Next Article in Journal
Determination of River Ecological Flow Thresholds and Development of Early Warning Programs Based on Coupled Multiple Hydrological Methods
Next Article in Special Issue
Investigation of Biotoxicity and Environmental Impact of Prometryn on Fish and Algae Coexistent System
Previous Article in Journal
Can Plant-Associated Chironomids Be Used as an Indicator of Lake Status with the Alternative States Theory?
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Water
Volume 16
Issue 14
10.3390/w16141985
water-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Alexandrium catenella (Group I) Causes Higher and Faster Toxicity Than A. pacificum (Group IV) in Mytilus eduis

by
Seok Jin Oh
1,
Soo Yong Jeong
1 and
Moonho Son
2,*
1
Division of Earth Environmental System Science, Pukyong National University, Busan 48513, Republic of Korea
2
Southeast Sea Fisheries Research Institute, National Institute of Fisheries Science, Tongyeong 53085, Republic of Korea
*
Author to whom correspondence should be addressed.
Water 2024, 16(14), 1985; https://doi.org/10.3390/w16141985
Submission received: 4 June 2024 / Revised: 5 July 2024 / Accepted: 9 July 2024 / Published: 12 July 2024
(This article belongs to the Special Issue Aquatic Environmental Pollution and Ecotoxicological Studies)
Browse Figures
Versions Notes

Abstract

:
Consuming poisoned shellfish can lead to severe health problems and even death. Alexandrium catenella (Group I) and A. pacificum (Group IV) cause paralytic shellfish poisoning (PSP) in Korea, and PSP is detected more in a wider area. However, the association between toxic dinoflagellates and shellfish poisoning is unclear. Therefore, it is necessary to understand the toxicity, detoxification, and compositional differences in PSP in Mytilus edulis exposed to PSP caused by A. catenella and A. pacificum. High-performance liquid chromatography with post-column oxidation was used to analyze PSP toxicity in poisoned M. edulis. PSP in M. edulis increased as the A. catenella and A. pacificum cell density increased. However, the cell density of A. catenella peaked faster than that of A. pacificum, and a high level of toxicity was detected. In the detoxification experiment, PSP in M. edulis decreased rapidly within 24 h in filtered seawater. However, PSP was continuously detected without decreasing below the detection limit until the last day of the experiment. In addition, the carbamate composition (GTX1+4) was detected as the main toxic composition in poisoned M. edulis, unlike in vegetative cells. GTX1+4 can poison shellfish quickly when toxic dinoflagellates appear in the marine environment. However, poisoned shellfish take a long time to be completely detoxified. Moreover, if shellfish continuously feed on poisonous dinoflagellates, their toxicity can increase rapidly due to biotransformation. Our results can help identify the mechanisms of shellfish toxicity and detoxification after PSP caused by toxic dinoflagellates.

1. Introduction

Bivalves feed on particulate organic matter floating in seawater, and toxic plankton can accumulate poison in the shellfish, leading to them being poisoned. Consuming poisoned shellfish can lead to food poisoning and even death [1,2,3,4,5,6,7]. Among various shellfish poisons, paralytic shellfish poisoning (PSP) is caused by a toxin produced primarily by the dinoflagellate Alexandrium species, Gymnodinium catenatum, and Pyrodinium bahamense. PSP has been occurring for a long time in coastal environments and has strong heat-resisting properties that are not easily destroyed by general heating and cooking [8,9,10]. Among the more than 20 Alexandrium species, six species are present in Korea (A. catenella, A. affine, A. insuetum, A. pacificum, A. minitum, and A. fraterculus) [11,12,13]. Moreover, early detection of shellfish toxins accelerates with increasing water temperature, and the area of occurrence also expands [14,15]. Although PSP caused by A. pacificum (Group IV), which grows at relatively higher temperatures than A. catenella (Group I) [16], has not yet been reported, bivalves in late spring or early summer may be toxified due to climate change.
Aquaculture in the coastal areas of Korea, dominated by seaweed and shellfish, accounts for over 60% of Korea’s fishery production [17]. However, during spring in the southeastern coastal area of Korea, the PSP in shellfish aquaculture caused by A. catenella exceeds the regulatory limit (<80 μg/100 g of tissue) annually. The blue mussel Mytilus edulis is the second most productive shellfish after the Pacific oyster (Crassostrea gigas) and is produced in large quantities on the southern coast of Korea [18]. M. edulis is a filter feeder more easily poisoned than other bivalves under the same environmental conditions [19,20,21] and has high bioaccumulation [22,23,24]. Thus, mussels are typical biomarkers that provide an early warning of PSP, as they accumulate PSP and reach high toxicity faster than other species [25].
However, the PSP of bivalves is occasionally unrelated to toxic dinoflagellate exposure according to the increasing and decreasing cell density of toxic dinoflagellates in coastal areas [26] because the maximum toxicity of bivalves does not always match the maximum cell density of toxic dinoflagellates [27,28]. Moreover, PSP in bivalves has been observed even in coastal areas where the cell density of toxic dinoflagellates is extremely low or where appearances have not been reported yet [26,27,29,30]. Therefore, the relationship between toxic dinoflagellates and shellfish poisoning remains unclear.
This study investigated the toxicity and detoxification of M. edulis after exposure to A. catenella and A. pacificum to clarify the environmental conditions contributing to PSP caused by toxic dinoflagellates in the natural environment. We discuss the changes in toxin amount, toxicity, and toxicity composition during toxification and detoxification.

2. Materials and Methods

2.1. Microalgae Culture

A. catenella (JM-1) was collected from the surface seawater of Jangmok Bay in January 2021. The cells were separated with a Pasteur pipette (length 230 mm) and washed with filtered seawater (0.22 μm pore size, Millipore, Burlington, MA, USA) to establish monoclonal cells. A. pacificum (LIMS-PS-2611) was obtained from the Library of Marine Samples at the Korea Institute of Ocean Science and Technology. f/2 medium [31] based on the Southern Sea of Korea was used, and the incubation temperature, salinity, and light conditions were 15 °C, 30 psu, and 300 µmoL/m2/s (12-h period), respectively, to maintain the A. catenella and A. pacificum cultures.
Two types of mass cultures were used for the exposure experiments. The batch culture for the initial culture was started in 250 mL of f/2 medium, and the culture conditions were the same as those for the maintenance culture. A mass culture system was then constructed by inoculating the two species in 10 L and 30 L water tanks, respectively, and the exposure experiment was performed by culturing until the late exponential phase.

