The Gulf of California is a subtropical, semi-enclosed sea with exceptionally high primary productivity [67]. It supports important commercial fisheries, tourism, shrimp aquaculture, and has a high influence of nutrient inputs mainly coming from agriculture activities of the East coast [68]. Several bays are found in this area: Bahía de Los Ángeles, Bahía Concepción, Bahía de La Paz, Bahía Bacochibampo, and Bahía de Mazatlán. The biggest urban developments in this region are the cities of La Paz and Mazatlán. The hydrography and seasonal productivity in the Gulf of California is governed by winds, upwelling, and large-scale climatic events [65,69–73]. During the last few decades, the number of species and duration of HAB events in the Gulf of California has increased [12,54], with G. catenatum being one of the toxic species that frequently forms blooms.

Graham [1] found G. catenatum for the first time in samples collected in March 1939 in the northern part of the Gulf of California (~29° N), forming a visible bloom of ~1 × 10⁶ cells L⁻¹ (Table 1). During the bloom, temperature and salinity ranged between 14–17 °C and 35.07–35.50 psu. More recently in this area, this species was reported in Puerto Libertad [9] and Bahía de Los Ángeles [11] (Table 1). In Bahía de Los Ángeles, paralytic shellfish toxins (PST) were detected in the scallop Nodipecten subnodosus(3–54 μg STXeq 100 g⁻¹).

In Bahía Concepción (Figure 1), G. catenatum is often present without forming blooms and is abundant when the water column is stratified with high concentrations of nutrients localized primarily at the sub-surface level (~20 m) [56,74]. In this bay, Gárate-Lizárraga et al. [16] reported a temperature range between 22 °C and 26 °C for G. catenatum (Table 1) and suggested that the temperature is an important factor in outbreaks of this species. They also concluded that the mesotrophic process, characterized by nitrogen limitation, partly explains the high concentration of neoSTX in G. catenatum. The highest PST concentration reported in bivalve mollusks in this bay is of 298 μg SXT eq 100 g⁻¹ in May 1999 [13]. Bahía Concepción is one of the few bays where studies on cyst dynamics have been done. Yields of cysts of G. catenatum are low, but seem to be a constant inoculum that sustains its population for long periods [75]. Cysts of this species have a short maturation period and can germinate under a wide range of environmental conditions [76,77].

In Bahía Bacochibampo(Figure 1), red tide events were monitored from 1970 through to 1994, with G. catenatum being one of the responsible species; however, no toxic events were reported [55] (Table 1). This bay is characterized by a high primary productivity associated with seasonal upwelling. In Bahía Kun Kaak (Figure 1), G. catenatum was reported during a multispecies bloom (April–May, 2003) that included a raphidophyte and other dinoflagellate species [10] and occurred under the influence of intensified upwelling and northwest winds. The raphidophyte dominated the bloom, which occurred at a mean temperature of 25.32 ± 0.99 °C, a salinity of 40.30 ± 1.03 psu, with phosphates and nitrates ranging from 0.54 to 3.0 mg L ⁻¹ and 0.1 to 0.2 mg L ⁻¹, respectively. In Bahía de La Paz (Figure 1), G. catenatum, has been registered several times since 1997 (Table 1), with cells densities varying from 1.6 × 10² to 6.0 × 10⁶ cell L⁻¹ within a temperature range from 18 to 26.5 ºC. In some events toxins have been detected in phytoplankton net samples and scallops, but toxin concentrations in scallops have never been above the maximum level for human consumption (0.14–67 μg SXT eq 100 g⁻¹) [15]. In this bay, G. catenatum has also coincided with other bloom forming species. In June 2003, low cell densities (800–1,200 cells L⁻¹) of this species were recorded during a bloom of Chaetoceros debilis Ehrenberg [18]. In February–March 2007, G. catenatum co-ocurred with N. scintillans [21], and during the bloom PST were found in several species of bivalve mollusks (Table 1). In June 2008, coinciding with a local upwelling event, Gárate-Lizárraga et al. [22] reported G. catenatum as one of the dominant species during a multispecies bloom of M. rubra, Katodinium glaucum(Lebour) Loeblich III, and Gyrodinium instriatum Freudenthal et Lee.

In June 2003, the presence of G. catenatum was associated with upwelling waters with high concentrations of nitrate, ammonium, and phosphate (4.5 μM, 7.4 μM, and 1.4 μM, respectively). However, these nutrient concentrations did not generate high G. catenatum densities, probably due to the dominance of the diatom. In June–July of 2006, another HAB event was recorded in Bahía de La Paz [19,20], under relatively low nutrient conditions. The average concentrations of nitrates, ammonium, and phosphates were low (1.0, 0.9, and 0.8 μM, respectively) [20].

