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EARLY ONLINE RELEASE Posted October 26, 2018

CITATION Krock, B., M.E. Ferrario, R. Akselman, and N.G. Montoya. 2018. Occurrence of marine bio- toxins and shellfish poisoning events and their causative organisms in Argentine marine waters. Oceanography 31(4), https://doi.org/10.5670/oceanog.2018.403.

DOI https://doi.org/10.5670/oceanog.2018.403

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Occurrence of MARINE BIOTOXINS AND SHELLFISH POISONING EVENTS and Their Causative Organisms in Argentine Marine Waters

By Bernd Krock, Martha E. Ferrario, Rut Akselman, and Nora G. Montoya

Micrographs courtesy of Urban Tillmann, AWI; Background NOAA photo courtesy of Vera Trainer

Oceanography48 Oceanography | Vol.31, | NoVol.4.31, | NoEarly.4 Online Release ABSTRACT. In the Argentine , marine phycotoxins of microalgal origin associated Santinelli et al., 1994a, 2002; Cadaillón, with five shellfish poisoning syndromes have been reported. The most problematic in 2012; Sunesen et al., 2014; Krock et al., terms of toxicity and geographic distribution is paralytic shellfish poisoning (PSP), fol- 2015a), lowed by diarrhetic shellfish poisoning (DSP). In contrast, amnesic shellfish poisoning 3. Spiroimine shellfish poisoning (SSP) (ASP), spiroimine shellfish poisoning (SSP), and azaspiracid shellfish poisoning (AZP) (Almandoz et al., 2014; Fabro et al., have not been reported to cause human illness or closures of shellfish harvest sites in 2017), to date but pose a potential risk, as associated toxins and producing organ- 4. Diarrhetic shellfish poisoning (DSP; isms are present in Southwest Atlantic waters and were detected at subregulatory lev- Gayoso et al., 2002; Sar et al., 2010, els in mollusks. Alexandrium catenella and Gymnodinium catenatum have been iden- 2012; Montoya et al., 2011; Sunesen tified as producers of the PSP toxins C1/2, gonyautoxins (GTX1-4), saxitoxin (STX), et al., 2014; Gracia Villalobos et al., and neosaxitoxin (NEO) in the Argentine Sea. Nine potentially toxigenic species of 2015; Krock et al., 2015a; Turner and the diatom genus Pseudo-nitzschia have been reported for Argentinean coastal waters: Goya, 2015; Akselman et al., 2015; P. australis, P. brasiliana, P. delicatissima, P. fraudulenta, P. multiseries, P. pseudodelica- Fabro et al., 2015, 2016), and tissima, P. pungens, P. seriata, and P. turgidula, all of which are known to produce the 5. Azaspiracid shellfish poisoning (AZP; neurotoxin domoic acid that causes ASP. Two genera have been identified as produc- Turner and Goya, 2015; Tillmann ers of DSP toxins in Argentina: the benthic dinoflagellate Prorocentrum lima and sev- et al., 2016). eral species of the pelagic dinoflagellate genus Dinophysis: D. acuminata, D. caudata, D. fortii, D. norvegica, and D. tripos. The occurrence of these species in Argentine waters This review compiles the recent is associated with okadaic acid (OA), dinophysistoxin-1 (DTX-1), pectenotoxin-2 knowledge on the occurrence of toxi- (PTX-2), and pectenotoxin-2 seco acid (PTX-2sa). Historically, yessotoxins (YTXs) genic microalgae and their phycotoxins were also included in DSP syndrome and all three known YTX-producers have been in this . confirmed in Argentinean waters: Gonyaulax spinifera, Lingulodinium polyedra, and Protoceratium reticulatum, but of these only P. reticulatum could be associated with YTX PARALYTIC SHELLFISH production to date. Several species of the family Amphidomataceae, which cause AZP, POISONING (PSP) have been reported for Argentina: Amphidoma languida, Azadinium dexteroporum, PSP toxins are among the most toxic Az. luciferelloides, Az. poporum, and Az. spinosum. In Argentinean coastal waters, out marine biotoxins. In addition to causing of these species only Az. poporum has been identified as toxigenic to date, as it produces muscular paralysis, they have been respon- azaspiracid-2 (AZA-2) and its phosphorylated form. Currently in Argentina, seafood is sible for hundreds of human fatalities monitored for the risk of ASP, AZP, DSP, and PSP. (Hallegraeff, 1995). Comprising a group of hydrated purine derivatives, variations INTRODUCTION organisms, among which shellfish are the consist of hydroxylation at N1, sulpha- Toxic marine microalgae are usually most relevant for humans. tation at C11, and various substitutions at responsible for human shellfish poisoning Shellfish poisoning events are catego- C13, which can be hydroxylation (decar- events. They produce secondary metabo- rized according to the symptoms they bamoyl toxins), carbamoylation (car- lites that may be taken up and concen- induce in humans. Although not all bamoyl toxins), N-sulfocarbamoylation trated to high levels by filter-feeding mol- types of shellfish poisoning syndromes (N-sulfocarbamoyl toxins), benzoylation lusks and cause severe illnesses or even have been reported to date in Argentine (benzoyl toxins), and all combinations death in vertebrates (including humans) waters, several toxigenic microalgal spe- of these substitutions (Figure 1a). Due to after consumption of contaminated shell- cies and their toxins have been identi- two guanidine moieties in the molecule, fish. Interestingly, these marine bio- fied in this region during the last four PSP toxins are charged and thus highly toxins usually trigger no or few adverse decades. They cause five different shell- hydrophilic in contrast to most other effects in primary consumers of toxic fish poisoning syndromes: phycotoxins. The positive charges and microalgae, such as crustaceans and mol- 1. Amnesic shellfish poisoning (ASP; the structural configuration of PSP tox- lusks. The low toxic effect of marine bio- Montoya et al., 2000, 2008; R.M. ins enable them to efficiently bind to and toxins on their direct predators seems to Negri et al., 2004; Sastre et al., 2007; block voltage-dependent ion channels argue against the function of marine bio- Cadaillón, 2012; Krock et al., 2015a; in neuronal cells, which inhibits sodium toxins as a defense mechanism against Almandoz et al., 2017), influx into excited cells and thus inhibits predation. In fact, the ecological function 2. Paralytic shellfish poisoning (PSP; signal relaxation (Hall et al., 1987). of marine biotoxins is still unknown. We Carreto et al., 1981, 1986, 1998, 2007; The intraperitoneal toxicity of saxi- do know that the phycotoxins produced Esteves et al., 1992; Benavides et al., toxin (the most potent of the PSP toxins) –1 by microalgae are easily accumulated and 1995; Akselman et al., 1998; Gayoso, in mice (LD50) is 8 µg kg body weight concentrated by filter-feeding marine 2001; Montoya et al., 2006, 2018; (Baden et al., 1995). However, toxicity of