2.2. Toxification of M. edulis by Continuous Exposure to A. catenella and A. pacificum

M. edulis were collected from the tidal zone of Jangmok Bay. The shell length, height, width, and wet weight were 65.34 ± 5.93 mm, 24.04 ± 2.59 mm, 35.86 ± 2.67 mm, and 5.52 ± 1.4 g, respectively. M. edulis transported to the laboratory were acclimatized (15 ± 1 °C; DBA-075, Daeil Cooler Co., Busan, Republic of Korea) in 10 L filtered (GF/C filter; 1.2 µm pore size) seawater in a 20 L water tank for 3–5 days, and aerated using an aquarium air pump. The same conditions were maintained during the experimental period, and freshly filtered seawater was exchanged once every two days.
Total 18 M. edulis individuals was continuously exposed to A. catenella and A. pacificum for five days. A. catenella at cell densities of 10, 100, and 1000 cells/mL and A. pacificum at cell densities of 10 and 100 cells/mL were constantly inoculated into the experimental tank containing M. edulis under 15 ± 1 °C, 30 psu, 100 μmoL/m2/s (12-h period), similar to the acclimatization conditions (Figure 1). Three M. edulis individuals in the experimental tank were randomly collected at the same time every day, and their whole flesh was analyzed. An aquarium air pump was used to prevent suffocation, and every effort was made to protect the M. edulis from external stimuli during the experimental period. Before initiating the experiment, the toxicity of M. edulis was below the detection limit (Day 0). Three M. edulis individuals in the experimental tank were randomly collected at the same time every day, and their whole flesh was analyzed. To compare the toxic compositions of Alexandrium species and M. edulis, the toxic compositions of Alexandrium species were analyzed immediately before exposure.

2.3. Detoxification of M. edulis Poisoned by A. catenella and A. pacificum

The exposure solution (10 L) containing A. catenella and A. pacificum was exposed to the 20 L experimental tank containing M. edulis (maximum cell densities of A. catenella and A. pacificum were approximately 2500 and 4500 cells/mL, respectively). Microscopic observations confirmed that M. edulis consumed A. catenella and A. pacificum in the exposure solution for 20 min. The experimental conditions of temperature, salinity, and light intensity were identical to those used for the continuous exposure experiments. For the detoxification analysis, three M. edulis individuals were randomly collected from the experimental tank at the same time each day, and their whole flesh was analyzed. The initial toxicity to M. edulis (day 0), before exposure, was below the detection limit. One day after the first exposure to Alexandrium, the entire volume of seawater in the experimental tank was replaced with freshly filtered seawater. The experiment was conducted over nine days.

2.4. PSP Analysis Using High-Performance Liquid Chromatography

PSP toxicity and toxin composition were measured in the whole flesh of three M. edulis individuals collected at 16:00 on the first, second, third, fourth, and fifth days after continuous exposure to A. catenella and A. pacificum. Fresh samples from three M. edulis individuals and two species of Alexandrium were immediately pretreated to toxin analysis by the following protocol. The supernatants were removed by centrifuging (3000× g, 10 min; Combi-514R, Hanmail Scientific Inc., Deajeon, Republic of Korea) using cells in the late exponential growth phase to analyze the PSP of A. catenella and A. pacificum. Then, 0.5 N acetic acid was added, and after freezing for 24 h (−20 °C), the cells were fragmented using a sonicator, and the supernatant was fractionated through centrifugation (3000× g, 10 min). The aliquoted supernatant was filtered with an ultrafiltration filter (10,000 MW, Millipore; Merk Millipore, Billerica, MA, USA) and frozen (−20 °C) until analysis.
For M. edulis PSP analysis, the same amount of 0.1 N HCl as the weight of the whole flesh was added, and the tissue was fragmented using a sonicator. After boiling at 100 °C for 5 min, the mixture was centrifuged at 3000× g for 10 min. The supernatant was passed through a Sep-pak C18 cartridge (Waters Associates Inc., Mulford, MA, USA), filtered through an ultrafilter (10,000 MW), and frozen (−20 °C) until analysis. All pretreated samples were subjected to a HPLC (high-performance liquid chromatography) with fluorescence detector (UtiMate 3000, Thermo Fisher Scientific, Sunnyvale, CA, USA) with post-column derivatization and a Hypersil Gold C8 column (250 mm × 4.6 mm i.d., particle size 5 μm) as previously described by Oshima [32]. The toxin content and composition of the samples were determined by comparing the detection time and peak area with those of a standard toxin. The toxicity of the mussels was calculated from the calculated toxin content using the non-toxicity value [32]. Standard toxins (N-sulfocarbamoyl toxin 1 and 2, gonyautoxin 1 and 4, gonyautoxin 2 and 3, gonyautoxin 5 and 6, neosaxitoxin, and saxitoxin) were purchased from the National Research Council Institute for Marine Biosciences. Abbreviations of toxins are as follows: C1+2 = N-sulfocarbamoyl toxin 1+2, GTX 1+4 = gonyautoxin 1+4, GTX 2+3 = gonyautoxin 2+3, GTX 5+6 = gonyautoxin 5+6, neoSTX = neosaxitoxin, STX = saxitoxin.