Along the coastal lagoons of Sinaloa (eastern shore of the Gulf of California), G. catenatum is a common bloom forming species [78,79]. The first HAB reported in Mexico of this species was in Bahía de Mazatlán (Figure 1) from February to April of 1979. The bloom was very intense and extensive, with average cell densities of 1.2 × 10⁶ cells L⁻¹ and high levels of PST in bivalves (Table 1). Since this event, this area has been one of the most extensively monitored in our country. Between 1981 and 2006, many blooms of G. catenatum have been reported, however toxin analyses have not always been reported. From 2003 to 2007, PST in mollusks were between 63 and 1315 μg SXTeq 100 g⁻¹[30]. Analysis of the HAB of G. catenatum occurring in this area demonstrate that these events occurred mainly in late winter and early spring [79], during upwelling events [6,12,25,28,32,78,80–84], and within a temperature range of 16.5 to 32.9 ºC [9,15,23]. The effect of the El Niño or La Niña event for this species is not clear since Alonso-Rodríguez and Ochoa [80] did not find any bloom of G. catenatum during La Niña 2000 in Bahía de Mazatlán, however in Bahía de Bacochibampo, blooms of G. catenatum were found to increase during a La Niña events[ 55].

In Bahía de Mazatlán, G. catenatum has also been reported with other bloom forming species [28,82]. Alonso-Rodríguez [28] related a multispecies bloom (February 1995 to August 1996) with wind mixing processes, which contributed to the resuspension of cysts and nutrient increases, however, there was no clear relationship to eutrophication. In February 1996, an abrupt decrease of 2.5 °C in the mean surface temperature (from 24.5 °C to 22 °C) followed by a rapid rise in temperature to 24.0 °C, over a three day time period, coincided with a bloom of G. catenatum [83], suggesting that the temperature change favored the growth of this species. Recently, in Laguna de Macapule, a coastal lagoon in Sinaloa, G. catenatum was reported with an abundance of 38.8 × 10³ cell L⁻¹ [32]. Clearly, Bahía de Mazatlán is one of the zones in Mexico with the highest number of studies on the presence of red tide events caused by G. catenatum. Palynological records show that G. catenatum cysts have been present in the Gulf of California since ~1483 [81], with higher abundances from 1888 to 1920. Cyst abundances seem to increase during La Niña conditions and decrease during warmer El Niño events, abundances were also inversely related with sea surface temperature (SST), decreasing steadily from 1972 to 1994 as the SST increased in this area.

The western coast of the Baja California Peninsula is influenced by the California and North-equatorial Currents [83], and El Niño events [86,90]. It has a low human influence that is mainly linked to local fisheries of sardines and mollusks [88]. Bahía Magdalena, found in this area (Figure 1), is a highly eutrophic ecosystem influenced by intense currents, mixing processes, and upwelling [89]. Red tides have been reported during coastal upwelling [90]. In this bay, G. catenatum has been recorded once in net phytoplankton samples [34] (Table 1). This species has also been found in low concentrations (1200 to 4200 cells L⁻¹) near Punta Colnett, during summer when regional upwelling is dominant [33].

This area is an important tourist zone, and recently aquaculture activities—mainly shrimp farms—have been developed. The principal bays in this area are Bahía Banderas and Bahía de Manzanillo. In Bahía de Manzanillo the main merchant ship commerce is found [91]. Eutrophication linked to tuna factories [38] and continental nutrient discharges have been observed [92].

In Puerto Vallarta, G. catenatum was reported for the first time in 1979 (Table 1), during the same event that extended from La Cruz de Elota, Sinaloa to Jalisco [6]. In the winter and spring of 1999, a bloom of G. catenatum lasted approximately three months covering a large part of Bahía de Manzanillo [40,41] (Table 1); high oxygen values (18 mg L⁻¹) and low nitrate concentrations were recorded (0.05 μg-at L⁻¹). Seasonal marine currents in the area seemed to have dispersed the biomass, which avoided its accumulation at the bottom, which would create anoxic conditions that may limit the length of the bloom [93].

During 2000 and 2001, HAB of G. catenatum were documented in Puerto Vallarta and Bahía de Banderas (Figure 1) [35–37]. During spring 2007, G. catenatum abundances between 450 to 2,134,000 cells L⁻¹; however toxin levels found in the oyster species Crassostrea iridescens Hanley were below the maximum limit for human consumption (Table 1) [37]. In 2007, toxin concentration in mollusks was high (235 μg STXeq 100 g⁻¹) [42]. In a recently monitored area (Lázaro Cárdenas, Michoacán), a G. catenatum bloom was reported for the first time in November 2005, with a cell density of 560,000 cells L⁻¹[ 94].

