The copepod Calanus finmarchicus: A potential vector for trophic transfer of the marine algal biotoxin, domoic acid

The marine algal biotoxin, domoic acid (DA), is produced by certain members of the diatom genus Pseudo-nitzschia. This neurotoxin has been responsible for several mass mortality events involving marine birds and mammals. In all cases, the toxin was transferred from its algal producers through marine food webs by one or more intermediate vectors. The ability of some copepod taxa to serve as vectors for DA has been demonstrated; however, the role played in DA trophic transfer by Calanus finmarchicus, which often dominates N. Atlantic zooplankton assemblages and is a primary dietary component of the highly endangered N. Atlantic right whale (Eubalaena glacialis), has been uncertain. In the present study, we examined the ability of C. finmarchicus to consume DA-producing algae and retain the toxin. Results of grazing and toxin accumulation/depuration experiments showed that C. finmarchicus consumed DA-producing Pseudo-nitzschia multiseries regardless of the presence or absence of morphologically similar, but non-toxic, P. pungens, across initial cell concentrations ranging from 1000-4000 cells mL^− 1. Furthermore, C. finmarchicus did not appear to preferentially consume or avoid either Pseudo-nitzschia species tested. After ingestion of P. multiseries, copepods accumulated DA and retained it for up to 48 h post-removal of the toxin source. These findings provide evidence for the potential of C. finmarchicus to facilitate DA trophic transfer in marine food webs where toxic Pseudo-nitzschia is present.     

Feeding,egg production,and egg hatching success of the copepods Acartia tonsa and Temora longicornis on diets of the toxic diatom Pseudo-nitzschia multiseries and the non-toxic diatom Pseudo-nitzschia pungens

In 1987, there was an episode of shellfish poisoning in Canada with human fatalities caused by the diatom Pseudo-nitzschia multiseries, which produced the toxin domoic acid. In order to examine whether domoic acid in this diatom serves as a grazing deterrent for copepods, we compared feeding rates, egg production rates, egg hatching success and mortality of the calanoid copepods Acartia tonsa and Temora longicornis feeding on unialgal diets of the toxic diatom P. multiseries and the similarly-sized non-toxic diatom Pseudo-nitzschia pungens. Copepods were collected in summers of 1994, 1995 and 1996 from Shediac Bay, New Brunswick, Canada, near Prince Edward Island, the site of the 1987 episode of domoic acid shellfish poisoning. Rates of ingestion of the toxic versus the non-toxic diatom by A. tonsa and T. longicornis were similar, with only one significantly different pair of values obtained in 1994, for which A. tonsa had a higher mean rate of ingestion of the toxic than the non-toxic diatom. Thus, domoic acid did not appear to retard grazing. Analyses of copepods with high performance liquid chromatography (HPLC) revealed that copepods accumulated domoic acid when feeding on P. multiseries. Egg production rates of copepods when feeding on P. multiseries and P. pungens were very low, ranging from 0 to 2.79 eggs female^–1 d^–1. There did not appear to be differential egg production or egg hatching success on diets of the toxic and non-toxic diatoms. Mortality of females on the toxic diet was low, ranging from 0 to 20%, with a mean of 13%, and there was no apparent difference between mortality of copepods feeding on toxic versus non-toxic diatoms. Egg hatching success on both diets, although based on few eggs, ranged between 22% and 76%, with a mean percentage hatching of 45%. Diets of the non-toxic diatom plus natural seawater assemblages supplemented with dissolved domoic acid, revealed similar rates and percentages when compared to previous experiments. In summary, none of the variables measured indicated adverse effects on copepods feeding on the toxic compared to the non-toxic diatom.     