Oceanography | December 2018 | https://doi.org/10.5670/oceanog.2018.403 individual variants can differ over more For this reason, monitoring of biotoxins recommended by the European Union than two orders of magnitude, depend- in mollusks is important in the regulation Toxicology Working Group (WG; FAO, ing on the net charge of the toxins and of seafood (Etheridge, 2010). 2006). To comply with European regula- their structural configuration. In con- Unpredictable toxic blooms often tions and to ensure consumer protection, trast to many other marine biotoxins, affect both commercial harvest areas monitoring of toxic phytoplankton in the which show a lower oral than intraperi- and aquaculture facilities. In addition water and PSP toxins in shellfish is a stat- toneal toxicity, both routes of applica- to seafood regulation and monitoring utory requirement for EU member states tion are efficient for PSP toxins, and thus of shellfish for biotoxins, in many cases and for others desiring to export shell- PSP toxinsA are considered a high risk for phytoplanktonB monitoring has been fish products to countries within the EU shellfish consumers (Hallegraeff, 1995). established as a preventive measure, as (Anonymous, 2004a).

O 31 Sanitary standards for the export of O 35 34

2 live bivalve mollusks from Argentina are 3 N based on Regulation (EC) No. 853/2004 regarding the regulated toxins and their OH A B O respective legislated limits. The con- b O trol system and monitoring of toxins in 13 O O 31 A B O HO A 35 34 B Argentina was initiated in 1980, after 2 a 3 N lethal poisonings of two fishermen caused O 31 O 35 34 O 31 O 35 34 by consumption of PSP-contaminated 2 3 N 2 OH 3 musselsN off Valdés Peninsula. The O O National Service for Health and Agro- OH 13 O Food Quality (SENASA) is responsi- O HO OH O O bleO for classification and monitoring 13 O HO 1of3 shellfishO harvest areas and for deci- 8' HO

D cC 7 6 1' sions regarding closures of these areas O OH HOOC O O HO (Resolution SAGPyA 829/06). SENASA O O O 3 4 OH 5' 7' OH O O 8 2 5 COOH coordinates this work with provincial OH HOOC N H 6' and regional governments. Each region

O has a Prevention and Control Plan that O O B C 14 8' E 1 7 A O includes, in addition to the monitoring O D O C 7 1' 34 OH 6 O OH HOOC 33 of toxic species, the control of toxins in OH O O OO 43 OH HOF O 8' O O D O 3 4 OH bivalve8' mollusks. Species of commercial O E 5' 7' D O O C 7 1' OH 6 2 5 OH 8 COOH O D GHOOC C 7 1' OH HOOC 6 O d O OH O O N HOOC interest in Argentina are common mus- HO HO O O 6' O O O 3 4 H OH HO 7' Me O O 5' 3 sels4 (Mytilus edulis platensis), mussels O O O O O OH OH H 8 2 5 O COOH 5' 7' O O O H O H O O OH OH HOOC 8 2 5 B O COOH C 14 OH N (Aulacomya ater), clams (Ameghinomya E 1 7 OH HOOC A O H H 6' N O H O H H 6' 34 OH OH antiqua), geoduck (Panopea abbrevi- O O H O 3O3 H OOH B O O 43 HO C 14 O O eE OH1 F 7 O O B Me NH ata), oysters (Ostrea puelchana), scallops A O D C 14 E O E 1 H 7 H O O O A O OH OH O H F34 O H G O (Aequipecten tehuelchus, Zygochlamys 3O3 34 OH OH O O H 43 O O O OH F O 33 HO OH O 43 D H O H O patagonica), razor clams (Ensis macha, OH F O H O E Me O H Me D O Me H H H H H E - O G O O SO O O O H O H Solen tehuelchus), and gastropods (Zidona O 3 g O OH G O HO O Me H HO H dufresnei, Adelomelon beckii). The local - Me Me O O3SO O O H O OH H H H H H H Me O O H O O O H H H H O HO legislationO establishes a maximum level O OH H O H O Me NH H O OH –1 H H H O OH H of <800 μg STXeq kg per edible part, H OHH H H O O F H O H H OH H O O HO O H O O and thisH limit is tested weekly in the areas O Me H O H NH HO H O Me H H O NH H OH Me that are classified as extraction and pro- Me H H H H H H H O - O H OH O F O3SO O O H O F H O H O O duction areas (Figure 2) using the mouse f O Me O O H O H H O - Me O H O3SO O H O Me H H Me H H H H H H H H H Hbioassay (MBA; AOAC method 959.08; - O H Me O3SO O O Me H H H H - O O3SO O O O Me AOAC, 2005). When PSP exceeds the - Me O Me O3SO O O H H H H H -O SO O O Me maximum permitted limit (MPL), the 3 H H H H H corresponding area is closed for shell- FIGURE 1. (a) Chemical structures of PSP toxins, (b) 13-desmethyl spirolide C (SPX-1), (c) domoic acid (DA), (d) okadaic acid (OA), (e) pectenotoxin-2 (PTX-2), (f) yessotoxin (YTX), fish harvest until shellfish toxicities are and (g) azaspiracid-1 (AZA-1). assessed as safe again.

Oceanography | Vol.31, No.4 | Early Online Release et al., 2014). However, several toxic spe- some cases have led to fish, bird, and cies of Alexandrium have been docu- whale mortalities and even human deaths mented in the Southwest Atlantic for (Elbusto et al., 1981; Carreto et al., 1981, 35˚S 35˚S many decades (Balech, 1995; Carreto 1986; Vecchio et al., 1986; Andrinolo et al., Province of Province of Buenos Aires et al., 1981, 1998; Benavides et al., 1995; Buenos1999; Aires Benavides et al., 1995; Montoya Sastre et al., 1997; Santinelli et al., 2002; et al., 1996, 1998, 2018; Uhart et al., 2004; El Rincón El Rincón 40˚S Akselman et al.,40˚S 2008). Montoya and Carreto, 2007; Wilson et al., The dominant PSP-producing spe- 2015). Toxin profiles of several isolates San Matías Gulf San Matías Gulf San José Gulf cies in the Argentine Sea is Alexandrium Sanof JoséArgentinean Gulf A. catenella have been Nuevo Gulf catenella, initially described as Gony- Nuevoanalyzed Gulf and found to be mostly domi- Chubut Chubut 45˚S aulax excavata45˚S, later re-identified as nated by the N-sulfocarbamoyl variants San Jorge Gulf Alexandrium tamarense, and very recentlySan Jorge GulfC1/C2 and gonyautoxins GTX1/GTX4. recognized as Alexandrium catenella fol- GTX2/GTX3; the carbamoyl variants lowing ribosomal phylogenetic stud- saxitoxin (STX) and neosaxitoxin (NEO) 50˚S Santa 50˚S Santa Cruz ies (John et al., 2014; Prud’hommeCruz van were minor components of these pro- Reine, 2017). Blooms of A. catenella files (Carreto et al., 1996, 2001; Montoya have been detected frequently since et al., 2010; Krock et al., 2015a). Toxin Tierra Beagle Channel Tierra Beagle Channel del Fuego del Fuego 55˚S 1980 and were55˚S recorded in a latitudinal profiles of A. aff. minutum to date have

