Morphology of Pyrodinium bahamense Plate (Dinoflagellata) near Isla San José, Gulf of California, Mexico

Available online at www.sciencedirect.com

Harmful Algae 7 (2008) 664–670 www.elsevier.com/locate/hal

Morphology of Pyrodinium bahamense Plate (Dinoflagellata) near Isla San Jose´, Gulf of California, Mexico Lourdes Morquecho * Centro de Investigaciones Biolo´gicas del Noroeste (CIBNOR), Mar Bermejo 195, Colonia Playa Palo de Santa Rita, La Paz, Baja California Sur 23090, Mexico Received 9 April 2007; received in revised form 31 January 2008; accepted 5 February 2008

Abstract The morphology of Pyrodinium bahamense south of Isla San Jose´ in the Gulf of California, Mexico was described using light and scanning electron microscopy. Morphological and dimensional examination of whole cells and thecal patterns were conducted to discriminate between P. bahamense var. compressum and P. bahamense var. bahamense. Microscopic examinations confirmed that specimens of P. bahamense from Isla San Jose´ are closely related to P. bahamense var. bahamense. The main average dimensions were: cells 41.9 mm long, 43.8 mm wide, 55.6 mm amplitude, apical horn 7.2 mm long, and the left antapical spine 19.5 mm long. The highest cell concentration was 240 cells l1 and occurred with a bloom of Pseudo-nitzschia spp. The presence of this dinoflagellate off the east coast of the Baja California Peninsula had not been previously reported. Recently, P. bahamense from Florida tested positive for saxitoxins. Paralytic shellfish poisoning from this species has occurred in Mexican waters. Here, significant aspects of taxonomy, toxicology, life cycle, and ecology are discussed. # 2008 Elsevier B.V. All rights reserved. Keywords: Dinoflagellata; Gulf of California; Mexico; Morphology; Pyrodinium bahamense

1. Introduction Pyrodinium bahamense Plate is represented by P. bahamense var. compressum (Bo¨hm) Steidinger, Tester et Taylor 1980 and P. bahamense Plate 1906 var. bahamense. The morphology of the two varieties are similar. P. bahamense var. compressum is slightly compressed antero-posteriorly and forms long chains of cells (4 cells) and P. bahamense var. bahamense is rounded and has a more pronounced apical horn and usually found as solitary or in pairs (Steidinger et al., 1980; Taylor and Fukuyo, 1989). Balech (1985) compared specimens from Puerto Rico and Jamaica with specimens from New Guinea and The Philippines and argued that morphological differences did not justify separate varietal status. However, the consistency of the differences of the two varieties collected from the Atlantic and Indo-Pacific regions over the past 20 years support differentiation into varieties (Badylak et al., 2004). Commonly, var. compressum has been reported in the Indo-Pacific Ocean and var. bahamense in the Atlantic Ocean.

* Tel.: +52 612 123 8484; fax: +52 612 125 3625. E-mail address: [email protected]. 1568-9883/$ – see front matter # 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.hal.2008.02.003

Toxicity and strong paralytic shellfish poisoning (PSP) in the tropical Indo-Pacific has mainly been linked to var. compressum (Harada et al., 1982; Gacutan et al., 1985; MacLean, 1989; Mata et al., 1990; Corte´s-Altamirano et al., 1993; Wiadnyana et al., 1996; Azanza and Miranda, 2001; Azanza and Taylor, 2001; Llewellyn et al., 2006). Landsberg et al. (2006) recently confirmed toxicity of P. bahamense in the Indian River Lagoon in Florida. Osorio-Tafall (1942) reported, for the first time, the presence of P. bahamense in Central America. In Mexico, occurrence and blooms of this species have been reported for the Pacific coast, southern Gulf of Mexico, and Caribbean coast (Osorio-Tafall, 1942; Corte´s-Altamirano et al., 1993; Go´mez-Aguirre, 1998a,b; Licea et al., 2004). The variety compressum has been linked to outbreaks of PSP with human fatalities on the southern Pacific coast (Corte´s-Altamirano et al., 1993; Sotomayor-Navarro and Domı´nguez-Cuellar, 1993; Sotomayor-Navarro, 1994; Orellana-Cepeda et al., 1998; Fierro et al., 2002). P. bahamense var. bahamense has been found in lagoons surrounding the Gulf of Mexico and the Caribbean Sea (Go´mez-Aguirre, 1998a; Licea et al., 2004), and along the coast of the State of Sinaloa on the southeastern edge of the Gulf of California (Martı´nez-Lo´pez et al., 2007). In