Note on the occurrence of Pseudo-nitzschia australis and domoic acid in squid from Monterey Bay, CA (USA)

Over the past decade diatom blooms of domoic acid (DA)-producing Pseudo-nitzschia spp. have been responsible for numerous marine mammal and bird mortalities in Monterey Bay, CA. One possible toxin vector is the market squid, Loligo opalescens, a small pelagic mollusk that plays an important role in the near-shore food web of the California Current ecosystem as a favored vertebrate prey species. This study examined the trophic link between toxic Pseudo-nitzschia and L. opalescens using toxin and stomach content analyses of animals collected from Monterey Bay, CA in 2000. Receptor binding assay data (confirmed by tandem mass spectrometry), demonstrated the presence of DA in squid during a toxic Pseudo-nitzschia event, with P. australis frustules observed in stomach samples. Though DA levels were low (<0.5 μg DA g⁻¹ tissue) in L. opalescens during the study period, it is now clear that this potent neurotoxin can occur in squid and is likely delivered through its krill prey species, which are known to retain DA after feeding on toxic Pseudo-nitzschia. Our findings suggest that further study of the relationship between Pseudo-nitzschia blooms and DA contamination of squid is warranted to better evaluate the potential health risk to humans and wildlife associated with this major commercial seafood species and important prey item.     

Characterization of a toxic Pseudo-nitzschia spp. bloom in the Northern Gulf of Mexico associated with domoic acid accumulation in fish

A toxic bloom of Pseudo-nitzschia spp. was observed in the Alabama coastal waters of the northern Gulf of Mexico (NGOM) in June 2009 that resulted in the accumulation of domoic acid (DA) in fish. The bloom initiated following a large storm event that likely caused increased groundwater discharge 16–20 days prior to peak densities. Eleven sites, located in littoral shoreline waters and inshore embayments spanning the entire Alabama NGOM coastline, were sampled during peak densities to assess Pseudo-nitzschia species composition and toxicity, and associated water-quality parameters. Small fish (0.27–11.9 g body weight) were collected at six of these sites for analysis of DA content. High Pseudo-nitzschia spp. densities (8.27 × 10⁴–5.05 × 10⁶ cell l⁻¹) were detected at eight sites located in the littoral shoreline and particulate DA was detected at six of these littoral sites (48.0–540 pg ml⁻¹). The bloom consisted primarily (>90%) of Pseudo-nitzschia subfraudulenta, a species previously characterized as forming only a minor component of Pseudo-nitzschia assemblages and not known to produce DA. Pseudo-nitzschia spp. were at low densities or not detected at the inshore sites and DA was detected at these sites. Pseudo-nitzschia spp. density varied along an estuarine gradient, with greater densities occurring in the most saline, clear, and nutrient-poor waters. Cell density was strongly and negatively correlated with silicate (Si) concentrations and the ratios of silicate to dissolved inorganic nitrogen and phosphate (Si:DIN and Si:PO₄). Cell toxin quota was negatively correlated with phosphate, and strongly and positively correlated with the ratio of total nitrogen to total phosphorus (TN:TP). These relationships are consistent with previous observations that indicate Pseudo-nitzschia spp. density and toxicity are likely to be greater in high salinity, high irradiance, and nutrient-poor waters. DA was detected in 128 of 131 (98%) of the fish collected, which included seven primary and secondary consumer species. This is the first demonstration of trophic transfer of DA in this region of the NGOM, indicating that toxic blooms of Pseudo-nitzschia spp. in Alabama coastal waters have the potential to transfer DA to recreationally and commercially important fish species.     

Host-specific adaptation governs the interaction of the marine diatom,Pseudo-nitzschia and their microbiota

The association of phytoplankton with bacteria is ubiquitous in nature and the bacteria that associate with different phytoplankton species are very diverse. The influence of these bacteria in the physiology and ecology of the host and the evolutionary forces that shape the relationship are still not understood. In this study, we used the Pseudo-nitzschia–microbiota association to determine (1) if algal species with distinct domoic acid (DA) production are selection factors that structures the bacterial community, (2) if host-specificity and co-adaptation govern the association, (3) the functional roles of isolated member of microbiota on diatom–hosts fitness and (4) the influence of microbiota in changing the phenotype of the diatom hosts with regards to toxin production. Analysis of the pyrosequencing-derived 16S rDNA data suggests that the three tested species of Pseudo-nitzschia, which vary in toxin production, have phylogenetically distinct bacterial communities, and toxic Pseudo-nitzschia have lower microbial diversity than non-toxic Pseudo-nitzschia. Transplant experiments showed that isolated members of the microbiota are mutualistic to their native hosts but some are commensal or parasitic to foreign hosts, hinting at co-evolution between partners. Moreover, Pseudo-nitzschia host can gain protection from algalytic bacteria by maintaining association with its microbiota. Pseudo-nitzschia also exhibit different phenotypic expression with regards to DA production, and this depends on the bacterial species with which the host associates. Hence, the influences of the microbiota on diatom host physiology should be considered when studying the biology and ecology of marine diatoms.     