Ocean Data View gradient from the Province of Buenos not Oceanbeen Data View analyzed. There is one report 75˚W 70˚W 65˚W 60˚W Aires to the Beagle75˚W Channel70˚W in almost65˚W of60˚W toxin profiles in a G. catenatum bloom FIGURE 2. Map of the study area in Argentina. the entire coastal ecosystem (Figure 3; near (Province of Buenos Red triangles indicate classified shellfish har- vesting areas. Carreto et al., 1981; Esteves et al., 1992; Aires, 38°S) consisting of 82% decar- Benavides et al., 1995; Akselman, 1996; bamoyl toxins C1/C2 (Montoya et al., Carreto et al., 1998; Gayoso and Fulco, 2006). All other detected toxins (GTX2/3, Three dinoflagellate genera are known 2006; Montoya et al., 2010; Krock et al., GTX4 and decarbamoyl GTX2/3) were to produce PSP toxins in the marine envi- 2015a; Fabro et al., 2017; Montoya et al., ronment: (1) Alexandrium, which has 2018). Such blooms have been recorded a broad geographical distribution from annually through spring and summer polar35˚S to subtropical waters worldwide seasons from South35˚S all the way (Anderson et al., 2012); (2)Province Pyrodinium of up to (Carreto et al., 1998, 2007; Province of Buenos35˚S Aires Buenos35˚S Aires bahamense, which is constrained to trop- Méndez et al.,Province 2001). of Province of Buenos Aires Buenos Aires ical waters (Harada et al., 1982;El RincónUsup and Another potentially PSP-producing El Rincón 40˚S 40˚S Azanza, 1998); and (3) Gymnodinium Alexandrium species is Alexandrium San Matías Gulf El Rincón San Matías Gulf El Rincón 40˚S 40˚S catenatum, which ranges fromSan tropical José Gulf to ostenfeldii, which has been reported to be San José Gulf warm-temperate environmentsNuevo (Trainer Gulf a PSP producerSan Matías in some Gulf coastal and estua- Nuevo Gulf San Matías Gulf Chubut San José Gulf Chubut San José Gulf 45˚Set al., 2010). There is an early report of a rine (Kremp45˚S et al., 2014). Though Nuevo Gulf Nuevo Gulf toxic shellfish event inSan JorgeBelgium Gulf caused by thisChubut species was also observed inSan the Jorge Gulf Chubut Pyrodinium phoneus (Wołoszyńska45˚S and Beagle Channel, it was found not to pro- 45˚S San Jorge Gulf San Jorge Gulf Conrad, 1939), which was later inferred duce PSP there (Almandoz et al., 2014). to50˚S be AlexandriumSanta ostenfeldii (Balech, Very recently, 50˚Showever, SantaA. ostenfeldii Cruz Cruz 1995). Among the PSP-producing marine was associated with PSP toxins detected 50˚S Santa 50˚S Santa dinoflagellates, G. catenatum is distinc- Cruzin San Matías and San Jorge Gulfs and Cruz Tierra Beagle Channel Tierra Beagle Channel tive because delin Fueg additiono to the classical in shelf waters close to Valdésdel Fueg Peninsulao 55˚S 55˚S PSP toxins it also produces a large variety Tierra(42°–43°S; BeagleFabro Channel et al., 2017). During Tierra Beagle Channel Data View del Fuego Ocean Data View del Fuego of benzoyl75˚W variants,70˚W so-called65˚W 55˚SGC-toxins60˚W the same survey, Alexandrium75˚W 70˚W aff. minu65˚W- 55˚S60˚W (A.P. Negri et al., 2007). tum was detected inOcean shelf Data View waters south of Ocean Data View 75˚W 70˚W 65˚W 60˚W 75˚W 70˚W 65˚W 60˚W Gymnodinium catenatum, the first PSP- the Province of Buenos Aires and east of FIGURE 3. Red dots indicate the geographic producing species recorded in Argentina Valdés Peninsula (40°–44°S; Fabro et al., location of records of the occurrence of par- (Balech, 1964), has only been found 2017). Pyrodinium bahamense has not alytic shellfish poisoning (PSP) events and/ during the autumn in northern coastal been found to occur in the Argentine Sea. or potentially PSP-producing species in the Argentine Sea. Blue dots indicate geographic waters off Buenos Aires (Akselman et al., Several Argentinean PSP events have locations of records of the occurrence of 1998; Montoya et al., 2006; Sunesen been documented since 1980 that in A. ostenfeldii and SPX.

Oceanography | December 2018 | https://doi.org/10.5670/oceanog.2018.403

35˚S 35˚S

Province of Province of Buenos Aires Buenos Aires

El Rincón El Rincón 40˚S 40˚S

San Matías Gulf San Matías Gulf San José Gulf San José Gulf Nuevo Gulf Nuevo Gulf Chubut Chubut 45˚S 45˚S San Jorge Gulf San Jorge Gulf