Several hypotheses have been proposed for this area to explain the presence of these blooms: eutrophication linked to tuna factories [38], continental nutrient discharges [89], and transportation of cysts by ballast water [38]. Further detailed studies need to be carried out to confirm these hypothesis.

In this area important tourist influence is observed with the concomitant impact in nutrient inputs. Also river drainage is an important source of nutrients [95,96]. The principal bays are Bahía de Acapulco, Laguna Corralero-Alotengo, and Bahías de Huatulco.

Bahía de Acapulco (Figure 1) is a shallow bay (average depth, 20 m) with high anthropogenic impact and land drainage [95,96]. In March–April 1999, a red tide of G. catenatum was registered for the first time in Bahía de Acapulco (Figure 1), with cell densities between 7.6 × 10³–37.6 × 10³ cells L⁻¹, despite these relatively low cell densities, toxin concentrations in mollusks were above the maximum limit for human consumption [45,46] (Table 1). This species appeared again in November 2005 (6.29 × 10³ cells L⁻¹), January 2006 (10 × 10⁶ cells L⁻¹), and December 2007 (1942 × 10³ cells L⁻¹) [47,97]. These G. catenatum abundances are the highest reported for the Mexican Pacific. Toxicity values in mollusks during these events varied between 25 and 1152 μg STXeq 100 g⁻¹(Table 1) [48].

Further south, in the coasts of Oaxaca, blooms of G. catenatum have occurred since 1989 [50] (Table 1). Cell abundances have varied from 13 × 10³ to 10 × 10⁶ cells L⁻¹ [38,51,52]. Paralytic toxins were above the maximum limit for human consumption in 2001, however toxicity was also related to the presence of Pyrodinium bahamense [53,98], another PSP toxin producer.

Toxin analyses from phytoplankton net samples is a method to confirm that a toxic organism is found in the plankton community, and can help us understand the toxin profile of a toxic species in the environment. The toxin profile in net phytoplankton samples for Bahía Concepción, Bahía de La Paz, and Bahía de Mazatlán has been variable, however STX, neoSXT, GTX2-3, dcGTX2-3, B1, C1, and C2 have been found [15,16,21] (Table 2). Decarbamoyl (dcGTX2 and dcGTX3) and N-sulfocarbamoyl (C1 and C2) are usually the toxins with a high molar contribution [15,21]. Average toxin content reported in field phytoplankton samples from Bahía Concepción varied from 3.8 to 639.1 ng PSP filter⁻¹, and in Bahía de La Paz from 4.32 to 90.54 ng PSP filter⁻¹, Differences in the toxin profile have been observed between sampling stations in net phytoplankton samples, despite being collected during the same event; these differences could be explained by the different development stages of the red tide [21]. More data are needed from field samples in order to explain these differences.

Very limited data exists on the toxin content of natural populations of G. catenatum. Gárate-Lizárraga et al. [102] and Band-Schmidt et al. [103,104], found that the toxin content of the G. catenatum strains of the Gulf of California was higher (average values of 25.7–101 pg STXeq cell⁻¹) than the toxin content of natural populations (1.01 pg STXeq cell⁻¹). This could be related to strain growth conditions, because, in culture, the nutrient concentrations are much higher than in the environment. However, more data on toxin content per cell under natural conditions needs to be obtained to confirm these differences.

Differences found in the toxin profile of G. catenatum strains in vitro can be explained partly by the culture medium used. For instance, when using modified f/2 media, Bahía Concepción strains produce dcSTX, dcGTX2-3, C1, and C2 (Table 3). Other toxins, such as neoSTX, GTX2-3, B1, and B2 are only present in some strains and in low molar percentage (below 3 mol%) [17]. In contrast, when using GSe media, the number of saxitoxin analogs is higher (STX, neoSTX, dcSTX, dcGTX2-3, B1-2, C1, C2, C3, and C4); and the contribution of neoSTX is higher (from 6–46%) [104]. Neosaxitoxin has not been reported for strains from G. catenatum of other regions.

Differences in the toxin profile have also been observed with strain origin [102,104]: Bahía Concepción strains had the highest content of C1; BAPAZ and BAMAZ strains had a higher percentage of neoSTX. Differences in the toxin composition with culture age were observed only in BAMAZ and BAPAZ strains. These differences with culture age seem to be related to chain length, since cultures with a higher percentage of long chains had more neoSTX, while those with a higher proportion of short chains had a lower concentration of neoSTX. Differences in toxicity per cell were also observed:BAPAZ and BAMAZ strains were the most toxic (101 pg STXeq cell⁻¹), whereas strains from BACO were the least toxic (13 pg STXeq cell⁻¹).