3. Results

3.1. A. catenella Causes Higher Toxicity in M. edulis Than A. pacificum

When M. edulis was exposed to 10 cells/mL of A. catenella, the toxin amount and toxicity accumulated in M. edulis gradually increased from the first day after exposure (Figure 2a). However, no values exceeding the regulatory limit of 4 MU/g were observed. At 100 cells/mL (Figure 2b), the toxin amount and toxicity increased continually by day 4. However, the toxicity exceeded the regulatory limit from day 1 (4.86 MU/g). On the fifth day, the toxicity was approximately 17.5 times higher than the maximum toxicity (1.51 MU/g) when M. edulis was exposed to 10 cells/mL A. catenella. After exposing M. edulis to 1000 cells/mL (Figure 2c), the accumulated toxin amount in M. edulis on the fifth day was the highest at 65.1 nmoL/g. This toxin amount was approximately 35 and 3.76 times higher than that after exposure to 10 and 100 cells/mL, respectively. The toxicity increased rapidly from the second day and exceeded the regulatory limit. On the fifth day, the toxicity was 41.7 and 23.8 times higher than that of exposure to 10 and 100 cells/mL, respectively.
The toxin amounts and toxicities of M. edulis exposed to A. pacificum were lower than those exposed to A. catenella (Figure 3a). When M. edulis was exposed to 10 cells/mL of A. pacificum, the toxin amount and toxicity increased; however, the values were much lower than those in the 10 cells/mL continuous exposure experiment of A. catenella. Toxin amounts and toxicities increased with increased time after exposure to 100 cells/mL and were the highest on day 5 (Figure 3b); however, the toxicity was approximately 5.2 times lower than the maximum toxicity achieved by exposure to 100 cells/mL of A. catenella. Considering the M. edulis toxicities after continuous exposure to A. pacificum at 10 and 100 cells/mL, the toxicities of M. edulis continually exposed to 1000 cells/mL of A. pacificum may be much lower than those of A. catenella, although an exposure of 1000 cells/mL of A. pacificum was not tested.

3.2. Fresh Seawater Detoxifies M. edulis

The toxin content and toxicity in M. edulis exposed to A. catenella reached the maximum values on the first day after exposure, exceeding the shipping prohibition toxicity standard value (Figure 4a). On the second day, after the water was replaced with fresh seawater, the toxin content and toxicity decreased sharply to below the shipping prohibition toxicity standard value and continued to maintain a similar level until the ninth day. The maximum toxin content and toxicity were detected on the second day after A. pacificum exposure. However, the maximum toxin content and toxicity of A. pacificum were lower than those of A. catenella even though the cell density of A. pacificum was approximately 1.8 times higher than that of A. catenella (Figure 4b). The toxin content and toxicity rapidly decreased from the third day, and then gradually decreased until the last day.

3.3. GTX1+4 Is the Most Prevalent Composition in M. edulis Poisoned by A. catenella and A. pacificum

Among the toxic compositions of A. catenella vegetative cells used in this study, C1+2, GTX1+4, and neoSTX were the main compositions, whereas GTX2+3 and GTX5 were minor compositions (Table 1, Figure 5). The toxic compositions of A. pacificum vegetative cells comprised C1+2 and GTX 5 as the main compositions, and neoSTX as the minor composition (Table 1, Figure 6).
When M. edulis was exposed to A. catenella at a cell density of 10 cells/mL (Figure 5a), GTX1+4 was the most prevalent composition in M. edulis. On the first day of exposure, GTX1+4 and C1+2 accounted for 54.7% and 45.1%, respectively. On the second day, GTX1+4 expression increased substantially and was maintained until the fifth day. When M. edulis was exposed to A. catenella at a cell density of 100 cells/mL (Figure 5b), GTX1+4 increased considerably from the first day after exposure, unlike that at 10 cells/mL. After that, a similar trend was observed until the fifth day. When M. edulis was exposed to A. catenella at a cell density of 1000 cells/mL (Figure 5c), GTX1+4 accounted for 78.1% of the primary composition, similar to that at 100 cells/mL. Unlike in 10 and 100 cells/mL, neoSTX was detected as a minor composition (13.7%). When M. edulis was exposed to 10 cells/mL A. pacificum, the toxic composition of M. edulis was C1+2 from days 1 until 5 (Figure 6a). Unlike in 10 cells/mL A. catenella, no carbamate toxins were detected. However, when 100 cells/mL A. pacificum was exposed to M. edulis (Figure 6b), the toxic composition of GTX1+4 on the first day accounted for approximately 98.8% of the main compositions. C1+2 was detected as a minor composition, and the pattern was similar until the fifth day.