50˚S Santa 50˚S Santa Cruz Cruz

Tierra Beagle Channel Tierra Beagle Channel del Fuego del Fuego 55˚S 55˚S

Ocean Data View Ocean Data View 75˚W 70˚W 65˚W 60˚W 75˚W 70˚W 65˚W 60˚W minor components of the toxin profile, mice was determined as 40 µg kg–1 body (Seki et al., 1995). below 10% each. The field samples were weight, whereas oral toxicity was found In Argentina, information on spe- also tested for some benzoyl GC toxins to be one and a half orders of magnitude cies producing spiroimine toxins is very (GC1-3) with negative results (Montoya higher (1 mg kg–1; Munday et al., 2012). scarce. Toxic strains of A. ostenfeldii iso- et al., 2006). As GC toxin variability It is important to note that there is no lated from the Beagle Channel (55°S) meanwhile has been proven to be much evidence of harmful effects in humans were proven to produce 20-methyl spiro- higher than the three tested variants, it caused by cyclic imines, as there is for lide G, 13-desmethyl spirolide C (SPX-1), cannot entirely be ruled out that G. cat- other marine biotoxins, and that the toxic and two more yet uncharacterized SPX enatum populations in the Argentine potential of cyclic imines by oral admin- (Almandoz et al., 2014). Nevertheless, Sea also produce benzoyl GC toxins, istration is significantly lower than after SPX-1 has been detected in very low con- as reported for most other parts of the intraperitoneal administration. The sig- centrations in shellfish harvested along world. But it is noteworthy that even- nificance of these toxins to food safety the entire Argentine coast in all provinces tually in planktonic field populations is unclear. The report by the European from Buenos Aires (36°S) to Tierra del of the Argentine Sea, PSP profiles other Union Toxicology WG (FAO, 2006) pro- Fuego (55°S) (Turner and Goya, 2015), than those of the well-​characterized vides evidence that spirolides could be suggesting widespread distribution of Argentinean A. catenella isolates were toxic to humans and that further stud- this dinoflagellate (Figure 3). Recently, detected (Montoya et al., 2010; Fabro ies are required. Based on the current A. ostenfeldii has been reported in coastal et al., 2017). This finding indicates that lack of historical information from reg- and open shelf waters of the Argentine either PSP-producing species other than ulatory programs regarding human ill- Sea associated with SPX-1 and 20-Methyl A. catenella are present or that other ness and the risk assessment provided spirolide G (Fabro et al., 2017), interest- A. catenella strains exhibit different by the Expert Consultation, the WG rec- ingly, the same SPX variants produced toxin profiles. Certainly, more research ommends not setting limitations for any by the isolates from the Beagle Channel is needed to fully assess and understand of the cyclic imine toxins in the Codex (Almandoz et al., 2014). Even though the presence of PSP-producing species in Standard at this time (EFSA, 2010). In GYM are widely distributed globally, to Argentinean waters. Argentina, SPX and GYM are not yet date there are no records of GYM in the included in the list of regulated toxins. Southwest Atlantic. SPIROIMINE SHELLFISH Benthic or epiphytic members of POISONING (SSP) the dinoflagellate genus Prorocentrum AMNESIC SHELLFISH POISONING Cyclic imines comprise a large group produce prorocentrolides and spiro-​ (ASP) of toxin classes consisting of spirolides prorocentrimine (Torigoe et al., 1988; Lu ASP is caused by the rare amino acid (SPX), gymnodimines (GYM), pinna- et al., 2001). Pinnatoxins and pteriatoxins domoic acid (DA). DA is structurally sim- toxins, pteriatoxins, prorocentrolides, initially were found in the bivalve shellfish ilar to glutamic acid (Figure 1c) and thus and spiro-prorocentrimines. Spiroimines, Pinna muricata (Uemura et al., 1995) and acts as a glutamic acid agonist that binds to like most lipophilic marine biotoxins, Pteria penguin (Takada et al., 2001), but glutamic acid receptors in the brain. This are polyketides; they have a macrocycle it was later proven that both toxin groups causes neuronal firing due to the inabil- as well as a six-membered cycloimine were shellfish metabolites of pinna- ity of glutamate transporters to clear DA moiety (Cembella and Krock, 2008). toxins produced by the dinoflagellate from the synaptic cleft, thus prolonging GYM are structurally very similar to SPX Vulcanodinium rugosum (Rhodes et al., neuronal excitation. Neurotoxicity com- (Figure 1b), but with an average molec- 2011). SPX are produced by Alexandrium prises neurobehavioral effects and loss ular weight of 500 Da they are approxi- ostenfeldii (Cembella and Krock, 2008), of short-term memory (Pulido, 2008). mately 200 Da smaller than SPX. GYM which to date is the only species known The toxicity of DA in mice was assessed –1 and SPX are thus collectively related to to produce this toxin class. Alexandrium as 2.4 mg kg body weight (LD50; Jeffrey SSP, based on their blocking of muscarinic peruvianum, which has been reported et al., 2004). According to EU Regulation acetylcholin receptors, which negatively as a spiroimine-producing dinoflagellate 854/2004/EC (Anonymous, 2004b), shell- affects neuromuscular, sensory, diges- (Van Wagoner et al., 2011), is currently fish production areas are periodically tive, and respiratory systems (Gill et al., assumed to be conspecific with A. osten- monitored to detect the presence of toxin-​ 2003; Cembella and Krock, 2008; Guéret feldii (Kremp et al., 2014). To complicate producing plankton and the occurrence and Brimble, 2010). Spiroimines are also the scenario even more, A. ostenfeldii has of their toxins in live bivalve mollusks. known as “fast-acting toxins” because of recently been reported to also be a pro- Because many regional regulatory agen- instantaneous reaction in rodents after ducer of GYM (Van Wagoner et al., 2011), cies have implemented effective seafood injection (Wright and Cembella, 1998). which until then only had been reported monitoring programs for the detection of Their intraperitoneal toxicity (LD50) in from some species of the genus Karenia DA in shellfish and coastal waters, human

Oceanography | Vol.31, No.4 | Early Online Release ASP events have not been documented the shape of this species is strongly sim- reported (Lange, 1985) and proven to be since DA was first detected in 2000. The ilar to P. australis, and its distribution is distributed along the entire Argentinean MPL for DA in mollusks has been set at restricted to the , it coastline from 35°S to 54°S (R.M. Negri 20 mg kg–1. The analysis method used in is highly probable that these determina- and Inza, 1998; Ferrario et al., 2002, 2017; Argentina, based on high-performance tions could be wrong. Almandoz et al., 2007, 2008, 2011, 2017; liquid chromatography with UV detec- More recent analyses of P. seriata Sastre et al., 2007; Cadaillón, 2012). tion, is performed once per month in (Almandoz et al., 2008) performed with Detection of the Pseudo-nitzschia pseu- classified areas (Figure 2). SEM were not sufficient to discriminate dodelicatissima complex in the Southwest Although DA was reported in 1958 between P. seriata and P. australis, indi- Atlantic dates back to 1998 (R.M. Negri (Takemoto and Daigo, 1958) and repeat- cating the need for additional studies with and Inza, 1998); however, for unambigu- edly afterward (Maeda et al., 1986; transmission electron microscopy and ous species identification of this complex, Zaman et al., 1997) as an insecticidal molecular analysis. The next species to be SEM and in some cases molecular analysis compound produced by the red alga reported was Pseudo-nitzschia australis are required, which were not available for Chondria armata in Japan, the first ASP in the San Matías Gulf (41°S; Frenguelli, most Argentinean reports. Therefore, most outbreak in humans did not occur until 1939), which later turned out also to records need confirmation. Nonetheless, 1987, in Prince Edward Island, Canada be present in the entire Argentine Sea the reports indicate a distribution along (Wright et al., 1989). Very shortly after, (Hasle, 1965; Lange, 1985) as P. pseudo- the entire Argentine Sea (Sastre et al., the pennate marine diatom Pseudo- seriata (Ferrario and Galván, 1989; Sastre 1997, 2001; Ferrario et al., 1989; Santinelli nitzschia multiseries was identified as the et al., 1997, 2001; R.M. Negri and Inza, et al., 2002; Almandoz et al., 2008, 2011 DA source of the Prince Edward Island 1998; Sar et al., 1998; Ferrario et al., [as P. calliantha]; Cadaillón, 2012 [as ASP incident (Bates et al., 1989). In the 1999, 2002, 2017; Montoya et al., 2000; P. calliantha]; Almandoz et al., 2017; following years, several other species of Santinelli et al., 2002; R.M. Negri et al., Ferrario et al., 2017). Pseudo-nitzschia the genus Pseudo-nitzschia were reported 2004; Almandoz et al., 2007, 2011, 2017; turgidula was also reported in 1998 from to be DA producers (Kotaki, 2008). Cadaillón, 2012; Krock et al., 2015a). the northern Argentine Sea (35°–39°S; Despite the relatively recent appearance In 1965, Pseudo-nitzschia multiseries R.M. Negri and Inza, 1998), and there are of ASP, the toxigenic Pseudo-nitzschia (as Nitzschia pungens fa. multiseries) and later records from the south (49°–52°S) species and species complexes were Pseudo-nitzschia pungens were simulta- (Almandoz et al., 2007, 2017). Finally, known to occur in Argentinean waters neously reported from Puerto Quequén only one very recent report of Pseudo- as far back to the 1930s. To date, nine (38°S, Province of Buenos Aires). In con- nitzschia brasiliana from the northern potentially toxigenic Pseudo-nitzschia trast to the previous species discussed, zone of the Argentine shelf (~39°–40°S) species and species complexes have been P. multiseries seems to be a more temper- was associated with the presence of low reported in Argentinean waters. The first ate species that has only been reported in concentrations of DA (Almandoz et al., species reported was Pseudo-nitzschia northern regions, from the Province of 2017; Figure 4). seriata (a species without accurate deter- Buenos Aires (37°S) to Nuevo Gulf (42°S, The fact that Argentina has never suf- mination up to now for the Argentine Sea Province of Chubut) (Sastre et al., 1997, fered from human ASP outbreaks is and initially named Nitzschia seriata), 2001; Ferrario et al., 1999, 2002; Montoya probably due to the extensive expertise in the southern Southwest Atlantic et al., 2000; Santinelli et al., 2002; Carreto in phytoplankton taxonomy and knowl- between 56°S and 59°S in 1937 (Hendey, et al., 2004). Distribution along the entire edge of the distribution of potentially 1937). In succeeding years, the occur- Argentine coast has been reported for toxic species in this country. When the rence of Pseudo-nitzschia seriata was P. pungens (Balech, 1976; Lange, 1985; DA and Pseudo-nitzschia were reported reported along the entire Argentinean R.M. Negri and Inza, 1998; Ferrario et al., as the cause of the Canadian ASP out- coastline and in shelf waters from the 1999, 2002; Gayoso, 2001; Sastre et al., break in 1987, the presence of Pseudo- Beagle Channel in to 2001; Sar et al., 2006; Almandoz et al., nitzschia in Argentine waters was already Mar del Plata in the northern Province of 2007, 2017; Sunesen et al., 2009; well documented and facilitated the Buenos Aires (Frenguelli, 1939; Balech, Cadaillón, 2012; Krock et al., 2015a). implementation of phytoplankton mon- 1959, 1964, 1971, 1979; Frenguelli and There are only two reports of the itoring and food safety programs. Even Orlando, 1959; Muller Melchers, 1959; Pseudo-nitzschia delicatissima complex though no ASP outbreaks have occurred Carreto and Verona, 1974; Verona et al., in Argentinean waters, both only in San in Argentina to date, the presence of 1974; Carreto et al., 1981; Almandoz Matías Gulf (41°S, Province of Río Negro), DA has been confirmed along the entire et al., 2008, 2011). Given that the anal- published in 1974 (Carreto and Verona, Argentinean coastline during the last sev- ysis of P. seriata in these references was 1974; Verona et al., 1974). Eleven years eral years, after methods for the specific carried out by light microscope and that later, Pseudo-nitzschia fraudulenta was detection of DA were implemented in the

Oceanography | December 2018 | https://doi.org/10.5670/oceanog.2018.403 laboratories related to food regulation. to marine mammals in Argentine waters body weight after intraperitoneal injec- Accordingly, the records of DA detection (Cadaillón, 2012; Willson et al., 2015). tion (Tubaro et al., 2008). have a strong bias toward shellfish har- During oceanographic expeditions, DA PTXs are structurally related to OA/ vest and production areas, but generally was also detected in phytoplankton fur- DTX and feature the same structural are still scarce. ther south in the San Jorge Gulf (46°S) elements (Figure 1d,e), but in contrast 35˚SThe first report of DA in Argentina and Beagle Channel35˚S (55°S) (Krock et al., to OA/DTX, PTXs are lactones and do Province of Province of dates to the beginning of thisBuenos century Aires with 2015a) and in San Matías Gulf (41°S) Buenosnot Aires have free carboxylic acid groups. the detection of DA in Pseudo-nitzschia and Nuevo Gulf (42°S) (Almandoz et al., However, PTXs are not diarrheagenic, australis and blue mussels (MytilusEl Rincón edulis) 2017). Very recently, high levels of DA Eldespite Rincón their structural similarity to OA/ 40˚S 40˚S and (Engraulis anchoita) o ff were detected in feces of the Southern DTX, but show cytotoxic and hepato- San Matías Gulf San Matías Gulf Mar del Plata (Province of BuenosSan José Aires) Gulf Right Whale Eubalaena australis (Wilson Santoxic José Gulfeffects in mammals (Munday, (Montoya et al., 2000; R.M. NuevoNegri Gulf et al., et al., 2015; D’Agostino, 2017), provid- Nuevo2008). Gulf In general, toxic mechanisms are Chubut Chubut 2004).45˚S A second record concerns Pseudo- ing evidence that45˚S ASP is a risk not only not well understood, but the LD50 toxic- nitzschia detected inSan Jorgethe GulfProvince of for humans but also for marine Sanwild Jorge- Gulfity (intraperitoneal injection in mice) of Chubut, specifically Nuevo Gulf (42°S) life in Argentina. the most abundant variant PTX-2 was and Camarones Bay (45°S) (Sastre et al., determined as 219 µg kg–1 body weight 50˚S Santa DIARRHETIC50˚S SHELLFISHSanta 2007). The isolationCruz of P. multiseries from Cruz (Munday, 2008). coastal waters of the Buenos Aires region POISONING (DSP) YTXs are also polyketides, but con- confirmed its capacity to produce DA in Historically, when MBA was the only sist almost completely of condensed Tierra Beagle Channel Tierra Beagle Channel culture (Montoyadel Fueg et al.,o 2008). Five years technique available for thedel detection Fuego of ether rings for which they are also called 55˚S 55˚S Figure 1f later, DA was reported in phyto-Ocean Dataand View marine biotoxins, all lipophilic toxins “ladderOcean Data frame” View toxins ( ). In com- zooplankton75˚W 70˚Wsamples 65˚Wof the two60˚W North were regarded as 75˚WDSP toxins,70˚W because65˚W parison60˚W to OA/DTX and PTXs, they have Patagonian gulfs surrounding Valdés they are extracted all together with meth- higher molecular weights (>1,000 Da) Peninsula, San José Gulf and Nuevo Gulf anol and, moreover, many of these lipo- and are sulfated compounds. The vari- (41°–42°S), indicating for the first time philic toxins give similar responses in ability of YTXs is very high with over potential vectors of the marine food chain the mouse bioassay. In addition, many of 90 variants reported (Miles et al., 2005). these lipophilic toxins respond to MBA in YTXs share the lack of diarrheagenity a similar manner. Traditionally, okadaic with PTXs, and their toxic mechanism is acid (OA; Figure 1d), dinophysistoxins not known (Alfonso and Alfonso, 2008). (DTXs, which are structural variants of The intraperitoneal toxicity (LD50) in 35˚S OA), pectenotoxins35˚S (PTXs; Figure 1e), mice was determined to be 286 µg kg–1 Province of and yessotoxins (YTXs; Figure 1f) were Provincebody of weight, whereas its oral toxicity was Buenos Aires Buenos Aires regarded as DSP toxins. Recently, how- found to be more than two orders of mag- –1 El Rincón ever, this classification has been debated. Elnitude Rincón higher (54 mg kg ; Alfonso and 40˚S Although they40˚S show similar responses Alfonso, 2008). San Matías Gulf in the MBA after intraperitoneal injecSan- MatíasDSP Gulf syndrome is a frequent concern of San José Gulf San José Gulf tion, PTXs and YTXs, other than OA and small-scale shellfish fisheries in Argentina, Nuevo Gulf Nuevo Gulf Chubut Chubut 45˚S DTXs, do not have45˚S diarrhetic effects after because it can cause prolonged closure of San Jorge Gulf oral ingestion (Ogino et al., 1997).San JorgeIn Gulfmussel harvest areas (Turner and Goya, 1980 in Japan, Yasumoto et al. ultimately 2015). Monitoring for lipophilic toxins is proved the dinoflagellate Dinophysis fortii currently conducted in the country fol- 50˚S Santa to be the cause50˚S of DSP, butSanta until then the lowing the EU Harmonised Standard Cruz Cruz causative compound was still unknown. Operating Procedure for detection of OA is a linear polyketide of ca. 800 Da, lipophilic toxins by the MBA (EURLMB, Tierra Beagle Channel Tierra Beagle Channel del Fuego with several ether rings anddel Fuega terminalo 2013). Positive MBA results bring closure 55˚S carboxylic acid55˚S function (Figure 1d). OA of harvesting areas, and bans on selling of Ocean Data View Ocean Data View 75˚W 70˚W 65˚W 60˚W and DTXs have been75˚W proven 70˚Wto be specific65˚W shellfish60˚W from affected areas. Currently, FIGURE 4. Red dots indicate the geographic inhibitors of protein phosphatases 1 and only MBA is used in Argentina for rou- locations of DSP events and/or potentially toxic 2a. Symptoms in humans include diarrhe- tine monitoring of lipophilic toxins, and Dinophysis species; blue dots indicate the agenic and tumorigenic effects (Yasumoto very few data are available regarding the occurrence of P. reticulatum; green dots indi- cate where domoic acid (DA) has been reported and Murata, 1993). LD50 toxicity of OA identity of the lipophilic toxins responsi- in the Argentine Sea. in mice was assessed as 204–225 µg kg–1 ble for toxicity. Only a few analogues of

Oceanography | Vol.31, No.4 | Early Online Release each group are legislated, and their quan- Santinelli et al., 1994b, 2002; Santinelli, DSP associated with the presence of tity has to be referred to the predominant 2008; Gracia Villalobos et al., 2015), from Dinophysis species (D. acuminata and compound of each group, called the ref- the San Jorge Gulf (Akselman, 1996), D. caudata) occurred in 2010 in the erence compound. For OA, the DTX and and from middle shelf waters along the Northern Province of Buenos Aires PTX MPL is 160 µg of OA eq kg–1, and Argentine Sea (Fabro et al., 2015), as (36°–37°S), expressed in cases of human for YTX it is 3.75 mg YTX eq kg–1. well as in stomach contents of the com- illness after shellfish consumption (Sar Originally, OA was isolated from the mercially exploited scallop Zygochlamys et al., 2010). Samples of the wild clams marine sponge Halichondria okadai patagonica (Schejter et al., 2002), while Mesodesma mactroides and Donax (Tachibana et al., 1981) after which the D. tripos was recorded from middle shelf hanleyanus were contaminated with com- compound was named, but shortly there- waters (Fabro et al., 2015) and the North plex DSP toxin profiles composed of OA, after, OA and DTX-1 were reported Patagonian gulfs (Gracia Villalobos et al., DTX-1, Acyl-OA, and Acyl-DTX-1 (Sar from the benthic marine dinoflagellate 2015). D. caudata is considered a warm et al., 2012), whereas OA, DTX-1 and Prorocentrum lima (Murakami et al., water species, but seems to be toler- PTX2 were detected in plankton samples 1982). PTX was isolated from the scallop ant in this region (Balech, 1988), having during this event (Montoya et al., 2011). Patinopecten yessoensis (Yasumoto et al., been recorded in San Jorge Gulf in win- A comprehensive survey of bivalves 1985) and YTX from the same species ter (Akselman, 1996). D. fortii, first found undertaken by the Argentine public (Murata et al., 1987). PTX were reported north of 39°S beyond the shelf mar- health program revealed the occurrence to be produced by Dinophysis (Yasumoto gin within waters of the Brazil Current of several DSP toxins not only in the et al., 1988), whereas Protoceratium retic- (Balech, 1988), was later recorded in San Province of Buenos Aires but also in the ulatum was identified as a producer José Gulf (Gil et al., 1989). Prorocentrum North Patagonian gulfs, San Jorge Gulf, of YTX (Satake et al., 1997). In addi- lima was recorded in water samples from and Beagle Channel (Figure 4). Detected tion, Lingulodinium polyedra (Draisci the North Patagonian San José Gulf and DSP toxins included OA, DTX-1, DTX-2, et al., 1999) and Gonyaulax spinifera Nuevo Gulf (Gayoso et al., 2002) and from PTX-2, and YTX (Turner and Goya, (Rhodes et al., 2006) were later found the Beagle Channel in Tierra del Fuego in 2015). In more recent reports, PTX-2 to be YTX sources. 2013 (pers. comms. from Hugo Benavides, was found in the entire Argentine Sea, In Argentina, among the microalgae Instituto Nacional de Desarrollo Pesquero, associated with several Dinophysis spe- found to produce OA/DTX and PTX, October 20, 2017, and Marcelo Hernando, cies (Gracia Villalobos et al., 2015; Krock six species are associated with these tox- Comisión Nacional de Energía Atómica, et al., 2015a; Fabro et al., 2016), and ins, five of which belong to the genus October 26, 2017); it has also been iden- PTX-2 seco acid (PTX-2sa) was associ- Dinophysis (Hoppenrath, 2017; Zingone tified as an epiphyte on seaweeds (Gayoso ated with D. tripos in the northern area and Larsen, 2017). Dinophysis acuminata, et al., 2002), including the brown alga (37°–43°S; Fabro et al., 2015). D. caudata, and D. tripos were cited for Dictyota dichotoma in San Matías Gulf All three known YTX producers the first time by Balech (1988, and refer- (Gauna, 2010). (Lingulodinium polyedra, Gonyaulax ences herein), D. fortii by Gil et al. (1989), Generally, records of the occurrence spinifera, and Protoceratium reticulatum) D. norvegica by Fabro et al. (2016), and of DSP toxins in Argentine waters in the have been reported in Argentine waters Prorocentrum lima by Santinelli et al. scientific literature are scarce. The first (Balech, 1988). While L. polyedra is rare (1995). Phalacroma rotundatum (as DSP outbreak in Argentina occurred and has been observed in warm waters Dinophysis rotundata) is quite frequent in March 1999, caused by mussels har- influenced by the Brazilian Current, in this region (Balech, 1988), and while vested in San José Gulf and Nuevo Gulf motile stages of G. spinifera and P. reti c - it may contain DSP toxins, it is sus- (Figure 4). This DSP event was caused by ulatum are widely distributed, with their pected to be not a de novo toxin producer O-acyl esters of DTX-1 (summarized as cysts found in surface sediments of (González-Gil et al., 2011; Figure 4). DTX-3) that were detected in the con- coastal and mid shelf areas (Akselman, Whereas the occurrence of D. nor- taminated mussels (Gayoso et al., 2002). 1996; Akselman et al., 2015; Krock et al., vegica seems to be constrained to south- DTX-3 has never been observed in dino- 2015a). However, there were no records ern Argentine waters (>52°S; Fabro et al., flagellates but is known to form from of YTX from the Argentine Sea until 2016), consistent with its description as a OA/DTX-1/2 through bivalve metabolic very recently when YTX was detected in boreal species, D. acuminata and D. tripos activity (Yasumoto et al., 1985; Quilliam scallops from the Provinces of Buenos have been found in the entire Argentine et al., 1996). Despite the recurrent pres- Aires (39°S) and Santa Cruz (46°S) Sea (Balech, 1988). D. acuminata has been ence of Dinophysis in the area, this DSP (Turner and Goya, 2015) and in plank- recorded in plankton samples from the event was associated with Prorocentrum ton from San Jorge Gulf (Akselman et al., Patagonian coasts and North Patagonian lima (Gayoso et al., 2002). 2015; Krock et al., 2015a). In addition, gulfs (Gil et al., 1989; Sastre et al., 1990; The first record of an outbreak of Akselman et al. (2015) describe the YTX

Oceanography | December 2018 | https://doi.org/10.5670/oceanog.2018.403 profiles of two P. reticulatum isolates from AZA, such as on arrangement of F-actin, bloom, including the toxigenic Az. spino- the San Jorge Gulf, consisting of >95% on cytoskeleton, and on increase of cyto- sum, Az. dexteroporum, and Am. languida YTX and some variants in minor quan- solic calcium levels in lymphocytes. But (Tillmann and Akselman, 2016). tities. Comparison of species abundances the mechanisms responsible for diarrhe- To date, nothing is known about the and YTX levels in planktonic samples agenic and tumorigenic effects in ver- toxicity of Az. luciferelloides, nor is any- suggests that G. spinifera did not contrib- tebrates are not yet well understood thing known about the possible produc- ute to YTX levels found in the San Jorge (Twiner et al., 2014). The LD50 toxicity tion of toxins by the other species identi- 35˚S Gulf35˚S (Akselman et al., 2015). of AZA-1 in mice after intraperitoneal fied in the same water mass. Cultures are Province of Province of injection was determined as 0.2 µg kg–1 needed to evaluate their AZA production Buenos Aires Buenos Aires AZASPIRACID SHELLFISH body weight (Twiner et al., 2014). potential because it is known that toxin

El Rincón POISONING (AZP) El Rincón The first documented AZP event production can be variable among strains 40˚S 40˚S AZP is the most recently described shell- occurred in The Netherlands in 1995, of a single species (e.g., Gu et al., 2013). San Matías Gulf fish poisoning syndrome.San Matías Like Gulf many when eight people became ill after the Traces of AZA-2 were detected in yel- San José Gulf San José Gulf dinoflagellate toxins, azaspiracids (AZAs) consumption of Irish mussels (McMahon low clams (Mesodesma mactroides) and Nuevo Gulf Nuevo Gulf Chubut Chubut 45˚S are45˚S large polyethers in the mass range of and Silke, 1996). In the following years, mussels (Brachidontes rodriguezii) from San Jorge Gulf approximately 700 DaSan toJorge 900 Gulf Da. AZA AZA-1 was identified as the causative the Northern Province of Buenos Aires structure is characterized by a long car- compound (Satake et al., 1998), and (37°S) in 2008 (Turner and Goya, 2015). bon chain with several rings generated more AZA variants were subsequently This is consistent with the occurrence of 50˚S Santa by50˚S the formationSanta of ether rings, an amino detected in shellfish (Ofuji et al., 1999; AZA-2 producing Azadinium poporum, Cruz Cruz function in the terminal ring, and a car- James et al., 2003). Because AZAs belong which was isolated from resting stages boxylic acid at the other side of the mol- to the group of large polyketides, they (dinocysts) from El Rincón area (40°S). Tierra Beagle Channel Tierra Beagle Channel del Fuego ecule (Figuredel 1gFueg). oTo date, more than were suspected to be of phytoplanktonic Interestingly, in addition to AZA-2, 55˚S 55˚S 50 AZA variants have been reported. origin. However, the producing organ- these isolates also produce a phosphor- Ocean Data View Ocean Data View 75˚W 70˚W 65˚W 60˚W This75˚W high diversity70˚W is65˚W partly due60˚W to bio- isms remained unknown until a small ylated form of AZA-2—the first report synthetic variation in dinoflagellate bio- marine dinoflagellate of the newly iden- of a phosphorylated marine biotoxin synthesis and also to metabolic activity of tified genus Azadinium was proven to be (Tillmann et al., 2016). accumulating bivalves (Hess et al., 2014). capable of the de novo synthesis of AZA Several species of amphidomataceans Studies reveal several cytotoxic effects of (Krock et al., 2009; Tillmann et al., 2009). were identified in plankton samples col- To date, four species of the family lected across a geographic range from Amphidomataceae are known to pro- the San Jorge Gulf to Tierra del Fuego duce AZA: Azadinium spinosum (Krock in autumn 2004 and spring 2005 (author et al., 2009), Azadinium poporum (Krock Akselman, unpublished), along with a

35˚S 35˚S et al., 2012, 2015b), Amphidoma lan- dinoflagellate whose morphology is sim-

Province of Province of guida (Krock et al., 2012), and Azadinium ilar to Azadinium in the Beagle Channel Buenos Aires Buenos Aires dexteroporum (Percopo et al., 2013; (Ferrario et al., 2017), records that are Rossi et al., 2017). Huge blooms of complemented by the detection of AZA-2 El Rincón El Rincón 40˚S 40˚S Azadinium cf. spinosum were reported in in plankton samples from the eastern San Matías Gulf San Matías Gulf Argentinean shelf margin and mid-shelf mouth of Beagle Channel (author Krock, San José Gulf San José Gulf waters (38°30'–41°S) in 1990 and 1991 unpublished; Figure 5). The very recent Nuevo Gulf Nuevo Gulf Chubut Chubut (Akselman and Negri, 2012), and again in discovery of toxic Azadinium and the 45˚S 45˚S San Jorge Gulf San Jorge Gulf 1998 (Akselman et al., 2014), before the recorded diversity of Amphidomataceae genus Azadinium was described, and AZP in Argentina, which include toxigenic was unknown. After a more thorough and non-toxigenic species, poses a poten-

50˚S Santa 50˚S Santa study of archived material of the 1991 tial health risk; thus, more knowledge Cruz Cruz bloom, it became obvious that the bloom- about their geographic distribution and ing organism in fact was a new species, their production of AZA is needed. Tierra Beagle Channel Tierra Beagle Channel Azadinium luciferelloides. It was assumed del Fuego del Fuego 55˚S 55˚S that the other 1990s blooms were also CONCLUSION Ocean Data View Ocean Data View dominated by this species (Tillmann In comparison to its neighbor , 75˚W 70˚W 65˚W 60˚W 75˚W 70˚W 65˚W 60˚W and Akselman, 2016). In addition to Az. Argentina has not been affected as heav- FIGURE 5. Red dots indicate the occurrence of azaspiracids (AZA) and blue dots of Azadinium luciferelloides, several species of amphi- ily by harmful algal blooms (HABs). This in the Argentine Sea. domataceans co-occurred in the 1991 is partly due to the fact the Argentinean

Oceanography | Vol.31, No.4 | Early Online Release shellfish production is far less but also 12th International Conference on Harmful Balech, E. 1971. Microplancton de la campaña Algae, Copenhagen, Denmark, September 4–8, Oceanográfica Productividad III. Rev. Mus. Arg. subject to different hydrodynamic con- 2006. Ø. Moestrup G. Doucette, H. Enevoldsen, Cs. Nat. “B. Rivadavia,” Hidrobiología 3(1):1–202, ditions, which in the Southwest Atlantic A. Godhe, G. Hallegraeff, B. Luckas, N. Lundholm, 39 lám. J. Lewis, K. Rengefors, K. Sellner, and others, eds. Balech, E. 1976. Fitoplancton de la Campaña generally are less favorable for mass pro- Almandoz, G.O., E. Fabro, M.E. Ferrario, U. Tillmann, Convergencia 1973. Physis 35:47–58. A.D. Cembella, and B. Krock. 2017. Species Balech, E. 1979. Dinoflagelados, Campaña liferation of HAB species. To date, human occurrence of the potentially toxigenic dia- Oceanográfica Argentina Islas Orcadas. Servicio de poisonings only have been reported tom genus Pseudo-nitzschia and the associated Hidrografía Naval H 655:1–76. neurotoxin domoic acid in the Argentine Sea. Balech, E. 1988. Los dinoflagelados del Atlántico for PSP and DSP, the former being the Harmful Algae 63:45–55, https://doi.org/10.1016/​ Sudoccidental. Publicación Especial, Instituto most notorious, for both its high tox- j.hal.2017.01.007. Español de Oceanografía 1:310 pp. Almandoz, G.O., M.E. Ferrario, G.A. Ferreyra, Balech, E. 1995. The Genus Alexandrium Halim icity and the ubiquitous distribution of I.R. Schloss, J.L. Esteves, and F.E. Paparazzo. 2007. (Dinoflagellata). Sherkin Island, County Cork, The genus Pseudo-nitzschia (Bacillariophyceae) Ireland, 151 pp. species that produce it in the Southwest in waters of Argentina Bates, S.S., C.J. Bird, A.S.W. de Freitas, Atlantic. It is noteworthy that the high- (Southwestern , 38–55°S). R. Foxall, M. Gilgan, L.A. Hanic, G.R. 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An exceptional bloom of Alexandrium (ASP, AZP, and SSP) have not yet led to ern (Beagle Channel, Argentina). catenella in the Beagle Channel, Argentina. human poisonings, but the presence of Journal of Sea Research 66:47–57, https://doi.org/​ Pp. 113–119 in Harmful Marine Algal Blooms: 10.1016/​j.seares.2011.03.005. Proceedings of the Sixth International Conference the causative species and their associated Almandoz, G.O., N.G. Montoya, M.P. Hernando, on Toxic Marine Phytoplankton, October 1993, toxins pose a potential risk for these syn- H.R. Benavides, M.O. Carignan, and M.E. Ferrario. Nantes, France. P. Lassus, G. Arzul, E. Erard, 2014. Toxic strains of the Alexandrium ostenfel- P. Gentien, and C. Marcaillou, eds. dromes. To assess the HAB risk to liv- dii complex in southern South America (Beagle Cadaillón, A.M. 2012. Floraciones algales nocivas y Channel, Argentina). 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Bárcena, and E.A. Sar. 2009. ing in gentoo penguins (Pygoscelis papua) from Gemeinschaft Deutscher Forschungszentren through Potentially harmful diatoms from the San Matías the Falkland (Malvinas) Islands. Pp: 481–486 in the research programme PACES of the Alfred Gulf (Argentina). Revista de Biología Marina y Proceedings AAZV/AAWV/WDA. Joint Conference, Wegener Institut-Helmholtz Zentrum für Polar- und Oceanografía 44:67–88. San Diego, California. Meeresforschung, the European Commission under Sunesen, I., A.S. Lavigne, A.B. Goya, and E.A. Sar. Usup, G., and R.V. Azanza. 1998. Physiology and the 7th Framework Programme through the Action– 2014. Episodios de toxicidad en moluscos de aguas bloom dynamics of the tropical dinoflagellate IMCONet (FP7 IRSES, Action No. 319718), and projects marinas costeras de la Provincia de Buenos Aires Pyrodinium bahamense. 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