Blooms of Pseudo-nitzschia and domoic acid in the San Pedro Channel and Los Angeles harbor areas of the Southern California Bight, 2003–2004

Abundances of Pseudo-nitzschia spp. and concentrations of particulate domoic acid (DA) were determined in the Southern California Bight (SCB) along the coasts of Los Angeles and Orange Counties during spring and summer of 2003 and 2004. At least 1500 km² were affected by a toxic event in May/June of 2003 when some of the highest particulate DA concentrations reported for US coastal waters were measured inside the Los Angeles harbor (12.7 μg DA L⁻¹). Particulate DA levels were an order of magnitude lower in spring of 2004 (February and March), but DA concentrations per cell at several sampling stations during 2004 exceeded previously reported maxima for natural populations of Pseudo-nitzschia (mean = 24 pg DA cell⁻¹, range = 0–117 pg DA cell⁻¹). Pseudo-nitzschia australis dominated the Pseudo-nitzschia assemblage in spring 2004. Overall, DA-poisoning was implicated in >1400 mammal stranding incidents within the SCB during 2003 and 2004. Ancillary physical and chemical data obtained during our regional surveys in 2004 revealed that Pseudo-nitzschia abundances, particulate DA and cellular DA concentrations were inversely correlated with concentrations of silicic acid, nitrogen and phosphate, and to specific nutrient ratios. Particulate DA was detected in sediment traps deployed at 550 and 800 m depth during spring of 2004 (0.29–7.6 μg DA (g sediment dry weight)⁻¹). The highest DA concentration in the traps was measured within 1 week of dramatic decreases in the abundances of Pseudo-nitzschia in surface waters. To our knowledge these are the deepest sediment trap collections from which DA has been detected. Sinking of the spring Pseudo-nitzschia bloom may constitute a potentially important link between DA production in surface waters and benthic communities in the coastal ocean near Los Angeles. Our study indicates that toxic blooms of Pseudo-nitzschia are a recurring phenomenon along one of the most densely populated coastal stretches of the SCB and that the severity and magnitude of these events can be comparable to or greater than these events in other geographical regions affected by domoic acid.     

Pseudo-nitzschia simulans sp. nov. (Bacillariophyceae), the first domoic acid producer from Chinese waters

The genus Pseudo-nitzschia has attracted attention because of production of the toxin, domoic acid (DA), causing Amnesic Shellfish Poisoning (ASP). Pseudo-nitzschia blooms occur frequently in Chinese coastal waters, and DA has been detected in several marine organisms, but so far no Pseudo-nitzschia strains from Chinese waters have been shown to produce DA. In this study, monoclonal Pseudo-nitzschia strains were established from Chinese coastal waters and examined using light microscopy, electron microscopy and molecular markers. Five strains, sharing distinct morphological and molecular features differentiating them from other Pseudo-nitzschia species, represent a new species, Pseudo-nitzschia simulans sp. nov. Morphologically, the taxon belongs to the P. pseudodelicatissima group, cells possessing a central nodule and each stria comprising one row of poroids. The new species is characterized by the poroid structure, which typically comprises two sectors, each sector located near opposite margins of the poroid. The production of DA was examined by liquid chromatography tandem mass spectrometry (LC–MS/MS) analyses of cells in stationary growth phase. Domoic acid was detected in one of the five strains, with concentrations around 1.05–1.54 fg cell⁻¹. This is the first toxigenic diatom species reported from Chinese waters.     