4. Discussion

Paralytic shellfish toxin in shellfish is expected to increase with the abundance of toxic dinoflagellates, including Alexandrium species. Continuous exposure to increasing A. catenella and A. pacificum cell densities rapidly increased the toxin amount and toxicity in M. edulis. Similarly, the toxicity of the Corbicula japonica clam gradually increased with the A. tamarense cell density, and the toxicity showed maximum values one week after exposure to the maximum A. tamarense cell density [33]. Furthermore, toxicity in mussels is associated with the abundance of A. catenella in Korean coastal areas [34]. Thus, if toxic dinoflagellates appear around bivalve aquaculture sites, the bivalves may be poisoned quickly. However, in some cases, bivalves were observed with PSP below the detection limit, even though the cell density of A. catenella and A. pacificum was high. Moreover, shellfish toxicity did not decrease, although non-toxic phytoplankton such as diatoms were dominant [35]. Discrepancies in the relationship between the cell density of toxic dinoflagellates and the toxicity of shellfish might have occurred because of biological factors such as temperature, salinity, and nutrients [36,37,38,39,40,41].
The paralytic shellfish toxin of M. edulis rapidly decreased within 24 h in the filtered seawater; however, it was continuously detected without decreasing below the detection limit until the last day of the experiment. The toxicity of low-poisoned (84 μg/100 g) blue mussels was reduced by approximately 36% after 10 days and decreased by approximately 40% after 1 month using a flow water tank, which was continuously supplied with seawater containing free toxic dinoflagellates. However, in highly poisoned (2684 μg/100 g) blue mussels, the toxicity was reduced by approximately 94% after 5 days and decreased by approximately 97% after 1 month [42]. Similarly, the toxicity of poisoned bivalves in a flow-water tank was reduced by 90% after 5 days, and toxicity was not detected after 1 month [43]. The detoxification of poisoned mussels possibly depends on excreting seawater from the gut containing digested or poorly digested toxic dinoflagellate cells in the early stages [44]. In contrast, Sekiguchi et al. [45] speculated that another unknown mechanism in toxin accumulation in the food chain involves toxin accumulation in bivalves. We hypothesized that the rapidly decreasing toxicity of mussels poisoned by A. catenella and A. pacificum in the early stages could be due to replacing the water with new filtered seawater. However, detoxification above 90% may require considerable time when using only filtered seawater.
Feeding activity is essential to detoxifying poisoned bivalves [46]. In a study on the detoxification rate of oysters exposed to A. minutum, the detoxification rate differed by more than two-fold depending on the presence of organic matter, and activating feeding behavior was due to promoting the overall metabolism (i.e., decomposition and excretion) of the intestinal excretion rate [47,48]. The results of our study, conducted under controlled conditions such as filtering seawater, would have differed from those of a natural environment where a large amount of organic matter exists. Therefore, to completely detoxify poisoned shellfish over a short period, continuously feeding non-toxic algae or moving shellfish to sea areas without toxic dinoflagellates rather than in a filtered seawater environment would be more effective. In Canada and the United States, detoxifying shellfish is achieved by moving poisoned shellfish to an area where no toxic plankton have been detected [49,50,51].
The toxic compounds produced by dinoflagellates remain constant and species-specific despite dramatic variations in toxicity [43,52,53,54,55,56]. Thus, the toxic composition has been used as a biochemical marker [55,57,58]. Although the toxin compositions of identified Alexandrium species in Korean coastal waters have rarely been reported, Kim et al. [57] and Cho and Lee [59] reported that the toxic compositions of A. tamarense in the southeastern coastal waters of Korea were C1 and neoSTX as major compositions, and GTX 1+4, GTX 2+3, and dcGTX 2+3 as minor compositions. However, STX and GTX 5 could not be detected in A. tamarense strains [59]. In addition, the major toxins produced by A. catenella (Group I) were C1+2, and those produced by A. tamarense (Group IV) were C1+2 and GTX4 in most isolates from similar coastal areas [60]. Recently, Baek et al. [34] found C1+2, GTX-1, and GTX-2 in A. catenella (Group I) bloom samples from the Geoje coast. In contrast, Shin et al. [16] found that GTX 3+4 (~90 mol%) was the dominant PSTs in A. catenella (Group I) and A. pacificum (Group IV). C2 (7.8 mole%) was the next most toxic compound in both species.
However, toxic compositions vary significantly with the growth phase and under different environmental conditions, such as temperature, salinity, and nutrients [36,38,39,41]. High salinity increases GTX 2+3 in A. minutum [36]. Furthermore, variations in toxic composition during exponential growth in batch cultures of Alexandrium isolates were also reported. The largest changes in the toxic composition occurred in response to variations in temperature [38]. Furthermore, the response of toxin composition under phosphorous depletion varied with the nitrogen source, such as urea, NH4, and NO3 [40]. Changes in the toxic composition of dinoflagellates under different nutrient conditions are strain-specific because apparent regular patterns of toxic composition changing under different nutrient conditions were not observed [39].
Poison in bivalves has a higher carbamoyl toxin than the N-sulfocarbamoyl toxin, which differs from the toxicity of ingested swimming cells [47,61,62]. When Aulacomy ater was exposed to A. catenella swimming cells, the main compositions of C1+2, GTX1+4, and GTX2+3 accounted for most of the primary toxic compositions in the bivalves [63]. In addition, the toxins detected in A. catenella swimming cells in the field were C1, GTX1, and GTX2. However, in M. galloprovincialis fed with them, toxic compositions were detected in the order of GTX1+4, GTX3, and STX [34]. Toxic dinoflagellates are converted into toxic carbamoyl toxins in shellfish tissues through hydrolysis at low pH and natural reducing agents when many unstable N-sulfocarbamoyl toxins are present owing to chemical toxin conversion [64,65,66]. In bivalves that feed on toxic dinoflagellates, chemical toxin conversion [65,66] through acid hydrolysis and natural reducing agents at low pH and bioconversion [32,47,67] through enzymatic reactions occur. Therefore, even if the toxic dinoflagellates have low toxicity owing to a large amount of N-sulfocarbamoyl toxin, it is likely that the toxicity level will be converted into a high-toxicity composition by the ingested dinoflagellates, which will increase the toxicity of shellfish and lead to public health risks. In this study, A. catenella required careful monitoring because this toxin conversion phenomenon was evident, and A. pacificum was expected to convert to a high level of toxicity in bivalves with continuous exposure.
In conclusion, M. edulis was exposed to toxic dinoflagellates, and toxicity was detected after 24 h. PSP accumulated in M. edulis was detected at a higher level when fed A. catenella than when fed A. pacificum and reached its maximum value quickly. The poisoned M. edulis was reduced to below the permissible PSP level within a short time in the absence of toxic dinoflagellates; however, it is expected that it will take a considerable amount of time to detoxify M. edulis below the detection limit completely. In addition, the N-sulfocarbamoyl composition (C1+2) was the main composition responsible for the toxicity of A. catenella and A. pacificum swimming cells, but the carbamate composition (GTX 1+4) was detected as the main composition because of biotransformation in M. edulis fed with it. Our study results can help to clarify the environmental conditions of PSP generation caused by toxic plankton in the future and help establish a preliminary forecast system for PSP. Therefore, continuous monitoring over more than 9 days is necessary to minimize damage. Furthermore, research on the differences in toxic compositions according to numerous A. catenella and A. pacificum strains and the changing toxic compositions under different environmental conditions is necessary to understand the PSP outbreak in Korean coastal areas.

Author Contributions

S.J.O. analyzed the data, designed the study and prepared the manuscript. S.Y.J. performed the experiments. M.S. participated in the design of the study and played the role of the corresponding author. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by grants from the National Institute of Fisheries Science (R2024047) and Korea Institute of Marine Science & Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries (20220252).

Institutional Review Board Statement

All organisms used for this research were phytoplankton and invertebrate bivalves and as such were not subject to the Korean Institutional Animal Care and Use Committee.

Data Availability Statement

The data presented in this study are available in the article.