L. Morquecho / Harmful Algae 7 (2008) 664–670

this area, the resting stage of P. bahamense has been reported in phosphorite sediments in the Gulf of California (Martı´nezHerna´ndez and Herna´ndez-Campos, 1991) and Bahı´a de Todos Santos in the State of Baja California (Pen˜a-Manjarrez et al., 2005). This study documents the presence of P. bahamense var. bahamense near the southwestern coast of Isla San Jose´ and provides a morphological description. P. bahamense var. bahamense has not been reported in Baja California Sur, Mexico. 2. Materials and methods

665

2.2. Sampling stations and field procedures The field crew collected 84 samples between 22 July and 14 August 2006 at seven stations located near the southwestern coast of Isla San Jose´ (Fig. 1). The general depth in the sampling area ranged from 5 to 77 m. Phytoplankton samples were collected every four days by using surface grabs and vertical hauls that used a 20-mm mesh net. Surface grabs were used for analyzing general phytoplankton composition and net hauls provided a concentrated aliquot of the Pyrodinium cell for morphological examination. Both types of samples were fixed with acid Lugol’s solution (Throndsen, 1978) and stored in a cool, dark area until analysis.

2.1. Study site description 2.3. Laboratory procedures Isla San Jose´ (258N, 1108400 W) is the largest island off the east coast of the State of Baja California Sur (19,400 ha), located at the northern end of Bahı´a de La Paz (Fig. 1). Since 1978, it has been a reserve for migratory birds and wildlife. On the west coast there are protected bays, while at the southwestern end, extensive beaches and a mangrove forest. The southern offshore area is exploited by fishermen from the isle of El Pardito (Fig. 1, sampling site 7).

Photographic records and measurements of the dinoflagellate were made with a digital camera (CoolSNAP-Pro, Media Cybernetics) and image processing software (Image-Pro Plus 4.1, Media Cybernetics). Microscopic observations were made with an inverted microscope (Axiovert 100, Carl Zeiss) and a phase contrast microscope equipped with an U-ECA 2 magnification changer (Olympus BX41TF). The squash technique was used to

Fig. 1. Location of sampling sites near Isla San Jose´, Gulf of California, Mexico.

666

L. Morquecho / Harmful Algae 7 (2008) 664–670

dissect thecal plates and observe key taxonomic features and to discriminate between varieties (Steidinger, 1979). Thecal arrangement and dimensions of our specimens were compared with those described in the literature (Osorio-Tafall, 1942; Steidinger et al., 1980; Balech, 1985; Taylor and Fukuyo, 1989; Corte´s-Altamirano and Herna´ndez-Becerril, 1992; Badylak et al., 2004; Faust et al., 2005; Martı´nez-Lo´pez et al., 2007). Scanning electron microscopy (SEM) was used to examine and define plate arrangement. Concentrated subsamples of P. bahamense cells were filtered directly onto to a Nucleopore polycarbonate filter (13-mm diameter, 3-mm pore size). The filter was rinsed twice with distilled water by gravity and covered with another Nucleopore filter to avoid the loss of material during dehydration and drying. The filter was dehydrated with a graded ethanol series (30, 50, 70, 90, 95, and 100%). After dehydration, the filter was dried in a critical-point dryer (Samdri, model PVT3B), and coated with palladium with a sputter coater (Denton Vaccum Desk II). The filter was observed on a PCcontrolled variable pressure SEM (Hitachi, model S-3000N), and digital images were obtained with Quartz PCI v.5.0 software. General phytoplankton composition and concentration of P. bahamense were determined by the method of Utermo¨hl (1958). In brief, samples were gently mixed by inverted rotation and aliquots were transferred into 50 or 100-ml sedimentation chambers and allowed to settle for 48 h. Aliquots were examined under the inverted microscope for phytoplankton compositions and counting of P. bahamense cells. The entire bottom of the chamber was scanned at 400. 3. Results 3.1. Light microscopy Specimens of P. bahamense found near Isla San Jose´ were single (Fig. 2A) or paired cells (Fig. 2B). Cell shape was