An assessment of Pseudo-nitzschia population dynamics and domoic acid production in coastal Louisiana

Over 1200 samples were collected from Louisiana estuarine and coastal shelf waters between 1989 and 2002, and analyzed to examine the population dynamics of Pseudo-nitzschia and to assess the potential threat posed by domoic acid (DA), a potent neurotoxin produced by some members within this toxigenic diatom genus. Results demonstrated that three species in this region (Pseudo-nitzschia multiseries, P. pseudodelicatissima complex, P. delicatissima) produce DA, and that particulate toxin levels were highest (up to 3.05 μg L⁻¹) during the spring bloom, while cellular concentrations were highest in the winter/early spring when P. multiseries was most abundant (up to 30 pg cell⁻¹). These particulate toxin levels are comparable to those seen in other regions (e.g., United States west coast) where DA poisoning events have occurred in the past. Pseudo-nitzschia were most abundant under dissolved inorganic nitrogen-replete conditions coupled with lower silicate and/or phosphate concentrations, and in the early spring months when temperatures were cooler. Pseudo-nitzschia were occasionally well-represented in the phytoplankton assemblage (≥10⁶ cells L⁻¹ in 14% of samples, over 50% of total phytoplankton in 5% of samples), indicating that planktivores (e.g., Gulf menhaden, Brevoortia patronus) may have little choice but to consume Pseudo-nitzschia cells, thereby providing potential vectors for DA transfer to higher trophic levels. By comparison, eastern oysters (Crassostrea virginica) present in estuarine waters may be more exposed to this toxin when Pseudo-nitzschia cells are part of a mixed assemblage, reducing selective grazing by these bivalves. C. virginica may thus represent the most effective vector for DA exposure in humans.     

Toxic Pseudo-nitzschia multistriata (Bacillariophyceae) from the Gulf of Naples: morphology,toxin analysis and phylogenetic relationships with other Pseudo-nitzschia species

The genus Pseudo-nitzschia includes several species capable of producing domoic acid, the causative agent of Amnesic Shellfish Poisoning. Some of these species have been recorded frequently in the Gulf of Naples. For one of the species, P. multistriata, which has been recurrently found in our sampling area since 1995, this is the first report for European waters. Here we provide further details on the fine structure of this species. Pseudo-nitzschia multistriata was the only one found to produce domoic acid among all the Pseudo-nitzschia species from the Gulf of Naples, and this finding raises the number of potentially toxic species in this genus to nine. Phylogenetic relationships among several Pseudo-nitzschia species were assessed using the hypervariable domains (D1–D3) of the large subunit (LSU) rDNA. The match between the phylogeny obtained and important taxonomic characters used in this genus are discussed. Results show that P. multistriata clusters with wider species lacking a central larger interspace in the raphe. Close genetic relationships were determined between P. fraudulenta and P. subfraudulenta, and between P. pungens and P. multiseries. Genetic differences among these pairs of species are comparable to those among isolates of P. pseudodelicatissima from the Gulf of Naples, indicating high intraspecific genetic diversity of Pseudo-nitzschia species in the relatively conserved LSU region. This could explain the problematic results obtained when testing a match between species-specific Pseudo-nitzschia LSU probes and our sequences.     

PSEUDO-NITZSCHIA SPECIES (BACILLARIOPHYCEAE) IN LOUISIANA COASTAL WATERS: MOLECULAR PROBE FIELD TRIALS, GENETIC VARIABILITY, AND DOMOIC ACID ANALYSES

An 18-month field survey of the Pseudo-nitzschia population present in Louisiana coastal waters was conducted comparing species abundance estimates by novel fluorescent molecular probes (16S large subunit rDNA oligonucleotide sequences) with traditional electron and differential-interference light microscopy. While the probe and microscopic analyses agreed on the presence or absence of four common Pseudo-nitzschia species ( P. multiseries (Hasle) Hasle, P. pseudodelicatissima (Hasle) Hasle, P. delicatissima (P.T. Cleve) Heiden, and P. pungens (Grunow) Hasle in 66% of the samples analyzed, the probes gave conflicting results with the microscopic methods in the remaining 34% of the samples. The majority of the discrepancies appear to be because of genetic variation within the Pseudo-nitzschia population, especially in P. pseudodelicatissima, indicating that the Monterey Bay Pseudo-nitzschia spp. may not be appropriate reference strains for distinguishing Louisiana Pseudo-nitzschia spp. Additionally, P. pseudodelicatissima has been associated with domoic acid (DA) activity in three field samples, at levels up to 22 times higher than the highest value given inother published reports of DA production by this species. The contemporaneous existence of multiple strains of P. pseudodelicatissima (toxic and non-toxic) presents new challenges to the study of the ecophysiology and population dynamics of this bloom-forming species.     