Conflicts of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

  1. Edebo, L.; Lange, S.; Li, X.P.; Allenmark, S.; Lindgren, K.; Thompson, R. Seasonal, geographic, and individual variation of okadaic acid content in cultivated mussels in Sweden. APMIS 1988, 96, 1036–1042. [Google Scholar] [CrossRef] [PubMed]
  2. Silvert, W.; Rao, D.V.S. Dynamic model of the flux of domoic acid, a neurotoxin, through a Mytilus edulis population. Can. J. Fish. Aquat. Sci. 1992, 49, 400–405. [Google Scholar] [CrossRef]
  3. Taylor, F.J.R.; Fukuyo, Y.; Larsen, J.; Hallegraeff, G.M. Taxonomy of harmful dinoflagellates. In Manual on Harmful Marine Microalgae; Hallegraeff, G.M., Anderson, D.M., Cembella, A.D., Eds.; UNESCO: Paris, France, 2003; pp. 389–432. [Google Scholar]
  4. Anderson, D.M. Turning back the harmful red tide. Nature 1997, 388, 513–514. [Google Scholar] [CrossRef]
  5. Indrasena, W.M.; Gill, T.A. Thermal degradation of partially purified paralytic shellfish poison toxins at different times, temperatures, and pH. J. Food Sci. 2000, 65, 948–953. [Google Scholar] [CrossRef]
  6. Toyofuku, H. Joint FAO/WHO/IOC activities to provide scientific advice on marine biotoxins (research report). Mar. Pollut. Bull. 2006, 52, 1735–1745. [Google Scholar] [CrossRef]
  7. EFSA. Marine biotoxins in shellfish–Saxitoxin group. EFSA J. 2009, 1019, 1–76. [Google Scholar]
  8. Asakawa, M.; Takagi, M. Quantitative Relationship between PSP Components of Protogonyaulax tamarensis and of Scallops, from Funka Bay, Hokkaido. Bull. Fac. Fish. Hokkaido Univ. 1983, 34, 345–349. [Google Scholar]
  9. Takata, K.; Mizuta, M.; Monden, T. Reduction in toxicity of PSP-infested oysters by heat treatment. Food Hyg. Saf. Sci. 1994, 35, 624–630. [Google Scholar] [CrossRef]
  10. Mizuta, M.; Takata, K.; Monden, T.; Yoneda, T.; Yamauchi, S. Reduction in toxicity of PSP infested oysters during canning process. Food Hyg. Saf. Sci. 1995, 36, 423–427. [Google Scholar] [CrossRef]
  11. Kim, K.Y.; Matoko, Y.; Yasuwo, F.; Kim, C.H. Morphological observation of Alexandrium tamarense (Lebour) Balech, A. catenella (Whedon et Kofoid) Balech and one related morphotype (Dinophyceae) in Korea. Algae 2002, 17, 11–19. [Google Scholar] [CrossRef]
  12. Oh, S.J.; Park, J.A.; Kwon, H.K.; Yang, H.S.; Lim, W. Ecophysiological studies on the population dynamics of two toxic dinoflagellates Alexandrium tamarense and Alexandrium catenella isolated from the Southern Coast of Korea-I. Effects of temperature and salinity on the growth. J. Korean Soc. Mar. Environ. Energy 2012, 15, 133–141. [Google Scholar] [CrossRef]
  13. Kim, E.S.; Li, Z.; Oh, S.J.; Yoon, Y.H.; Shin, H.H. Morphological identification of Alexandrium species (Dinophyceae) from Jinhae-Masan Bay, Korea. Ocean Sci. 2017, 52, 427–437. [Google Scholar] [CrossRef]
  14. Kim, C.H.; Lee, J.S. Occurrence of toxic dinoflagellates and PSP toxin profiles in Alexandrium spp. from Jinhae bay, Korea. In Harmful and Toxic Algal Blooms; Yasumoto, T., Oshima, Y., Fukuyo, Y., Eds.; UNESCO: Paris, France, 1996; pp. 61–64. [Google Scholar]
  15. Lee, K.J.; Kwon, S.J.; Jung, Y.J.; Son, K.T.; Ha, K.S.; Mok, J.S.; Kim, J.H. Comparison of analytical methods for the detection of paralytic shellfish toxins (PSTs). Korean J. Fish. Aquat. Sci. 2017, 50, 669–674. [Google Scholar]
  16. Shin, H.H.; Li, Z.; Kim, H.J.; Park, B.S.; Lee, J.; Shin, A.-Y.; Park, T.-G.; Lee, K.W.; Han, K.H.; Youn, J.Y.; et al. Alexandrium cetenlla (Group I) and A. pacificum (Group IV) cyst germination, distribution, and toxicity in Jinhae-Masan Bay, Korea. Harmful Algae 2021, 110, 102122. [Google Scholar] [CrossRef]
  17. MOF. Statistical Yearbook of Oceans and Fisheries; MOF: Sejong, Republic of Korea, 2021. [Google Scholar]
  18. Lee, J.S.; Shin, I.S.; Kim, Y.M.; Chang, D.S. Paralytic shellfish toxins in the mussel, Mytilus edulis, caused the shellfish poisoning accident at Geoje, Korea, in 1996. Korean J. Fish. Aquat. Sci. 1997, 30, 158–160. [Google Scholar]
  19. Chun, J.H.; Lee, J.T.; Kim, S.C.; Lee, C.U.; Kim, J.Y.; Kim, B.S.; Paik, N.W. Bioassay on PSP in Some Shellfishes from Pusan and Kyungnam Area. Korean J. Malacol. 1986, 2, 1–9. [Google Scholar]
  20. Jeon, J.K.; Yi, S.K.; Huh, H.T. Paralytic Shellfish Poison of Bivalves in the Korean Waters. J. Korean Soc. Oceano. 1988, 23, 123–129. [Google Scholar]
  21. Shon, M.B.; Kim, Y.S.; Kim, C.R. Paralytic Shellfish Poisoning of Mediterranean mussels from Jinhae Bay in Korea. Korean J. Fish. Aquat. Sci. 2009, 42, 366–372. [Google Scholar] [CrossRef]
  22. Park, M.J.; Lee, H.J.; Lee, T.S.; Son, K.T.; Byun, H.S.; Park, J.H.; Jang, D.S. Comparison of paralytic shellfish poison contents and components in the different bivalve species. J. Fd. Hyg. Saf. 2000, 15, 293–296. [Google Scholar]
  23. Kim, Y.S.; Shon, M.B.; Kim, C.H. Paralytic Shellfish Poisoning Toxin Accumulation in Four Mussel Species Fed on Toxic Alexandrium tamarense. Korean J. Fish. Aquat. Sci. 2006, 39, 49–54. [Google Scholar]
  24. Mok, J.S.; Oh, E.G.; Son, K.T.; Lee, T.S.; Lee, K.J.; Song, K.C.; Kim, J.H. Accumulation and Depuration of Paralytic Shellfish Poison in Marine Organisms. Korean J. Fish. Aquat. Sci. 2012, 45, 465–471. [Google Scholar]