rounded with epitheca and hypotheca about equal in size. Mean length (without apical horn and antapical spines) was 41.9 mm (s = 5.6, n = 52), and mean width and amplitude were 43.8 (s = 4.8, n = 54) and 55.6 mm (s = 7.0, n = 53), respectively. A prominent apical horn, apical spine, and a list were observed (Fig. 2A). The apical horn had a mean length of 7.2 mm, ranging from 3.8 to 16.3 mm (s = 2.6, n = 25). In some specimens, an associated spine with the apical horn was observed (Fig. 2A) with a mean length of 10 mm, ranging from 5.6 to 13.9 mm (s = 2.5, n = 14). The left antapical spine had a mean length of 19.5 mm (s = 3.7, n = 36), ranging from 11.5 to 26.4 mm (Fig. 2B). The right antapical spine was bifurcated and had a mean length of 9.6 mm (s = 2.4, n = 7), ranging from 7.2 to 13.6 mm (Fig. 2C). The cingulum was ascending and displaced by approximately its width (Fig. 2C). Ten pores were identified on the Po plate; the comma-shaped canopy and anterior attachment pore was easily observed under light microscopy (Fig. 2D). The prominent ventral pore located on the 40 plate near its margin and the 10 plate were also easily observed under light microscopy (Fig. 2E). The cingular plates had aligned anterior and posterior pores (Fig. 2F). Sulcal plate numbers and arrangement were not defined; the squash technique exposed the posterior sulcal plate (Fig. 2G). 3.2. Scanning electron microscopy The Kofoidian plate formula for P. bahamanse was Po, pc, 40 , 600 , 6c, ?s, 6000 , 20000 (Fig. 3A and B). The plate sutures had a raised crest between the plates (Fig. 3A and B) and the cingular equatorial list was well developed (Fig. 3C and D). Pv ranged from 0.8 to 1 mm (Fig. 3E). The surfaces of the thecal plates were densely denticulated (Fig. 3F), and the size of the trichocyst pores ranged from 0.4 to 0.7 mm. Po is triangular and was 10.3 mm long and 7.7 mm wide with 10 pores on its surface (Fig. 3F).

Fig. 2. Light microphotographs of Pyrodinium bahamense from Isla San Jose´ in the Gulf of California. Scale bars = 20 mm (A–C) and 10 mm (D–G). (A) Ventral view of a cell showing apical and antapical spines; (B) pair of cells in ventral view; (C) ventral view of an empty theca, showing plate arrangement and cingulum displacement; (D) Po plate with comma-shaped canopy and pores; (E) hypotheca plate arrangement with 40 and ventral pore (arrow); (F) cingulum plate with anterior and posterior pores aligned; (G) S.p. plate separated with the squashing technique from the sulcal area.

L. Morquecho / Harmful Algae 7 (2008) 664–670

667

Fig. 3. Scanning electron microphotographs of Pyrodinium bahamense from Isla San Jose´ in the Gulf of California. Scale bars = 20 mm unless specified. (A) Apical view showing hypotheca arrangement; (B) antapical view showing epitheca arrangement; (C) ventral view of cell showing sulcal area; trychocyst pores (Tp) are indicated with arrows; (D) lateral view of cell showing the apical horn (Ah), bifurcated right antapicals (bra), and left antapical spine (las); (E) apical view with ventral pore in 40 plate (arrow); (F) detailed view of apical pore complex showing Po plate, pores, and comma-shaped canopy (scale bar = 5 mm).

3.3. General phytoplankton composition The population density of P. bahamense near the surface ranged from 20 to 240 cells l1, and the vegetative stage was only observed in four quantitative phytoplankton samples collected in late June 2006 at stations 1, 3, and 4 (Fig. 1). Station 3 had the highest cellular density. P. bahamense appeared with a bloom of Pseudo-nitzschia spp. (1.2  103– 7.3  105 cells l1), and contained other phytoplankton of the genera Ceratium Schrank, Chaetoceros Ehrenberg, Dactyliosolen Castracane, Eucampia Ehrenberg, Gonyaulax Diesing, Hemiaulus Heiberg, Phalacroma Stein, Prorocentrum Ehrenberg, Protoperidinium Bergh, and Skeletonema Greville. The