First record of the dynamics of domoic acid producing Pseudo-nitzschia spp. in Indonesian waters as a function of environmental variability

Within the past few decades, harmful algal blooms (HABs) have occurred frequently in Indonesian waters, resulting in environmental degradation, economic loss and human health problems. So far, HAB related studies mainly addressed ecological traits and species distribution, yet toxin measurements were virtually absent for Indonesian waters. The aim of the present study was to explore variability of the potentially toxic marine diatom genus Pseudo-nitzschia, as well as its neurotoxin domoic acid as a function of environmental conditions in Ambon Bay, eastern Indonesia. Weekly phytoplankton samples, oceanographic (CTD, nutrients) and meteorological (precipitation, wind) parameters were analyzed at 5 stations in the bay during the dry and wet seasons of 2018. Liquid chromatography – tandem mass spectrometry (LC–MS/MS) was used to detect particulate DA (pDA). Vegetative cells of Pseudo-nitzschia spp. and pDA were found in 98.6% and 51.4% of the samples, respectively. pDA levels were low, yet detected throughout the campaign, implying that Ambon Bay might potentially be subject to amnesic shellfish poisoning. The highest levels of both Pseudo-nitzschia spp. cell abundance and pDA were found in the wet season, showing a strong positive correlation between both parameters, compared to the dry season, (r = 0.87 and r = 0.66 (p < 0.01), respectively). Statistical analyses revealed that temperature and mixed layer depth positively correlated with Pseudo-nitzschia spp. and pDA during the dry season, while ammonium showed positive correlations in both seasons. This study represents the first successful investigation of the presence and variability of Pseudo-nitzschia spp. and its neurotoxin DA in Indonesian waters.     

Domoic acid in a marine pelagic food web: Exposure of southern right whales Eubalaena australis to domoic acid on the Península Valdés calving ground,Argentina

The gulfs that surround Península Valdés (PV), Golfo Nuevo and Golfo San José in Argentina, are important calving grounds for the southern right whale Eubalaena australis. However, high calf mortality events in recent years could be associated with phycotoxin exposure. The present study evaluated the transfer of domoic acid (DA) from Pseudo-nitzschia spp., potential producers of DA, to living and dead right whales via zooplanktonic vectors, while the whales are on their calving ground at PV. Phytoplankton and mesozooplankton (primary prey of the right whales at PV and potential grazers of Pseudo-nitzschia cells) were collected during the 2015 whale season and analyzed for species composition and abundance. DA was measured in plankton and fecal whale samples (collected during whale seasons 2013, 2014 and 2015) using liquid chromatography coupled to tandem mass spectrometry (LC–MS/MS). The genus Pseudo-nitzschia was present in both gulfs with abundances ranging from 4.4 × 10² and 4.56 × 10⁵ cell l⁻¹. Pseudo-nitzschia australis had the highest abundance with up to 4.56 × 10⁵ cell l⁻¹. DA in phytoplankton was generally low, with the exception of samples collected during a P. australis bloom. No clear correlation was found between DA in phytoplankton and mesozooplankton samples. The predominance of copepods in mesozooplankton samples indicates that they were the primary vector for the transfer of DA from Pseudo-nitzschia spp. to higher trophic levels. High levels of DA were detected in four whale fecal samples (ranging from 0.30 to 710 μg g⁻¹ dry weight of fecal sample or from 0.05 and 113.6 μg g⁻¹ wet weight assuming a mean water content of 84%). The maximum level of DA detected in fecal samples (710 μg DA g⁻¹ dry weight of fecal sample) is the highest reported in southern right whales to date. The current findings demonstrate for the first time that southern right whales, E. australis, are exposed to DA via copepods as vectors during their calving season in the gulfs of PV.     

摄食信息对球形棕囊藻和布氏双尾藻竞争结果的影响

浮游动物的摄食信息能增大棕囊藻囊体体积,囊体形成被认为是棕囊藻的诱导性防御机制。利用桡足类火腿伪镖水蚤和异养甲藻海洋尖尾藻释放的摄食信息,研究了诱导性防御对球形棕囊藻和布氏双尾藻的竞争的影响。结果表明,球形棕囊藻接收了火腿伪镖水蚤和海洋尖尾藻释放的摄食信息之后形成更大的囊体。防御启动后的球形棕囊藻比未接收摄食信息的球形棕囊藻更快地形成囊体,且囊体维持的时间更长。对照组和火腿伪镖水蚤摄食信息诱导的球形棕囊藻的生物体积比布氏双尾藻更高,且球形棕囊藻在竞争中占优势;而海洋尖尾藻摄食信息诱导的球形棕囊藻生物体积低于布氏双尾藻,且球形棕囊藻相对布氏双尾藻的竞争力下降。微型浮游动物海洋尖尾藻摄食信息导致球形棕囊藻相对硅藻布氏双尾藻的竞争力的下降,有利于解释硅藻先于棕囊藻发生藻华。     

Growth dynamics and domoic acid production of Pseudo-nitzschia sp. in response to oil and dispersant exposure

The diatom genus Pseudo-nitzschia is a common component of phytoplankton communities in the Gulf of Mexico and is potentially toxic as some species produce the potent neurotoxin domoic acid. The impact of oil and chemical dispersants on Pseudo-nitzschia spp. and domoic acid production have not yet been studied; preliminary findings from a mesocosm experiment suggest this genus may be particularly resilient. A toxicological study was conducted using a colony of Pseudo-nitzschia sp. isolated from a station off the coast of Louisiana in the Gulf of Mexico. The cultures were exposed to a water accommodated fraction (WAF) of oil and a diluted chemically enhanced WAF (DCEWAF) which was a mix of oil and dispersant (20:1). Exposure to WAF induced a lag phase but did not inhibit growth rates once in exponential growth. Cultures grown in DCEWAF did not experience a lag phase but had significantly lower growth rates than the Control and WAF cultures. The cellular quota of domoic acid was higher in cultures treated with DCEWAF and WAF relative to their control values, and half of the domoic acid had leaked out of the cells into the surrounding seawater in the DCEWAF cultures while all the domoic acid remained inside the cells in WAF-treated cultures. These results suggest that the presence of oil could lead to toxic blooms, but that the application of dispersant could decrease bioaccumulation of domoic acid through the food web.     

A toxic Pseudo-nitzschia bloom in Todos Santos Bay,northwestern Baja California,Mexico

A toxic Pseudo-nitzschia spp. bloom in the Todos Santos Bay area (31.8°N), Mexico, is described. This is the southernmost report of the presence of domoic acid (DA) in the California Current System and it is also the first report of the distribution of toxic Pseudo-nitzschia species and DA on the Baja California west coast. The maximum cell abundance of Pseudo-nitzschia was 3.02 × 10⁵ cells L^?1 and the maximum concentration of DA in particulate matter (pDA) was 0.86 μg L^?1. P. australis constituted the major proportion of cells identified as Pseudo-nitzschia. The environmental conditions associated with wind-driven upwelling were the cause for the accumulation of toxic cells. Maximum pDA and cell concentration were detected around 14 °C. The ratio of the concentration of macronutrients seemed to be the important factor for the accumulation of P. australis. The highest cell abundance was detected in areas with a high Si(OH)₄ to N ratio in the entire water column. Therefore, the relative increase of silicate concentration related to upwelling conditions was the probable cause for the accumulation of P. australis. Maximum photosystem II (PSII) quantum efficiency of charge separation (F_v/F_m) was negatively correlated to the pDA to fucoxanthin ratio. This ratio was used in this work as an index of cellular DA content. Therefore, the photosynthetic competence of the cells might be an important factor that affected their DA cellular content.     

The influence of salinity in the domoic acid effect on estuarine phytoplankton communities

Toxic species of the diatom genus Pseudo-nitzschia, observed worldwide from coastal waters to the open ocean, produce the neurotoxin domoic acid (DA). DA is an important environmental and economic hazard due to shellfish contamination with subsequent effects on higher trophic levels. Previous research has demonstrated that, among other environmental factors, salinity influences the abundance and toxicity of Pseudo-nitzschia. In this study, the environmental factors driving the growth of Pseudo-nitzschia and the production of dissolved DA (dDA) in North Inlet estuary were examined. The effect of salinity on the growth inhibition of phytoplankton induced by the initial presence as well as by an addition of dDA was also assessed. Initially, the diatom abundance was negatively correlated with the abundance of Pseudo-nitzschia and with the concentration of dDA. With the addition of a concentrated solution of dDA, the percent inhibition of cryptophytes and diatoms was significantly correlated with salinity and suggested a higher sensitivity to dDA at extreme salinities. These results emphasize the importance of salinity in assessing the properties of DA and potentially of other phycotoxins on phytoplankton.     

Empirical models of toxigenic Pseudo-nitzschia blooms: Potential use as a remote detection tool in the Santa Barbara Channel

The Santa Barbara Channel, CA is a highly productive region where wind-driven upwelling and mesoscale eddies are important processes driving phytoplankton blooms. In recent years, the spring bloom has been dominated by the neurotoxin-producing diatom, Pseudo-nitzschia spp. In this paper, we relate a 1.5-year time series of Pseudo-nitzschia spp. abundance and domoic acid concentration to physical, chemical, and biological data to better understand the mechanisms controlling local Pseudo-nitzschia spp. bloom dynamics. The data were used to define the ranges of environmental conditions associated with Pseudo-nitzschia spp. bloom development in the Santa Barbara Channel. The time series captured three large toxic events (max. particulate domoic acid concentration, pDA ～6000 ng L^?1; max. cellular domoic acid concentrations, cDA ～88 pg cell^?1) in the springs of 2005–2006 and summer 2005 corresponding to bloom-level Pseudo-nitzschia spp. abundance (>5.0 × 10⁴ cells L^?1). In general, large increases in Pseudo-nitzschia spp. abundance were accompanied by increases in cDA levels, and cDA peaks preceded pDA peaks by at least one month in both the springs of 2005 and 2006. Statistical models incorporating satellite ocean color (MODIS-Aqua and SeaWiFS) and sea surface temperature (AVHRR) data were created to determine the probability that a remotely sensed phytoplankton bloom contains a significant population of toxic Pseudo-nitzschia spp. Models correctly estimate 98% of toxic bloom situations, with a 7–29% rate of false positive identification. Conditions most associated with high cDA levels are low sea surface temperature, high salinity, increased absorption by cDOM (412 nm), increased reflectance at 510/555 nm, and decreased particulate absorption at 510 nm. Future efforts to merge satellite and regionally downscaled forecasting products with these habitat models will help assess bloom forecasting capabilities in the central CA region and any potential connections to large-scale climate modes.     

Factors controlling the production of domoic acid by Pseudo-nitzschia (Bacillariophyceae): A model study