  25. Shumway, S.E. A review of the effects of algal blooms on shellfish and aquaculture. J. World Aquac. Soc. 1990, 21, 65–104. [Google Scholar] [CrossRef]
  26. Dong, D.S.; Shin, I.S.; Cho, H.R.; Kim, J.H.; Pyeun, J.H.; Park, Y.H. Studies on distribution, characterization and detoxification of shellfish in Korea 1. A study on the distribution of paralytic shellfish poison. Korean J. Fish. Aquat. Sci. 1988, 21, 113–126. [Google Scholar]
  27. Nishitani, L.; Hood, R.; Wakeman, J.; Chew, K.K. Potential importance of an endoparasite of Gonyaulax in paralytic shellfish poisoning outbreaks. In Seafood Toxin; Edward, P.R., Ed.; American Chemical Society: Washington, DC, USA, 1984; pp. 139–149. [Google Scholar]
  28. Shin, I.S.; Chang, D.S. Studies on thermal resistance of paralytic shellfish poison in blue mussel. Korean J. Food Sci. Technol. 1990, 22, 799–801. [Google Scholar]
  29. Prakash, A.; Medcof, J.C.; Tennant, A.D. Paralytic Shellfish Poisoning in Eastern Canada; Fisheries Research Board of Canada: Ottawa, ON, Canada, 1971. [Google Scholar]
  30. Hashimoto, Y.; Noguchi, T.; Adachi, R. Occurrence of toxic bivalves in association with the bloom of Gonyaulax sp. in Owase Bay. Nippon Suisan Gakk. 1976, 42, 671–676. [Google Scholar] [CrossRef]
  31. Culture methods. In Manual on Harmful Marine Microalgae; Hallegraeff, G.M.; Anderson, D.M.; Cembella, A.D. (Eds.) UNESCO: New York, NY, USA, 1995; pp. 45–62. [Google Scholar]
  32. Oshima, Y. Post-column derivatization HPLC methods for paralytic shellfish poisons. In Manual on Harmful Marine Microalgae; Hallegraeff, G.M., Anderson, D.M., Cembella, A.D., Eds.; UNESCO: Pairs, France, 1995; pp. 81–94. [Google Scholar]
  33. Yamamoto, K.; Tsujimura, H.; Nakajima, M.; Harrison, P.J. Flushing rate and salinity may control the blooms of the toxic dinoflagellate Alexandrium tamarense in a river/estuary in Osaka Bay, Japan. J. Oceanogr. 2013, 69, 727–736. [Google Scholar] [CrossRef]
  34. Baek, S.H.; Choi, J.M.; Lee, M.; Park, B.S.; Zhang, Y.; Arakawa, O.; Takatani, T.; Jeon, J.K.; Kim, Y.O. Change in paralytic shellfish toxins in the mussel Mytilus galloprovincialis depending on dynamics of harmful Alexandrium catenella (Group I) in the Geoje coast (South Korea) during bloom season. Toxins 2020, 12, 442. [Google Scholar] [CrossRef]
  35. Siu, G.K.Y.; Young, M.L.C.; Chan, D.K.O. Environmental and nutritional factors which regulate population dynamics and toxin production in the dinoflagellate Alexandrium catenella. Hydrobiologia 1997, 352, 117–140. [Google Scholar] [CrossRef]
  36. Hwang, D.F.; Lu, Y.H. Influence of environmental and nutritional factors on growth, toxicity, and toxin profile of dinoflagellate Alexandrium minutum. Toxicon 2000, 38, 1491–1503. [Google Scholar] [CrossRef]
  37. Hamasaki, K.; Horie, M.; Tokimitsu, S.; Toda, T.; Taguchi, S. Variability in toxicity of the dinoflagellate Alexandrium tamarense isolated from Hiroshima Bay, western Japan, as, a reflection of changing environmental conditions. J. Plankton Res. 2001, 23, 271–278. [Google Scholar] [CrossRef]
  38. Etheridge, S.M.; Roesler, C.R. Effects of temperature, irradiance, and salinity on photosynthesis, growth rates, total toxicity, and toxin composition for Alexandrium fundyense isolates from the Gulf of Maine and Bay of Fundy. Deep-Sea Res. PT II 2005, 52, 2491–2500. [Google Scholar] [CrossRef]
  39. He, H.; Chen, F.; Li, H.; Xiang, W.; Li, Y.; Jiang, Y. Effect of iron on growth, biochemical composition and paralytic shellfish poisoning toxins production of Alexandrium tamarense. Harmful Algae 2010, 9, 98–104. [Google Scholar] [CrossRef]
  40. Xu, J.; Ho, A.Y.T.; He, L.; Yin, K.; Hung, C.; Choi, N.; Lam, P.K.S.; Wu, R.S.S.; Anderson, D.M.; Harrison, P.J. Effects of inorganic and organic nitrogen and phosphorus on the growth and toxicity of two Alexandrium species from Hong Kong. Harmful Algae 2012, 16, 89–97. [Google Scholar] [CrossRef]
  41. Han, M.S.; Lee, H.; Anderson, D.M.; Kim, B. Paralytic shellfish toxin production by the dinoflagellate Alexandrium pacificum (Chinhae Bau, Korea) in axenic, nutrient-limited chemostat cultures and nutrient-enriched bath cultures. Mar. Pollut. Bull. 2016, 104, 34–43. [Google Scholar] [CrossRef]
  42. Chang, D.D.; Shik, C.S.; Goo, H.Y.; Oh, E.G.; Pyun, J.H.; Park, Y.H. (Studies on distribution, characterization and detoxification of shellfish toxin in Korea. Bull. Korean Fish. Soc. 1988, 21, 297–302. [Google Scholar]
  43. Oshima, Y.; Hayakawa, T.; Hashimoto, M.; Kotaki, Y.; Yasumoto, T. Classification of Protogonyaulax tamarensis from northern Japan into three strains by toxin composition. Bull. Jpn. Soc. Sci. Fish. 1982, 48, 851–854. [Google Scholar] [CrossRef]
  44. Suzuki, T.; Ichimi, K.; Oshima, Y.; Kamiyama, T. Paralytic shellfish poisoning (PSP) toxin profiles and short-term detoxification kinetics in mussels Mytilus galloprovincialis fed with the toxic dinoflagellate Alexandrium tamarense. Harmful Algae 2003, 2, 201–206. [Google Scholar] [CrossRef]