Pseudo-nitzschia bloom was associated with seasonal upwelling in Bahı´a de La Paz. 4. Discussion The morphological features and cell size of P. bahamense from Isla San Jose´ in the Gulf of California are closely related to var. bahamense, as described by Steidinger et al. (1980), Badylak et al. (2004), Faust et al. (2005), and Martı´nez-Lo´pez et al. (2007) (see Table 1). As these authors had documented, the specimens were less compressed antero-posteriorly than var. compressum and exhibit a prominent apical horn with a spine and prominent antapical spines with wide bases. Only

668

L. Morquecho / Harmful Algae 7 (2008) 664–670

Table 1 Morphometry of Pyrodinium bahamense from the Indo-Pacific and Atlantic Oceans Location

Indo-Pacific SE Mexico SE Mexico, Central America

Taxon

c a

Length (mm) (without horn and spines)

Wide (mm)

Average

Average

Range

50 66

a

Brunei Sabah Papua New Guinea

c c c

38 41 38

34–45 34–47

SE Mexico

c

48

SE Mexico Northern Sinaloa Mexico Southern Baja California Mexico

c b b

48 44 42

a a b b b a

35–47

43 41 72

Left antapical spine length (mm)

Average

Average

Range

Osorio-Tafall (1942) 34–64

3–6

43 45  3 44

38–47 40–53

46

37–60

44

42–51

37–60

44 43 44

42–51

33–55

37–71 44–58 34–77 33–47 62–85

40 43 53

Reference

Range

48 54

New Guinea, Philippines

Atlantic Puerto Rico Jamaica Florida, Jamaica Florida Belize Mexican Caribbean Sea

Range

Apical horn length (mm)

3–20

37–56

6 7

38–62 40–54 34–68

Steidinger et al. (1980)

Reduced

4–16

20 20

12–26

Corte´s-Altamirano and Herna´ndez-Becerril (1992) Corte´s-Altamirano et al. (1993) Martı´nez-Lo´pez et al. (2007) This study

Balech (1985) 2–6 7

37–52 48–59

11–19 15–21

2–8 Reduced

Balech (1985)

5–9

16

12–20

Steidinger et al. (1980) Badylak et al. (2004) Faust et al. (2005) Corte´s-Altamirano and Herna´ndez-Becerril (1992)

a, Pyrodinium bahamense; b, P. bahamense var. bahamense; c, P. bahamense var. compressum. All measurements were rounded.

single cell and paired-cell variations were observed in all samples. This feature was also found by Steidinger et al. (1980). Badylak et al. (2004) did find four-cell chains in samples from Indian River Lagoon in Florida. Except for the size of the cells, the illustrations of P. bahamense published by Osorio-Tafall (1942, Figs. 12 and 13) are similar to the features of var. bahamense found in Baja California Sur (Table 1). Osorio-Tafall (1942) documented P. bahamense and P. bahamense var. compressum as Pyrodinium schilleri (Matzenauer) Schiller near the coast of the State of Chiapas, Mexico. After this report and for about six decades, var. compressum was only reported in the Pacific off southern Mexico as a toxic red tide species (Corte´s-Altamirano et al., 1993; SotomayorNavarro and Domı´nguez-Cuellar, 1993; Sotomayor-Navarro, 1994; Orellana-Cepeda et al., 1998; Fierro et al., 2002). Only with the beginning of the 21th century was var. bahamense reported again along the Pacific coast of Central America and the Gulf of California (FWRI; Martı´nez-Lo´pez et al., 2007). Osorio-Tafall (1942) observed only a few specimens of P. bahamense in collections, as would be expected from the low concentrations recorded in the Gulf of California. Martı´nezLo´pez et al. (2007) found an average concentration of 100 cells l1 in the stretch of lagoons from Topolobampo to Santa Maria (25.58N, 1098W to 258N, 1088W) on the east side of the Gulf of California, while in the State of Baja California Sur on the opposite side of the Gulf, the concentration ranged from 20 to 240 cells l1. The presence of two recognized varieties of P. bahamense in tropical and subtropical waters of the Pacific Ocean off Central