The most abundant toxins in phytoplankton samples (dcSTX, dcGTX2-3, C1, and C2) do not vary in concentration in response to changes in culture media, strain origin, and N:P ratios. For example, when cultivating a strain from BACO with N:P ratios ranging from 1:6 to 32:1, no observable differences were found in the toxin profile across the different treatments [105]. However, the production of neoSTX often varies with the strain origin and with different culture media (Table 3). Additionally, the culture age seems to play a role in a differential production of saxitoxin analogs of G. catenatum [104,105]: after the tenth day of growth with different N:P ratios, an increase in the percentage of carbamoyl and decarbamoyl toxins occurred (18–26% and 11–16%, respectively) as compared with the toxin composition during the first eight days of culture, with a carbamoyl production from 9 to 14% and decarbamoyl production below 5% [105].

It seems that strains from the Gulf of California are characterized by the presence of neoSTX, and they seem to have evolved particular physiological responses to their environment that are reflected in their toxin profiles, suggesting different populations. Also, the variation in the toxin profiles of G. catenatum isolated from different zones of the Mexican Pacific (Bahía Concepción, Bahía de Mazatlán, and Bahía de La Paz), could be related to the differences in the source and concentration of nutrients of each embayment [102].

The analyses of the toxin content in different clams and scallops of several embayments from the Gulf of California has been done during the presence of G. catenatum (Table 1). Toxicity was variable: the highest toxicity values in mollusks were found in Bahía de Mazatlán (up to 7,500 μg STXeq 100 g⁻¹) [6] (Table 1).

The toxin profile of mollusks feeding naturally with wild populations of G. catenatum has also been determined in several species [15,21,30,37,103] (Table 4). The toxin profile varied within each zone and with mollusk species. In general, mollusks usually contained a high molar percentage of C1 and C2 toxins (see Table 4), similar to cultured G. catenatum strains, and phytoplankton net samples. Decarbamoyl toxins (dcSTX, dcGTX2-3) were also found in high molar percentages in mollusk samples.

An annual variation of toxicity and toxin profile in marine bivalves has been performed in Bahía de Los Ángeles, Bahía Concepción, Bahía de La Paz, and Bahía de Mazatlán [11,13,15,17,30,34]. Toxicity levels were correlated to the presence and abundance of G. catenatum cells in the water column, showing a clear seasonal pattern with higher toxin content in mollusks in May–June [13,17]. Toxin profiles of PST varied monthly, probably according to the cell abundance and metabolism of the mollusk. In most cases, N-sulfocarbamoyl toxins were the most abundant toxins, contributing usually more than 60% of the total toxin content. These high molar percentage contributions of the N-sulfocarbamoyl toxins may explain the low toxicity found in the shellfish (Table 2). Most shellfish contain a mixture of several PST, depending on the species of algae, geographic area, and shellfish species involved. For instance, toxic shellfish that grow in cold or temperate waters usually contain sulfated C toxins, GTX2-3, and STX [106]. When bivalves have recently ingested toxin-containing dinoflagellates, they typically contain high proportions of C1–C2 [4,13,15,107]. Experimental studies of toxicity in the scallop species M. squalida fed with G. catenatum also presented a high percentage of N-sulfocarbamoyl toxins, supporting the hypothesis that toxicity in scallops from the Gulf of California are linked to this dinoflagellate [108].

The presence of PST (GTX-2 and C1) has also been found in the liver of puffer fish Sphoeroides annulatus Jenyns from Bahía de La Paz and the mucus of Arothron meleagris Laceepéde from Punta Pericos. The analyses of the feeding behavior of these organisms, and the existence of PST dinoflagellates (e.g. G. catenatum) in the zone suggest the transfer of these toxins via mollusks[109].

Experimental work utilizing G. catenatum has focused on diverse physiological aspects of mammals, crustaceans, and bivalves (Table 5). Necropsy in mice (Swiss CD1 and BALB/c) with an acute saxitoxin exposure show a pronounced ischemic zone in the liver border. A degeneration of Purkinje cells in the cerebellum was also observed in histological observations of mice exposed to toxic extracts of G. catenatum [110]. Effects on grazing rates, egg production, and hatching success when the copepod Acartia clausi was fed with the dinoflagellate [101], showed no apparent harmful effects. However, egg production and hatching success increased with a higher consumption of G. catenatum. In the same experiment, the toxin profile of the copepod was analyzed, finding neoSXT, dcSTX, dcGTX2-3, B1-2, and C2 with a toxicity value of 12.7 pg STXeq copepod⁻¹ [16]. In conclusion, A. clausi not only accumulates PST but can also transform them. In natural populations, the effect on white shrimp larvae (Litopenaeus vannamei Boone) was lethal at concentrations of 50,000 cells L⁻¹ [99] (Table 1). Juvenile and adult shrimps injected with varying quantities of PST showed a time-to-death below seven minutes [111]. Chronic assays in shrimp also demonstrated significant differences in survival rates, percentage of feed, and weight gain [112]. Gastric glands and muscle of shrimp retained PST for a longer period and histological damages were observed in the heart, gastric gland, and brain tissue. These effects may explain the relationship of shrimp nauplii and postlarvae mortality in farms during a bloom of G. catenatum [23]. 10–20% mortality was observed in adults and metanauplii in Artemia exposed to G. catenatum. Behavioral symptoms such as erratic swimming, spasm, and convulsions were observed in Artemia when exposed to G. catenatum cells. Mortality of Artemia exposed to G. catenatum has been observed previously [113], and it has been demonstrated that Artemia can transfer PST via the marine food chain (Alexandrium tamarense to Artemia salina to Neomysis awatschensis to Lateolabrax japonicus)[114].

STX and neoSTX accumulated in the bivalves, M. squalida and Nodipecten subnodosus Sowerby, when exposed to G. catenatum cultures [108,115]. Differences in the toxin profile of the G. catenatum strains used in these studies were observed; the strain used by Estrada et al. [115] was rich in gonyautoxins, while the toxin profile of the strain used by Pérez-Cruz [108] was composed of STX, neoSTX, dcSTX, dcGTX2-3, C1, and C2, which is similar to those reported previously [17]. These differences could be due to culture conditions of the dinoflagellate, culture age, strain differences or extraction methods used. In both mollusks, the presence of highly toxic analogs suggests a biotransformation process [117] in a short time from N-sulfocarbamoyl to carbamoyl toxins. The depuration rate was moderate, between 0.19 and 0.23 day in the clam [108] and 0.4 day in the scallop [115], the toxin content after the thirteenth day in clams was only 4–5% of that found at the time of initiation. Short-term effects (24 h) on the immunological system of the clam N. subnodosus, when fed with G. catenatum, were also studied by Estrada et al. [118,119]. Several enzymes involved in antioxidant, lipid peroxidation, and hydrolytic activity were considered. Important changes were noted in the exposed scallops with an increase of antioxidant and hydrolytic enzymes mainly in the gills and the digestive gland. A melanization in gills, mantle, and labial palps was also reported. Lipid peroxidation has also been observed in Dosinia ponderosa and Crassostrea gigas exposed to G. catenatum cells [120]. Different responses to toxin exposure can be expected, since life history exposure to toxins plays an important role [116].

Blooms of G. catenatum, among other toxic species along the coast of Sinaloa (Gulf of California), caused the death of nauplii and adult shrimps in shrimp farms [23,24,121]. These authors assumed that the toxicity was caused by G. catenatum in the water introduced to the ponds by the pumping system. The mortality occurred with the events of HAB of G. catenatum from February to March 2001, concluding that the contamination, climatic conditions, and inadequate management in fertilization, feeding rate, and food composition can provoke delay in the growth of the shrimp and decrease their production through massive mortality. Sierra-Beltrán et al. [122] speculated that in the central part of the Gulf of California, the urban aquatic residues and the eutrophication generated by the shrimp farmers could be responsible for the proliferation of G. catenatum and other species. García-Hernández et al. [10] concluded that the residues of the shrimp farms and shrimp larvae producing laboratories are deposited without treatment to Bahía Kun Kaak, which is known to be a highly productive ecosystem. This natural condition, and the water input with high content of nitrogen and phosphorus compounds, probably contributes to the formation of red tides. Other regions of the coasts of Sonora (Gulf of California) have also had high nitrogen contributions, related to fertilization process, which are added to coastal waters by runoff (36.8 × 10⁶–201 × 10⁶ moles of N) [64]. These findings suggest that this loss by irrigation can support phytoplankton blooms in the Gulf of California. It is probable that the eutrophication processes in this ecosystem are seasonal events [123] and are influenced by upwelling events, agriculture, and aquaculture contributions. Dumping and wastewater treatment regulations are recommended to obtain a good water quality, and equilibrium in the phytoplanktonic communities. These results show the importance of establishing continuous monitoring of the water quality that flows into and out of shrimp culture systems.