sound, juvenile oysters were able to compensate for reduced growth during the lab exposure, even though survival was reduced for juveniles previously exposed to low pH during the first two weeks in the field. In general, early oyster life stages were relatively tolerant of the duration and stressor concentrations tested, but negative sublethal impacts of flood-associated stressors must be considered in the face of increasing frequency and duration of flooding events due to climate change.
... One concern of P. minimum blooms in Chesapeake Bay is their potential impact on oyster growth and reproduction. While laboratory results have been mixed, with Brownlee et al. (2005) and Stoecker et al. (2008) finding no negative effects of P. minimum on oysters for short exposures, Luckenbach et al. (1993) and Wikfors and Smolowitz (1995) found high mortality of Chesapeake Bay juvenile oysters exposed for N10 days to high bloom densities (10 4 to 10 5 cells mL −1 ) and negative effects on several life stages of eastern oysters. ...
Article
Retrospective analysis of water quality monitoring data reveals strong interannual shifts in the spatial distribution of two harmful algal species (Prorocentrum minimum and Karlodinium veneficum) in eutrophic Chesapeake Bay. A habitat model, based on the temperature and salinity tolerance of the two species as well as their nutrient preferences, provides a good interpretation for the observed seasonal progression and spatial distribution of these taxa. It also points to climate-induced variability in the hydrological forcing as a mechanism driving the interannual shifts in the algal distributions: both P. minimum and K. veneficum shift downstream during wetter years but upstream during dry years. Climate downscaling simulations using the habitat model show upstream shifts of the two species in the estuary and longer blooming seasons by the mid-21st century. Salt intrusion due to sea level rise will raise salinity in the estuary and cause these HAB species to migrate upstream, but increasing winter-spring flows may also drive favorable salinity habitat downstream. Warming leads to longer growing seasons of P. minimum and K. veneficum but may suppress bloom habitat during their respective peak bloom periods.
... Although the potential toxicity of P. minimum is not clear (Landsberg 2002;Vlamis et al., 2015), a number of events causing damages are associated with high concentrations of P. minimum (> 10 3 cells mL −1 ) (Alonso-Rodrıguez and Azanza et al., 2005;Heil et al., 2005;Tango et al., 2005). According to the previous studies, high concentrations of P. minimum can have detrimental effects on the survival or growth of aquatic organisms, such as fish (Azanza et al., 2005;Heil et al., 2005;Sierra-Beltrán et al., 2005;Tango et al., 2005), shellfish (Luckenbach et al., 1993;Hégaret and Wikfors 2005;Heil et al., 2005) and shrimp (Alonso-Rodrıguez and Páez-Osuna, 2003;Páez-Osuna et al., 2003;Sierra-Beltrán et al., 2005). ...
Article
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Prorocentrum minimum is a bloom-forming, planktonic mixotrophic dinoflagellate, and can cause stress in shrimp ponds. In this study, healthy Exopalaemon carinicauda were exposed to 5 ×10⁴ cells mL⁻¹P. minimum for 72 hours to investigate the adverse effect of P. minimum on shrimps. Elevated superoxide dismutase (SOD) activity and malondialdehyde (MDA) content, reduced total antioxidant capacity (T-AOC) and catalase (CAT) activity, and regulatory glutathione peroxidase (GPX) activity were found in the hemolymph of E. carinicauda after exposure to P. minimum. In this study, P. minimum exposure induced oxidative stress and caused significant oxidative damage to E. carinicauda. P. minimum exposure increased the expression of HSP70 gene in the hemocyte, gills and hepatopancreas. Compared with the enhanced level of caspase-3 gene mRNA in the hemocyte and gills, the up-regulation of caspase-3 gene in the hepatopancreas was only observed from 3 to 6 h, and then the mRNA level of glutathione-S-transferase (GST) gene increased. These results indicated that GST might be involved in the shrimp hepatopancreas’ defense against P. minimum exposure. The present study demonstrates that exposure to P. minimum could induce oxidative stress and apoptosis in E. carinicauda. The SOD activity, HSP70 and GST (in the hepatopancreas) were evoked to protect cells from oxidative stress and apoptosis. This study will provide new insights into the toxic mechanism of P. minimum on shrimps.
... Concentrations of Prorocentrum minimum were generally very low with the highest concentrations found in late April and May. Although several studies have demonstrated a detrimental impact of P. minimum on Crassostrea virginica health and growth (Luckenbach et al. 1993, Wikfors & Smolowitz 1995, their concentrations were more than 10 times higher than 254 cells/mL, the highest concentration in samples analyzed here. Furthermore, no other harmful algal species were observed. ...
Article
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Since 2012, aquacultured eastern oysters Crassostrea virginica have been reported by oyster farmers to display mortality approaching 30%, and in some cases 85%, in areas of the lower Chesapeake Bay, VA. Based on accounts from industry, this mortality has typically affected 1-y-old oysters between May and early July, and has tended to occur in triploid oysters, which represent the vast bulk of production in the area. During this period, samples submitted for pathology have not revealed the presence of major pathogens as a cause. In 2015, to gain deeper insight into this mortality and determine whether specific sites, ploidy condition, or genetic lines were affected, oyster seed commercially produced in early 2014 were obtained from four lines, one diploid (2N DEBY) and three triploid (3N DEBY, 3N hANA, and 3N Northern). These lines were deployed in July 2014 at aquaculture farms at five Chesapeake Bay locations: Locklies Creek and Milford Haven on the western shore, and Pungoteague Creek, Nassawadox Creek, and Cherrystone Creek on the Eastern Shore. During this study, mortality was observed to peak in June at most sites, reaching a mean mortality across all tested lines of 17.0% and a cumulative mortality for the study period of 32.0% at Nassawadox Creek, the site most severely affected by mortality that followed the expected early summer mortality pattern. Interval mortality at all sites decreased to under 5% after June, but cumulative levels for the study period reached from 8.8% to 18.6% even at the sites least affected by mortality. This represents a high level of mortality given the documented absence of material involvement by major oyster pathogens such as Hapolosporidium nelsoni and Perkinsus marinus. Infiltration of gill tissues by hemocytes, observed in up to 33% of individuals at Nassawadox Creek coincident with the increase in mortality, was the only pathology observed. Harmful algal blooms were not associated with the mortality, nor were abnormal temperatures or salinities. There was no clear relationship of mortality to oyster genetic heritage, although there was variability in susceptibility among oyster lines and interactions between lines and specific sites. At some locations and in comparison with diploids, triploid oysters appeared to be more susceptible to mortality. Mortality in triploids was coincident with the timing of peak gametogenic development in diploids. Given the lack of involvement by major pathogens and the possible association of mortality with oyster gametogenesis, future work should seek to better understand the suite of environmental stressors potentially impacting cultured oysters in these systems and their interactions with the physiology and energetics of these animals.
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