America and Mexico and the toxicity of var. bahamense off the Florida coast led us to reconsider the conclusions of Balech (1985) and explore whether P. bahamense is truly a potentially toxic species, with no infraspecific taxa, whose toxicity and morphological variations result from external ambient factors. In fact, Landsberg et al. (2006) were testing the hypothesis that varietal distinctions may no longer be valid. Toxicity or lack of toxicity as a taxonomic characteristic to discriminate between varieties should also be reconsidered. Variations in toxin composition and toxin content, as well as loss of toxicity under laboratory conditions, have been studied in species of the genus Alexandrium Halim (Anderson, 1990; Anderson et al., 1990; Hansen et al., 2003; Martins et al., 2004). Similarly, diatoms of the genus Pseudo-nitzschia are not always toxic (Bates, 2000). In the Gulf of California, it is important to explore whether P. bahamense was introduced from Central America related to global climate change and El Nin˜o phenomena or if this dinoflagellate occurs mainly in the resting stage. P. bahamense cysts have a wide distribution, from Australia to Europe and Japan (Wall and Dale, 1969; Amorim and Dale, 1997). This distribution may reflect the relatively recent rise in seawater temperature, and if demonstrated, would lead to further shifts in geographical range. In that case, migration of tropical species to subtropical and temperate coastlines will continue (Llewellyn et al., 2006). This hypothesis agrees with Martı´nez-Herna´ndez and Herna´ndez-Campos (1991), who suggested that the low relative frequency of P. bahamense cysts in the Gulf of California may indicate the influence of warm water from the Eastern Tropical Pacific. Therefore, it is probable that El Nin˜o

L. Morquecho / Harmful Algae 7 (2008) 664–670

may transport vegetative cells or cysts of this species from Central America because these periodic climatic phenomena promote the incursion of low salinity seawater from tropical areas into the Gulf of California (Lo´pez et al., 2005; Castro et al., 2006). In coastal waters of Florida, P. bahamense var. bahamense has a salinity tolerance from 10 to 45, and from a broader perspective, presence in the Indian River Lagoon showed a response to longer term climatic cycles, like El Nin˜o and La Nina and stochastic rainfall events (Phlips et al., 2006). Even with cysts of P. bahamense occurring in the Gulf of California, blooms or seasonal occurrence of the vegetative stage had not been recorded. Other possible scenarios that could explain sporadic occurrences are that the dinoflagellate remains most of the time as resting cysts, with short periods as motile cells, because of adverse environmental conditions. Higher water temperatures (30 8C) are often correlated with P. bahamense blooms in Southeast Asia (Azanza and Taylor, 2001). High temperatures in the Gulf of California prevail in summer (July–October), the time when P. banamense occurred off Isla San Jose´. The toxicity of strains from the Gulf of California also needs to be confirmed, considering that elsewhere P. bahamense is involved in incidents of human fatality and economic losses in areas of aquaculture activity (Azanza and Taylor, 2001; Llewellyn et al., 2006). In Mexico, human health is endanger, particularly along the coast of Oaxaca and Chiapas because of P. bahamense toxic red tides (Corte´s-Altamirano et al., 1993; Sotomayor-Navarro and Domı´nguez-Cuellar, 1993; Fierro et al., 2002). In the Gulf of California, only Gymnodinium catenatum Graham has been linked with PSP outbreaks and fatal cases have only been recorded in the State of Sinaloa (Mee et al., 1986; Corte´s-Altamirano et al., 1995). In Baja California Sur, there are no reports of human fatalities from paralytic toxins; however, poisoning from consumption of the liver of Colorado snapper Lutjanus colorado Jordan et Gilbert and sawtail grouper Mycteroperca prionura Rosenblatt et Zahuranec, reported by Heredia-Tapia et al. (2002), was probably caused by saxintoxin-producing microorganisms. The victim fishermen showed classical symptoms of neurotoxin-contaminated fish ingestion: diarrhea; nausea; eye, muscle and abdominal pain; headache; numbness; vomiting; weakness; pruritus; desquamation; hyperesthesia; lip and tongue paralysis; and convulsions within 4–12 h after eating fish. Saxitoxin poisoning from puffer fish has linked with P. bahamense (Landsberg et al., 2006). In summary, this study is the first report of the occurrence and description of the morphology of P. bahamense var. bahamense in Baja California Sur, Mexico. It is clear that a comparative genetic-taxonomic survey of P. bahamense must to be done for the Pacific coast of Mexico, as well as biological, ecological, and toxicological studies to clarify the potential impact of this dinoflagellate within the Gulf of California. Acknowledgements Ana Luisa Guluarte-Castro of the Comite´ Estatal de Contingencias para el Control de Biotoxinas Marinas of Baja

669

California Sur kindly consented to the use of official data for this report. Ariel Cruz-Villacorta provided technical assistance in the SEM Laboratory; Amada Reyes-Salinas, Renato Mendoza-Salgado, Gerardo Herna´ndez-Garcı´a, and Oscar Armenda´riz-Ruı´z provided logistical support; and Erick Nun˜ez-Va´zquez and Yuri Okolodkov provided helpful suggestions and comments. This study was supported by CIBNOR research project #749-0.[TS] References Amorim, A., Dale, B., 1997. Distribution of cysts from toxic or potentially toxic dinoflagellates along the Portuguese coast. In: Reguera, B., Blanco, J., Fernandez, M.L., Wyatt, T. (Eds.), Harmful Algae. IOC-UNESCO, Paris, pp. 64–65. Anderson, D.M., 1990. Toxin variability in Alexandrium species. In: Grane´li, E., Sundstro¨m, B., Edler, L., Anderson, D.M. (Eds.), Toxic Marine Phytoplankton. Elsevier, New York, pp. 41–51. Anderson, D.M., Kulis, D.M., Sullivan, J.J., Hall, S., 1990. Toxin composition variations in one isolate of the dinoflagellate Alexandrium fundyense. Toxicon 28, 885–893. Azanza, R.V., Miranda, L.N., 2001. Phytoplankton composition and Pyrodinium bahamense toxic blooms in Manila Bay, Philippines. J. Shellfish Res. 20, 1251–1255. Azanza, R.V., Taylor, F.J.M., 2001. Are Pyrodinium blooms in the Southeast Asian region recurring and spreading? A view at the end of the millennium. Ambio 30, 356–364. Badylak, S., Kelley, K., Philips, E.J., 2004. A description of Pyrodinium bahamense (Dinophyceae) from the Indian River Lagoon, Florida, USA. Phycologia 43, 653–657. Balech, E., 1985. A revision of Pyrodinium bahamense Plate (Dinoflagellata). Rev. Paleobot. Palynol. 45, 17–34. Bates, S.S., 2000. Domoic-acid-producing diatoms: another genus added! J. Phycol. 36, 978–983. Castro, R., Durazo, R., Mascarenhas, A., Collins Curtis, A., Trasvina, A., 2006. Thermohaline variability and geostrophic circulation in the southern portion of the Gulf of California. Deep-Sea Res. (I Oceanogr. Res. Pap.) 53, 188– 200. Corte´s-Altamirano, R., Herna´ndez-Becerril, D.U., 1992. Plancton: Pyrodinium bahamense var. compressum. Ciencias del Mar 12, 24–26. Corte´s-Altamirano, R., Herna´ndez-Becerril, D.U., Luna-Soria, R., 1995. Mareas rojas en Me´xico: una revisio´n. Rev. Lat.-Am. Microbiol. 37, 343–352. Corte´s-Altamirano, R., Mun˜oz-Cabrera, L., Sotomayor-Navarro, O., 1993. Envenenamiento paralı´tico por mariscos (PSP), causado por el dinoflagelado Pyrodinium bahamense var. compressum en la costa suroeste de Me´xico. An. Inst. Cienc. Mar y Limnol. Univ. Nac. Auto´n. Me´xico 20 (1), 43–54. Faust, M.A., Litaker, R.W., Vandersea, M.W., Kibler, S.R., Tester, P.A., 2005. Dinoflagellate diversity and abundance in two Belizean coral-reef mangrove lagoons: a test of Margalef’s mandala. Atoll Res. Bull. 534, 103–131. Fierro, F., Lluch-Cota, S.E., Lluch-Cota, D.B., Corte´s-Alatamirano, R., SierraBeltra´n, A., 2002. Pyrodinium bahamense var. compressum bloom in Chiapas, Mexico, during 2001. Onset and effects.In: Xth International Conference on Harmful Algae, October 21–25, 2002. Book of abstracts. St. Pete Beach, Florida, USA, p. 93. FWRI (Fish and Wildlife Research Institute, Florida Fish and Wildlife Conservation Commission). Pyrodinium bahamense var. compressum and Pyrodinium bahamense var. bahamense – a comparison. General species descriptions. http://www.floridamarine.org/features/view_article. asp?id=24273 (viewed 23 Jan 2008). Gacutan, R.Q., Tabbu, M.Y., Aujero, E.J., Icatlo Jr., F., 1985. Paralytic shellfish poisoning due to Pyrodinium bahamense var. compressa in Mati, Davao Oriental, Philippines. Mar. Biol. 87, 223–227. Go´mez-Aguirre, S., 1998a. First record of Pyrodinium bahamense (Dinoflagellata) in brackish waters of the Mexican Caribbean coast. An. Inst. Biol. Univ. Nac. Auto´n. Mex. (Zool.) 69, 121–123.