A mechanistic model has been developed to explore the factors controlling the production of domoic acid (DA) by the pennate diatom Pseudo-nitzschia. The idealized model allows consideration of the uncoupling between photosynthesis and growth, while DA production has been set as a secondary metabolism sharing common precursors with growth. Under growth limitation, these precursors can accumulate, resulting in an increased DA production. The model was first evaluated based on its ability to simulate the observed DA production by either silicon (Si) or phosphorus (P) limited batch cultures of Pseudo-nitzschia available in the literature. Sensitivity tests were further performed to explore how the ambient nutrients and the light regime (intensity and photoperiod length) are possibly directing the Pseudo-nitzschia toxicity. The general pattern that emerged is that excess light, in combination with Si or P limitation, favours DA production, provided nitrogen (N) is sufficient. Model simulations with varying nutrient stocks supporting Pseudo-nitzschia blooms under non-limiting light suggest two potential ways for nutrients to control DA production. First, N excess in comparison to available Si and P relieves DA production from its limitation by N, an absolute requirement of the DA molecule. Second, increased nutrient stocks amplify the DA production phase of the blooms (in addition to enhancing Pseudo-nitzschia biomass) which leads to an even more toxigenic bloom. Simulations investigating the light regime suggest a light threshold below which an important delay in DA production could be expected in Pseudo-nitzschia cultures. In the natural environment, the monitoring of light conditions during Pseudo-nitzschia blooms might help to anticipate the magnitude of the toxic event. Pseudo-nitzschia toxicity is indeed linked to the excess of primary carbon that accumulates during photosynthesis under growth limitation by nutrients.     

Concurrent exposure of bottlenose dolphins (Tursiops truncatus) to multiple algal toxins in Sarasota Bay, Florida, USA

Sentinel species such as bottlenose dolphins (Tursiops truncatus) can be impacted by large-scale mortality events due to exposure to marine algal toxins. In the Sarasota Bay region (Gulf of Mexico, Florida, USA), the bottlenose dolphin population is frequently exposed to harmful algal blooms (HABs) of Karenia brevis and the neurotoxic brevetoxins (PbTx; BTX) produced by this dinoflagellate. Live dolphins sampled during capture-release health assessments performed in this region tested positive for two HAB toxins; brevetoxin and domoic acid (DA). Over a ten-year study period (2000–2009) we have determined that bottlenose dolphins are exposed to brevetoxin and/or DA on a nearly annual basis (i.e., DA: 2004, 2005, 2006, 2008, 2009; brevetoxin: 2000, 2004, 2005, 2008, 2009) with 36% of all animals testing positive for brevetoxin (n = 118) and 53% positive for DA (n = 83) with several individuals (14%) testing positive for both neurotoxins in at least one tissue/fluid. To date there have been no previously published reports of DA in southwestern Florida marine mammals, however the May 2008 health assessment coincided with a Pseudo-nitzschia pseudodelicatissima bloom that was the likely source of DA observed in seawater and live dolphin samples. Concurrently, both DA and brevetoxin were observed in common prey fish. Although no Pseudo-nitzschia bloom was identified the following year, DA was identified in seawater, fish, sediment, snails, and dolphins. DA concentrations in feces were positively correlated with hematologic parameters including an increase in total white blood cell (p = 0.001) and eosinophil (p<0.001) counts. Our findings demonstrate that dolphins within Sarasota Bay are commonly exposed to two algal toxins, and provide the impetus to further explore the potential long-term impacts on bottlenose dolphin health.     

“Windows of opportunity” for dinoflagellate blooms: Reduced microzooplankton net growth coupled to eutrophication

Links between eutrophication, plankton community structure, microzooplankton grazing and dinoflagellate abundance were investigated in two tributaries of the Chesapeake Bay, the Choptank and Patuxent Rivers (MD, USA). Sampling and experiments were conducted during the spring of consecutive dry (below average freshwater flow) and wet (above average freshwater flow) years. During the wet year (2003), dissolved inorganic nitrogen, phytoplankton, and copepod biomass, but not microzooplankton abundance, were greater than in the dry year. In 2003, but not 2002, small cell size photosynthetic dinoflagellates were abundant and blooms occurred in both rivers. Average potential microzooplankton grazing pressure on small dinoflagellates was spatially and temporally variable, but was not significantly different between years. Our data suggest that the variability in microzooplankton grazing pressure provided “windows of opportunity” for net growth of dinoflagellates in response to nutrient loading. The lack of net population growth of micrograzers in response to increases in dinoflagellate prey allowed dinoflagellate blooms to reach relatively high densities, however grazing also appeared to be important in limitation or demise of some blooms. We hypothesize that uncoupling of micrograzer–prey dynamics was partly due to strong top-down control by copepods of microzooplankton in the proportionately more eutrophic year, and perhaps also due to inhibition of microzooplankton grazing/growth once dinoflagellate densities are high.