  45. Sekiguchi, K.; Sato, S.; Ogata, T.; Kaga, S.; Kodama, M. Accumulation and depuration kinetics of paralytic shellfish toxins in the scallop Patinopecten yessoensis fed Alexandrium tamarense. Mar. Ecol. Prog. Ser. 2001, 220, 213–218. [Google Scholar] [CrossRef]
  46. Qiu, J.; Fan, H.; Liang, X.; Meng, F.; Quiliam, M.; Li, A. Application of activated carbon to accelerate detoxification of paralytic shellfish toxins from mussels Mytilus galloprovincialis and scallops Chlamys farreri. Ecotoxicol. Environ. Saf. 2018, 148, 402–409. [Google Scholar] [CrossRef]
  47. Bricelj, V.M.; Shumway, S.E. Paralytic shellfish toxins in bivalve molluscs: Occurrence, transfer kinetics, and biotransformation. Rev. Fish. Sci. 1998, 6, 315–383. [Google Scholar] [CrossRef]
  48. Guéguen, M.; Bardouil, M.; Baron, R.; Lassus, P.; Truquet, P.; Massardier, J.; Amzil, Z. Detoxification of Pacific oyster Crassostrea gigas fed on diets of Skeletonema costatum with and without silt, following PSP contamination by Alexandrium minutum. Aquat. Living Resour. 2008, 21, 13–20. [Google Scholar] [CrossRef]
  49. Gibbard, J.; Naubert, J. Paralytic shellfish poisoning on the Canadian Atlantic coast. Am. J. Public Health Nations Health 1948, 38, 550–553. [Google Scholar] [CrossRef] [PubMed]
  50. Jamieson, G.S.; Chandler, R.A. Paralytic shellfish poison in sea scallops (Placopecten magellanicus) in the west Atlantic. Can. J. Fish. Aquat. Sci. 1983, 40, 313–318. [Google Scholar] [CrossRef]
  51. Shumway, S.E.; Sherman-Caswell, S.; Hurst, J.W. Paralytic shellfish poisoning in Maine: Monitoring a monster. J. Shellfish Res. 1988, 7, 643–652. [Google Scholar]
  52. Maranda, L.; Anderson, D.M.; Shimizu, Y. Comparison of toxicity between populations of Gonyaulax tamarensis of eastern north American waters. Estuar. Coast. Shelf Sci. 1985, 21, 401–410. [Google Scholar] [CrossRef]
  53. Boyer, G.L.; Sullivan, J.J.; Anderson, R.J.; Harrison, P.J.; Taylor, F.J.R. Effects of nutrient limitation on toxin production and composition in the marine dinoflagellate Protogonyaulax tamarensis. Mar. Biol. 1987, 96, 123–128. [Google Scholar] [CrossRef]
  54. Cembella, A.E.; Sullivan, J.J.; Boyer, G.L.; Taylor, F.J.R.; Anderson, R.J. Variation in paralytic shellfish toxin composition within the Protogonyaulax tamarensis/catenella species complex: Red tide dinoflagellates. Biochem. Syst. Ecol. 1987, 15, 171–186. [Google Scholar] [CrossRef]
  55. Anderson, D.M. Toxin variability in Alexandrium species. In Toxic Marine Phytoplankton; Graneli, E., Sundstrom, B., Edler, L., Anderson, D.M., Eds.; Elsevier: Amsterdam, The Netherlands, 1990; pp. 41–51. [Google Scholar]
  56. Ishida, Y.; Kim, C.-H.; Sako, Y.; Hirooka, N.; Uchida, A. PSP toxin production is chromosome dependent in Alexandrium spp. In Toxic Phytoplankton Blooms in the Sea; Smayda, T.J., Shimizu, Y., Eds.; Elsevier: Amsterdam, The Netherlands, 1993; pp. 881–887. [Google Scholar]
  57. Kim, C.-H.; Sako, Y.; Ichida, Y. Comparison of toxic composition between populations of Alexandrium spp. from geographically distant areas. Nippon Suisan Gakk. 1993, 59, 641–646. [Google Scholar] [CrossRef]
  58. Oshima, Y.; Blackburn, S.I.; Hallegraeff, G.M. Comparative study on paralytic shellfish toxin profiles of the dinoflagellate Gymnodinium catenatum from three different countries. Mar. Biol. 1993, 116, 471–476. [Google Scholar] [CrossRef]
  59. Cho, E.S.; Lee, H.J. Thecal plates, toxin content and growth of five clones of Alexandrium tamarense (Dinophyceae) isolated from Jinhae Bay. Korea. Phycologia 2001, 40, 435–439. [Google Scholar] [CrossRef]
  60. Kim, C.J.; Kim, C.H.; Sako, Y. Paralytic shellfish poisoning toxin analysis of the genus Alexandrium (Dinophyceae) occurring in Korean coastal waters. Fish. Sci. 2005, 71, 1–11. [Google Scholar] [CrossRef]
  61. Oshima, Y.; Fallon, W.E.; Shimizu, Y.; Noguchi, T.; Hashimoto, Y. Toxins of the Gonyaulax sp. and infested bivalves on Owase bay. Bull. Jpn. Soc. Sci. Fish. 1976, 42, 851–856. [Google Scholar] [CrossRef]
  62. Oshima, Y.; Sugino, K.; Itakura, H.; Hirota, M.; Yasumoto, T. Comparative studies on paralytic shellfish toxin profile of dinoflagellate and bivalves. In Toxic Marine Phytoplankton; Graneli, E., Sundstorm, B., Edler, L., Anderson, D.M., Eds.; Academic Press: New York, NY, USA, 1990; pp. 391–396. [Google Scholar]
  63. Krock, B.; Seguel, C.G.; Cembella, A.D. Toxin profile of Alexandrium catenella from the Chilean coast as determined by liquid chromatography with fluorescence detection and liquid chromatography coupled with tandem mass spectrometry. Harmful Algae 2007, 6, 734–744. [Google Scholar] [CrossRef]
  64. Shimizu, Y.; Yoshioka, M. Transformation of paralytic shellfish toxins as demonstrated in scallop homogenates. Science 1981, 212, 547–549. [Google Scholar] [CrossRef] [PubMed]
  65. Cembella, A.; Shumway, S.E.; Lewis, N. A comparison of anatomical distribution and spatio-temporal variation of paralytic shellfish toxin composition in two bivalve species from the Gulf of Maine. J. Shellfish Res. 1993, 12, 389–403. [Google Scholar]