670

L. Morquecho / Harmful Algae 7 (2008) 664–670

Go´mez-Aguirre, S., 1998b. Red tide occurrences recorded in Mexico from 1980 to 1992. An. Inst. Biol. Univ. Nac. Auto´n. Mex. (Zool.) 69 (1), 13–22. Hansen, G., Daugbjerg, N., Franco, J.M., 2003. Morphology, toxin composition and LSU rDNA phylogeny of Alexandrium minutum (Dinophyceae) from Denmark, with some morphological observations on other European strains. Harmful Algae 2, 317–335. Harada, T., Oshima, Y., Kamiya, H., Yasumoto, T., 1982. Confirmation of paralytic shellfish toxins in the dinoflagellate Pyrodinium bahamense var. compressa and bivalves in Palau. Bull. Jap. Soc. Sci. Fish. 48, 821–825. Heredia-Tapia, A., Arredondo-Vega, B.O., Nun˜ez-Va´zquez, E.J., Yasumoto, T., Yasuda, M., Ochoa, J.L., 2002. Isolation of Prorocentrum lima (Syn. Exuviaella lima) and diarrhetic poisoning (DSP) risk assessment in the Gulf of California, Mexico. Toxicon 40, 1121–1127. Landsberg, J.H., Sherwood, H., Johannessen, J.N., White, K.D., Conrad, S.M., Abbott, J.P., Flewelling, L.J., Richardson, R.W., Dickey, R.W., Jester, E.L.E., Etheridge, S.M., Deeds, J.R., Van Dolah, F.M., Leighfield, T.A., Zou, Y., Beaudry, C.G., Benner, R.A., Rogers, P.L., Scott, P.S., Kawabata, K., Wolny, J.L., Steidinger, K.A., 2006. Saxitoxin puffer fish poisoning in the United States, with the first report of Pyrodinium bahamense as the putative toxin source. Environ. Health Persp. 114, 1502–1507. Licea, S., Zamudio, M.E., Luna, R., Soto, J., 2004. Free-living dinoflagellates in the southern Gulf of Mexico: report of data (1979–2002). Phycol. Res. 52, 419–428. Llewellyn, L., Negri, A., Robertson, A., 2006. Paralytic shellfish toxins in tropical oceans. Toxin Rev. 25, 159–196. Lo´pez, M., Zamudio, L., Padilla, F., 2005. Effects of the 1997–1998 El Nin˜o on the exchange of the northern Gulf of California. J. Geophys. Res. (C Oceans) 110, C11005. MacLean, J.L., 1989. An overview of Pyrodinium red tides in the Western Pacific. In: Hallegraeff, G.M., Maclean, J.L. (Eds.), Biology, Epidemiology and Management of Pyrodinium Red Tides, Management and Training Workshop. ICLARM, Bandar Seri Begawan, Brunei Darussalam, Manila, pp. 19–26. Martı´nez-Herna´ndez, E., Herna´ndez-Campos, H.E., 1991. Distribucio´n de quistes de dinoflagelados y Acritarcas en sedimentos holoce´nicos del Golfo de California. Paleontol. Mex. 57, 1–133. Martı´nez-Lo´pez, A., Ulloa-Pe´rez, E., Escobedo-Urias, D., 2007. First record of vegetative cells of Pyrodinium bahamense (Gonyalucales: Goniodomataceae) in the Gulf of California. Pacific Sci. 61 (2), 289–293. Martins, C.A., Kulisa, D., Franca, S., Anderson, D.M., 2004. The loss of PSP toxin production in a formerly toxic Alexandrium lusitanicum clone. Toxicon 43, 195–205. Mata, L., Abarca, G., Marranghello, L., Viquez, R., 1990. Paralytic shellfish poisoning (PSP) due to Spondylus calcifer contaminated with Pyrodinium bahamense, Costa Rica, 1989–1990. Rev. Biol. Trop. 38, 129–136. Mee, L.D., Espinosa, M., Dı´az, G., 1986. Paralytic shellfish poisoning with Gymnodinium catenatum red tide on the Pacific coast of Mexico. Mar. Environ. Res. 19, 77–92. Orellana-Cepeda, E., Martı´nez-Romero, E., Mun˜oz-Cabrera, L., Lo´pezRamı´rez, P., Cabrera-Mancilla, E., Ramı´rez-Camarena, C., 1998. Toxicity

associated with blooms of Pyrodinium bahamense var. compressum in southwestern Mexico. In: Reguera, B., Blanco, J., Ferna´ndez, M.L., Wyatt, T. (Eds.), Harmful algae. Proc. VIII Interntl. Conf. on Harmful Algae. Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO, Vigo, Spain, p. 60. Osorio-Tafall, B.F., 1942. Notas sobre algunos dinoflagelados plancto´nicos marinos de Me´xico, con descripcio´n de nuevas especies. An. Esc. Nac. Cienc. Biol. 2, 435–450. Pen˜a-Manjarrez, J.L., Helenes-Escamilla, J., Gaxiola-Castro, G., OrellanaCepeda, E., 2005. Dinoflagellate cysts and bloom events at Todos Santos Bay, Baja California, Me´xico, 1999–2000. Cont. Shelf Res. 25 (11), 1375– 1393. Phlips, E.J., Badylak, S., Bledsoe, E., Cichra, M., 2006. Factors affecting the distribution of Pyrodinium bahamense var. bahamense in coastal waters of Florida. Mar. Ecol. Prog. Ser. 322, 99–115. Sotomayor-Navarro, O., 1994. Desarrollo de una marea roja to´xica producida por Pyrodinium bahamense var. compressum en el Golfo de Tehuantepec, Me´xico, 1989-1990. In: Compendio Oceanogra´fico del Golfo de Tehuantepec 1994, Estacio´n de Investigacio´n Oceanogra´fica, Secretarı´a de Marina, Direccio´n General de Oceanografı´a Naval, Salina Cruz, Oaxaca, Me´xico, pp. 87–113. Sotomayor-Navarro, O., Domı´nguez-Cuellar, E., 1993. Toxic red tide of Pyrodinium bahamense var. compressum, in the Tehuantepec Gulf of Mexico and the Central American Pacific system.In: VI Int. Conf. Toxic Marine Phytoplankton, Nantes, France, p. 185. Steidinger, K.A., 1979. Collection, enumeration and identification of free living marine dinoflagellates. In: Taylor, D.L., Seliger, H.H. (Eds.), Toxic Dinoflagellate Blooms. Elsevier, New York, pp. 435–442. Steidinger, K.A., Tester, L.S., Taylor, F.J.R., 1980. A redescription of Pyrodinium bahamense var. compressa (Bohm) stat. nov. from Pacific red tides. Phycologia 19, 329–334. Taylor, F.J.R., Fukuyo, Y., 1989. Morphological features of the motile cell of Pyrodinium bahamense. In: Hallegraeff, G.M., Maclean, J.L. (Eds.), Biology, epidemiology and management of Pyrodinium bahamense red tides: ICLARM Conference Proceedings 21. Fisheries Department, Ministry of Development, Brunei Darussalam, and International Center for Living Aquatic Resources Management, Manila, Philippines, pp. 207–217. Throndsen, J., 1978. Preservation and storage. In: Sournia, A. (Ed.), Phytoplankton Manual. UNESCO, Paris, pp. 69–74. Utermo¨hl, H. 1958. Zur Vervollkommnung der quantitativen PhytoplanktonMethodik. Mitteilungen-Internationale Vereinigung fu¨r Theoretische und Angewandte Limnologie 9, pp. 1–38. Wall, D., Dale, B., 1969. The hystrichospaerid resting spore of the dinoflagellate Pyrodinium bahamense Plate 1906. J. Phycol. 5, 140–149. Wiadnyana, N.N., Sidabutar, T., Matsuoka, K., Ochi, T., Kodama, M., Fukuyo, Y., 1996. Note on the occurrence of Pyrodinium bahamense in eastern Indonesian waters. Harmful and Toxic Algal Blooms. Intergovernmental Oceanographic Commission, Paris, pp. 53–56.