Ismael Gárate-Lizárragal, Martha Laura Hernández-Orozco2, Christine Band- Schmidt1 & Gustavo Serrano-Casillasi
iDepartamento de Plancton y Ecología Marina. CICIMAR-I.P.N. Apartado postal 592, La Paz, Baja California Sur, 23000 México. 2 lnstituto Mexicano del Seguro Social. Calle 5 de Febrero y Héroes de Independencia s/n. La Paz, Baja California Sur, México. I.G.L. is COFAA and EDI fellowship.
ABSTRACT. Thirty red tide spots were observed from 1984 to 2001 on both coasts of Baja California Sur.
The involved species were: Gonyaulax polygramma, Noctiluca scintillans, Mesodinium rubrum, Akashiwo sanguinea, Scrippsiella trochoidea, Ceratium furca, Prorocentrum mexicanum, and Cylindrotheca closterium. The most frequent species were N. scintillans and M. rubrum. The seawater discolorations by N.
scintillans were seen mainly in Bahía Concepción during Autumn-Winter. The blooms of M. rubrum were recorded in Bahía de La Paz and off Isla Cerralvo during Spring-Summer. The highest concentration of this species was 23,000 cells m1-1 during April 1994. Toxic species, producers of Paralytic Shellfish Poisoning (PSP) such as Alexandrium catenella, A. molinatum, and Gymnodinium catenatum, and a producer of haemolytic toxin P. mexicanum, were identified for Bahía Concepción and the west coast of the península.
However, most proliferations caused no PSP or other officially known public health problems. In this study, only three cases of fish, lobster, and marine bird mortality has been recorded for a coastal lagoon of Baja California Sur. The first was at Laguna San Ignacio and was caused by C. closterium and A. sanguinea. The second fish mortality occurred in la Ensenada de La Paz and was related to G. polygramma. The third (jellyfish mortality) was observed during a red tide of M. rubrum occurred in the southern part of the Gulf of California.
Key words: Red tides, Harmful algae blooms, Dinoflagellates, Baja California Sur.
Mareas rojas a lo largo de las costas de Baja California Sur, México (1984 a 2001)
RESUMEN. Un total de 30 manchas de mareas rojas se han registrado desde 1984 hasta 2001 en ambas costas de Baja California Sur. Las especies responsables fueron: Gonyaulax polygramma, Noctiluca scintillans, Mesodinium rubrum, Akashiwo sanguinea, Scrippsiella trochoidea, Ceratium furca, Prorocentrum mexicanum y Cylindrotheca closterium. Las especies más frecuentes fueron N. scintillans y M. rubrum. Las discoloraciones de N. scintillans fueron observadas principalmente en Bahía Concepción durante otoño-primavera. Los florecimientos de M. rubrum fueron registrados en Bahía de La Paz y alrededor de Isla Cerralvo durante la primavera-verano. La concentración más alta de esta última especie fue de 23,000 cels m1 -1 y se registró durante abril de 1994. Especies tóxicas productoras de envenenamiento paralítico por consumo de mariscos (PSP) tales como Alexandrium catenella, A.
molinatum, y Gymnodinium catenatum y especies productoras de toxinas hemolíticas como P. mexicanum fueron identificadas para Bahía Concepción. Sin embargo, la mayoría de las proliferaciones no han causado problemas de salud pública. En este estudio sólo tres casos de mortandad de peces, langostas y aves marinas fueron registrados para las costas de Baja California Sur. El primero ocurrió en la Laguna San Ignacio, y fue provocado por C. closterium y A. sanguinea. El segundo fue relacionado con G. polygramma y el tercero (mortalidad de medusas) fue observado durante una marea roja de M. rubrum ocurrida en la parte sur del Golfo de California.
Palabras clave: Mareas rojas, Florecimientos algales nocivos, Dinoflagelados, Baja California Sur.
Gárate-Lizárraga, I., M.L. Hernández-Orozco, C. Band-Schmidt & G. Serrano-Casillas. 2001. Red tides along the coasts of the Baja California Península, México (1984 to 2001). Oceánides, 16(2): 127-134.
INTRODUCTION
Red tides are natural phenomena. Howe- ver, the increase in the frequency, intensity, and geographical distribution of these events in the Iast two decades has had a great impact on health care and on the economy world-wide
Fecha de aceptación: 17 de mayo, 2001.
(Hallegraeff, 1993, 1995). In México, red tides and their toxicity have been known for centu- ries. It was known that it was dangerous to eat seafood collected during the first months of the year when red tides occurred (Carreto et al.
1981). Along the west coast of the Baja Cali- fornia Península and in the Gulf of California,
these events are common throughout the year. The gulf is also known as the Vermilion Sea, on account of the colour of the red tides (Cortés-Altamirano et al., 1987).
Along the coasts of Baja California Sur, marine fisheries constitute one of the main economic resources with the bivalve molluscs being one of the most important fisheries. For that reason, the occurrence of toxic phytoplan- kton species and the potential for blooms could have negative effects in this area, where the bivalves Argopecten ventricosus, Tivela stultorum, Lyropecten subnudosus, Anadara tuberculosa, Megapitaria aurantianca and Pin- na rugosa, are able to accumulate phycoto- xins. The purpose of this work is to provide an account of red tides occurred from 1984 to 2001 in different areas along the coasts of Ba- ja California Sur such as Bahía Concepción,
Bahía de La Paz, Bahía Magdalena, Laguna Ojo de Liebre and Laguna San Ignacio.
STUDY AREA
Red tides have been recorded along the west coast of Baja California peninsula and in the Gulf of California (Fig. 1). The currents sys- tem of the region is under the influence of the Equatorial Eastern Pacific Current, the Califor- nia Current (CC), and the North-equatorial Cu- rrent (CNE) (Wyrtky, 1967). Bahía Concep- ción is located on the western coast of the Gulf of California, and it is one of the largest bays in Baja California Sur (Fig 1). Shallow, with a mean depth of 22 m, it can reach a maximum depth of about 37 m in the central basin (Ramí- rez-Guillén, 1983). Laguna San Ignacio is bet- ween 26°43"and 26°58"N and 113°06'and 113°16"W, with an area of 17,500 ha. This la- goon is shallow, with a depth 2 to 4 m over the most of its area. In the channels that connect it with the ocean, the depth reaches 20 m (Swartz & Cummings, 1978). Laguna Ojo de Liebre is located between 27°35" and 27°52'N and 113°58" and 114°10"W, with an area of approximately 36,600 ha and it is 27 m depth (Contreras, 1988). Bahía de La Paz is a pro- tected water body, located between 24°10"
and 24°47"N and 110°20" and 110°44"W (Fig.
2). In the southern part it is relatively shallow,
Figure 1. Study areas and distribution of red tides recor- ded in the coasts of Baja California Sur, México.
Figura 1. Áreas de estudio y distribución de las mareas ro- jas en las costas de Baja California Sur, México.
increasing its depth to 400 m at the Alfonso ba- sin (Contreras, 1988).
MATERIAL AND METHODS
The samples used in this study come from Bahía de La Paz, off Isla Cerralvo, Bahía Concepción, Bahía Magdalena, Laguna San Ignacio and Laguna Ojo de Liebre. They were taken from the surface with Van-Dorn bottles and were fixed and preserved with Lugol and 3% formalin. Quantitative and qualitative analyses were done with a Zeiss inverted mi- croscope using 1 and 5 ml sedimentation chambers. All the organisms observed in the chamber were counted. For taxonomic identifi- cations the works of Osorio-Tafall (1942), Stei- dinger & Williams (1970), Taylor (1976), Do- dge (1982), Balech (1988), and Nezan (1996) were consulted.
RESULTS AND DISCUSSION From 1984 to 2001 several studies have been conducted with the marine phytoplan- kton communities along the Baja California península. During this period, more than thirty red tides have been recorded on both coasts.
11030 110
24
Figure 2. Distribution of red tides occurred at Bahía de La Paz, and off Isla Cerralvo.
Figura 2. Distribución de las mareas rojas ocurridas en Bahía de La Paz, y en el área adyacente de Isla Cerralvo.
The main species of dinoflagellates involved were: Gonyaulax polygramma, Noctiluca scin- tillans, Akashiwo sanguinea (=Gymnodinium sanguineum), Scrippsiella trochoidea, Cera- tium furca, Prorocentrum mexicanum, and the protozoan Mesodinium rubrum (Table 1).
Most of the red tides along the Baja California coasts have been of the non-toxic type, and fortunately have caused few cases of massive mortalities of marine organisms or health pro- blems to the human population (Sierra-Beltrán et al., 1996). In this study, the three most common blooming species found were N.
scintillans, M. rubrum, and A. sanguinea.
Noctiluca scintillans. This species is common in warm and cold waters (Steidinger
& Tangen, 1996). The largest number of red ti- de records of N. scintillans was for Bahía Con- cepción (Fig 1), where red tides are characte- ristic of Autumn-Winter (Gárate-Lizárraga, 1991, 1995), and occur mainly from November to May. This period is characterized by the disruption of the thermocline, the consequent homogenization of the water column, and an increase in the concentration of nutrients (Re- yes-Salinas, 1994). These conditions allow the proliferation of phytoplankton such as diatoms, dinoflagellates and other flagellates, which serve as food for N. scintillans (Kimor, 1979;
Gárate-Lizárraga, 1991). In this study, cope-
pod eggs were observed to serve as food of N.
scintillans. Cell density ranged from 125 to 881 cells m1 -1 (Table 1). A small patch of this spe- cies was observed for the first time in Bahía de La Paz (Fig. 2; Table 1), however, in January 2001 a very extended red tide of N. scintillans was observed from Playa el Coyote, Ensena- da de La Paz, and San Juan de la Costa (Fig.
2). Noctiluca abundance values were estima- ted at 2,550, 1,400 and 3,700 cells m1 -1 , res- pectively. Red tides caused by N. scintillans have also been reported for Bahía Bacochi- bampo, Sonora. These were related to upwe- Iling conditions caused by NW winds (Manri- que & Molina, 1997). This species is nota toxin producer, however, Fukuyo & Ishimari (1986) and Taylor et al. (1995) have indicated that it can accumulate large quantities of ammonia in its vacuole, which can be toxic to fish if inges- ted. In this study, blooms of N. scintillans occu- rred within a temperature interval of 18 to 21°C.
Mesodinium rubrum. This is a plankto- nic ciliate of cosmopolitan distribution (Taylor et al., 1971; Smith & Barber, 1979). The red ti- des of this species have occurred mainly in the area adjacent to Isla Cerralvo, and in Bahía de La Paz, for the most part in Winter-Spring (Fig.
2). Off Isla Cerralvo, two events were recorded in February 1994 and June 1995, with con- centrations between 400 and 525 cells m1 1 , respectively.
In Bahía de La Paz, M. rubrum blooms were recorded from May to June. The high concentrations of M. rubrum observed here (Table 1) were greater than those reported by Cortés-Altamirano (1984), Hernández-Bece- rril (1987), and Manrique & Molina (1997) for various areas of the Gulf of California.
Lindholm (1985) reported densities of 17,000 cells m1-1 along the Dutch coast, coinciding with the densities observed in this study. M. ru- brum may be considered a phytociliate becau- se it is completely autotrophic and is a primary producer (Pierce & Turner, 1992), because it has a degenerated cryptomonad endosym- biont. Leackey et al. (1992) mentioned that M.
rubrum could be responsible for local increa- ses in the concentrations of chlorophyll a. In March 1998 at the southern part of the Gulf of
Table 1. Red tides recorded in the coasts of the Baja California Sur and the Gulf of California from 1984 to 2001.
Tabla 1. Mareas rojas registradas en las costas de Baja California Sur y en el Golfo de California de 1984 a 2001.
Loca lity Species Date Density (cells
1. Bahía Concepción Noctiluca scintillans February 1988 156-189
2. Bahía Concepción Noctiluca scintillans December 1992 125
3. Bahía Concepción Noctiluca scintillans February 1994 881
4. Bahía Concepción Noctiluca scintillans November 1994 245
5. Canal de San Lorenzo Noctiluca scintillans March 1994 40,6
6. Bahía de La Paz Noctiluca scintillans March 2001 1,400-3,700
7. Bahía de La Paz Mesodinium rubrum April 1994 17,000-23,000
8. Bahía de La Paz Mesodinium rubrum May 1993 3,250
9. Isla Cerralvo Mesodinium rubrum February 1994 400
10. Isla Cerralvo Mesodinium rubrum June 1996 525
11. Bahía de La Paz Mesodinium rubrum February 1995 2,730
12. Bahía de La Paz Mesodinium rubrum April 1995 7,848
13. Bahía de La Paz Mesodinium rubrum May 1997 424
14. Bahía Magdalena Mesodinium rubrum December 1998 174
15. Costa Occidental BCS Akashiwo sanguinea August 1989 2,000-2,200
16. Costa Occidental BCS Akashiwo sanguinea July 1996 669
17. Laguna Ojo de Liebre Akashiwo sanguinea September 1996 248,6
18. Costa Occidental BCS Ceratium furca July 1996 1,636
19. Laguna Ojo de Liebre Cylindrotheca closterium September 1996 481,500
20. Bahía de La Paz Gonyaulax polygramma August 1984 1,200
21. Bahía de La Paz Prorocentrum mexicanun April 1992 3,135
22. Laguna de San Ignacio Scrippsiella trochoidea September 1996 1,307-1,703 23. Bahía de La Paz Scrippsiella trochoidea November 1998 102-65,156
24. Bahía de La Paz Scrippsiella trochoidea April 1999 7,542
California three patches of M. rubrum were ob- served with concentrations between 364 and 855 cels A jellyfish mortality was observed during this red tide. Recently, We found a small patch of 174 cells m1 -1 , in December 1998, at Bahía Magdalena, being the first report of this species for that area (Fig. 2).
Because of the exceptionally wide distri- bution of M. rubrum, it can be separated into two principal types: one extremely neritic within bays and fiords, and another offshore, invariably associated with upwelling areas (Taylor et al., 1971). Thus, the proliferations of M. rubrum off Isla Cerralvo and in Bahía de La Paz can be the result of upwelling, which occur during this season (De Silva, 1997) and also because of the "Island mass effect". The red ti- des of this species are very important in terms of the fertility of the coastal zone.
Akashiwo sanguinea. An estuarine and coastal species (Steidinger & Tangen, 1996).
Along the West Coast of the Baja California Peninsula and in the Gulf of California, red ti- des of A. sanguinea occur during the Summer (Fig. 1). Samples of a red tide produced by this species were collected at Punta San Hipólito (August 1989; Table 1). Low concentrations (2 cells m1 -1 ) of the toxic species Dinophysis forthü were estimated in the same samples. A similar case was reported for Bahía Tortugas with lower densities, between 93 and 860 cells ml -' (Turrubiates-Morales, 1994). Although considered a non-toxic species, Tindall et al.
(1984), Carlson & Tindall (1985), and Turru- biates-Morales (1994) noted the presence of dead fish in this bay, which was caused by gill obstruction due the high concentrations of A.
sanguinea. We found several red tides of A.
sanguinea and C. furca between Punta Colo-
1 p 14. I 11 p I
nett and Bahía San Quintín with concentra- tions between 669 and 1,636 cells m1 -1 and va- lues of chlorophyll a between 9.6 and 16 mgm-3 (Gárate-Lizárraga & Martínez-López, 1996). For this last case, other species that cause red tides, such as S. trochoidea, and A.
molinatum were identified. In September 1996, we sampled three yellow-brown patches at Laguna San Ignacio (Fig. 1; Table 1). These patches weresainly produced by Cylindrothe- ca closterium and A. sanguinea with average abundances of 481 cells m1 -1 and 248 cells m1 -1 , respectively. Fish, lobster, and marine bird mortality was observed during the presen- ce of these patches in the bay. This mortality could be caused by toxin producer species such as Dinophysis sacculus (8,4 cells Dinophysis acuminata (2,4 cells m1 -1 ), and P.
mexicanum (1,2 cells m1 -1 ).
Gonyaulax polygramma. This is a cos- mopolitan species in tropical and cold tempe- rate waters (Steidinger & Tangen, 1996). In this study, a single case of a red tide of G.
polygramma was recorded, this occurred in August 1984 at Ensenada de La Paz (Fig. 2).
Concentrations were approximately 1,200 cells m1 -1 and was related to fish mortality.
Even though this species is not toxic it can be harmful. Millán-Núñez (1988) reported a case for Bahía de Los Angeles in August 1978, which coincided with the death of several tons of fish. However, this author mentioned that such mortality was not attributed to toxins, but was associated with oxygen depletion in the water column.
Prorocentrum mexicanum. A yellowish band of approximately 20 meters long was ob- served for the first time in Bahía de La Paz (24° 21'N, 110° 21'W) in April 1992. A total of 3,135 cells m1 -1 of P. mexicanum were coun- ted. Other red tide producing taxa, such as P.
micans (174 cells m1 -1 ) and P. gracile (268 cells m1 -1 ), were identified and recorded (Gára- te-Lizárraga & Martínez-López, 1997). This species has been associated with the produc- tion of an haemolytic toxin and a fast-acting to- xin detected in culture (Bomber & Aikman, 1989). We have recently identified this species for the west coast of Baja California Sur and Bahía Concepción.
Scrippsiella trochoidea. A cosmopoli- tan species of neritic and estuarine waters (Steidinger & Tangen, 1996). During Septem- ber 1996, two patches present for three days at Laguna Ojo de Liebre were sampled (Fig.
1). They were composed mainly by S. trochoi- dea reaching densities of 1,307 cells m1 -1 , and 1,703 cells m1 -1 . Cysts of S. trochoidea were al- so observed. Abundances up to 5 cells m1 -1 of Dinophysis acuminata were also estimated in the samples. This is the first case of a red tide of S. trochoidea along the West Coast of Baja California Sur. From 17 to 24 November 1998 a very dense bloom of S. trochoidea occurred in a shrimp culture pond located in Playa Eren- dira, Bahía de La Paz (Fig. 2; Table 1). Scripp- siella abundances varied from 102 to 65,156 cells m1 -1 , and they occurred at temperatures between 26 and 28 °C. In April 1999 a highly concentrated bloom (7,000 cells m1 -1 ) constitu- ted totally of S. trochoidea was observed in Bahía de La Paz (Fig. 2; Table 1).
In the Gulf of California, particulary in Ba- hía Concepción during Winter-Spring we have identified species that produce PSP (Halle- graeff, 1995) such as Gymnodinium catena- tum, Alexandrium catenella (Gárate-Lizárra- ga, 1995; Verdugo-Díaz, 1997), and A. moli- natum. Low abundances of G. catenatum (1,8-3 cells m1 -1 ) have been recorded, and they occurred from March to August within a temperature interval of 18 to 28°C. From areas with moderate and high abundances of G. catenatum, Gárate-Lizárraga et al. (2001) have found that NeoSTX, dcSTX, dcGTX2, dcGTX2, B1-2, and C1-2-3 are quantitatively the most important PSP toxin in phytoplankton and scallop flesh samples.
Dinoflagellates which produce okadaic acid, such as Dinophysis acuminata, D. forthii, and D. sacculus, have also been recorded in this study, but in low concentrations. However, they should be considered as a potential dan- ger because they produce toxins that cause diarrheic shellfish poisoning (DSP) in humans due to consumption of filter-feeding molluscs.
The fishery of bivalve molluscs represents an important resource in several coastal lagoons of the Baja California Peninsula, such as Ba- hía Concepción, Bahía de La Paz, and Laguna
San Ignacio, where saxitoxin, okadaic acid, hepatoxin, and domoic acid have been found (Morquecho-Escamilla, 1996; Sierra-Beltrán et al., 1996).
In this study, only three cases of fish and other marine organism mortality have been re- corded. The first was related to G.
polygramma, and the second to C. closterium and A. sanguinea. The third was observed du- ring a red tide of M. rubrum. However, Ochoa et al. (1997) reported several toxic events on the northwest Pacific coastline, which caused mortality at different trophic levels. For this reason we are developing a sampling program to detect toxic or potentially toxic species, not only during their plankton phase, but also in their benthic phase (resistant cysts). The benthic phase (cysts) can be ten times more toxic than the vegetative cells (Carreto et al., 1981), and the presence of cysts in sediments could help to explain the onset of the red tides in a given area. We have observed cysts of S.
trochoidea in samples of Bahía Concepción, Laguna Ojo de Liebre and Bahía de La Paz.
ACKNOWLEDGEMENTS
The authors acknowledge the partial fi- nancial support by Conacyt (beca 138138), the Dirección de Estudios de Posgrado e In- vestigación (Projects: DEPI 966584, DEPI 980318, and DEPI 990446) to carry out this study. We also thank L. E. Paredes, R. Palo- mares, R. Saldierna, G. Vinatier, R. Avenda- ño, Verónica Maldonado, and D. Gendron for providing some of the red tide samples. We are also indebted to D.A. Siqueiros-Beltrones and Rosalba Alonso Rodríguez for their criti- cismo of the manuscript.
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