  66. Oshima, Y. Chemical and enzymatic transformation of paralytic shellfish toxins in marine organisms. In Harmful Marine Algal Blooms; Lassus, P., Arzul, G., Erard-Le Denn, E., Gentien, P., Marcaillou-Le Baut, C., Eds.; Lavoisier Science Publishers: Paris, France, 1995; pp. 475–480. [Google Scholar]
  67. Sullivan, J.J.; Iwaoka, W.T.; Liston, J. Enzymatic transformation of PSP toxins in the littleneck clam (Protothaca staminea). Biochem. Biophys. Res. Commun. 1983, 114, 465–472. [Google Scholar] [CrossRef] [PubMed]
Water 16 01985 g001
Figure 1. Schematic of the experimental design for continuous exposure of Alexandrium catenella (Group I) and A. pacificum (Group IV) to Mytilus edulis. A. catenella at cell densities of 10, 100 and 1000 cells/mL and A. pacificum at cell densities of 10 and 100 cells/mL were constantly exposed to the experimental tank containing M. edulis under 15 ± 1 °C, 30 psu, and 100 μmoL/m2/s. The exposure solution contained the dinoflagellates. Exposure solution was 10 L, and the experimental tank was 20 L.
Figure 1. Schematic of the experimental design for continuous exposure of Alexandrium catenella (Group I) and A. pacificum (Group IV) to Mytilus edulis. A. catenella at cell densities of 10, 100 and 1000 cells/mL and A. pacificum at cell densities of 10 and 100 cells/mL were constantly exposed to the experimental tank containing M. edulis under 15 ± 1 °C, 30 psu, and 100 μmoL/m2/s. The exposure solution contained the dinoflagellates. Exposure solution was 10 L, and the experimental tank was 20 L.
Water 16 01985 g001
Water 16 01985 g002
Figure 2. Changes in toxin content and toxicity of Mytilus edulis exposed to Alexandrium catenella (Group I) at a cell density of 10 (a), 100 (b), and 1000 cells/mL (c).
Figure 2. Changes in toxin content and toxicity of Mytilus edulis exposed to Alexandrium catenella (Group I) at a cell density of 10 (a), 100 (b), and 1000 cells/mL (c).
Water 16 01985 g002
Water 16 01985 g003
Figure 3. Changes in toxin content and toxicity of Mytilus edulis exposed to Alexandrium pacificum (Group IV) continuously exposed at a cell density of 10 (a) and 100 cells/mL (b).
Figure 3. Changes in toxin content and toxicity of Mytilus edulis exposed to Alexandrium pacificum (Group IV) continuously exposed at a cell density of 10 (a) and 100 cells/mL (b).
Water 16 01985 g003
Water 16 01985 g004
Figure 4. The comparison of the toxin content and toxicity of Mytilus edulis after a one-time exposure to Alexandrium catenella (Group I) (a) and A. pacificum (Group IV) (b).
Figure 4. The comparison of the toxin content and toxicity of Mytilus edulis after a one-time exposure to Alexandrium catenella (Group I) (a) and A. pacificum (Group IV) (b).
Water 16 01985 g004
Water 16 01985 g005
Figure 5. Changes in the toxic compositions of Mytilus edulis exposed to Alexandrium catenella (Group I) at a cell density of 10 (a), 100 (b), and 1000 cells/mL (c).
Figure 5. Changes in the toxic compositions of Mytilus edulis exposed to Alexandrium catenella (Group I) at a cell density of 10 (a), 100 (b), and 1000 cells/mL (c).
Water 16 01985 g005
Water 16 01985 g006
Figure 6. Changes in the toxic compositions of Mytilus edulis when continuously exposed to Alexandrium pacificum (Group IV) at a cell density of 10 (a) and 100 cells/mL (b).
Figure 6. Changes in the toxic compositions of Mytilus edulis when continuously exposed to Alexandrium pacificum (Group IV) at a cell density of 10 (a) and 100 cells/mL (b).
Water 16 01985 g006
Table 1. Toxic contents detected in Alexandrium catenella (Group I) and A. pacificum (Group IV) in this study.
Table 1. Toxic contents detected in Alexandrium catenella (Group I) and A. pacificum (Group IV) in this study.
ToxinA. catenella
(fmol/Cells)		A. pacificum
(fmol/Cells)
C1+237.91 ± 5.17 *9.73 ± 1.13
GTX 1+410.96 ± 0.30-
GTX 2+30.16 ± 0.02-
GTX 50.72 ± 0.0710.67 ± 0.26
neo STX17.49 ± 1.461.49 ± 0.21
Total67.24 ± 6.8321.89 ± 0.61
Note: * Mean and standard deviation were calculated from cellular toxic cotents in the late exponential phase after 2 times repeatedly incubating to each same strain.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Oh, S.J.; Jeong, S.Y.; Son, M. Alexandrium catenella (Group I) Causes Higher and Faster Toxicity Than A. pacificum (Group IV) in Mytilus eduis. Water 2024, 16, 1985. https://doi.org/10.3390/w16141985

AMA Style

Oh SJ, Jeong SY, Son M. Alexandrium catenella (Group I) Causes Higher and Faster Toxicity Than A. pacificum (Group IV) in Mytilus eduis. Water. 2024; 16(14):1985. https://doi.org/10.3390/w16141985

Chicago/Turabian Style

Oh, Seok Jin, Soo Yong Jeong, and Moonho Son. 2024. "Alexandrium catenella (Group I) Causes Higher and Faster Toxicity Than A. pacificum (Group IV) in Mytilus eduis" Water 16, no. 14: 1985. https://doi.org/10.3390/w16141985

APA Style

Oh, S. J., Jeong, S. Y., & Son, M. (2024). Alexandrium catenella (Group I) Causes Higher and Faster Toxicity Than A. pacificum (Group IV) in Mytilus eduis. Water, 16(14), 1985. https://doi.org/10.3390/w16141985

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop