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6.3 Harmful algal blooms in the austral Chilean channels and fjords

Georgina Lembeye

Departamento de Acuicultura, Subsecretaría de Pesca.E-mail: glembeye@subpesca.cl

Progress in the oceanographic knowledge of Chilean interior waters, from Puerto Montt to Cape Horn.N. Silva & S. Palma (eds.). 2008Comité Oceanográfico Nacional - Pontificia Universidad Católica de Valparaíso, Valparaíso, pp. 99-103.

Harmful algal blooms (HABs), also known as “red tides”, are natural events in all the oceans of the world. In Chile, since the first report in 1972 in the Strait of Magellan, until a more recent one (2002) south of Chiloé, HABs have increased in both frequency and geographic coverage. Because HABs are highly toxic, they have come to create a serious problem for human health and the local economy.

HABs are caused by the proliferation of certain toxic microalgae, which are regular constituents of the planktonic microflora found in aquatic ecosystems. Their harmful effects can be caused by the presence of toxins, as occurs with the dinoflagellates responsible for paralytic shellfish poison (PSP) and diarrheic shellfish poison (DSP) and the diatoms responsible for amnesic shellfish poison (ASP). Some of the marine organisms that filter microalgae such as bivalve shellfish concentrate these toxins. Consumption of these organisms may seriously harm human health and may even be lethal. HABs can also affect farmed fish, with damaging and sometimes fatal consequences. The spines or silicic structures on some microalgae damage fish gills and impair respiration. Thus, HABs also have an economic impact on the development of aquaculture in the austral region.

The toxin-producing microalgae found in Chilean waters include the dinoflagellate Alexandrium catenella (Figs. 1a and 1b), which causes PSP; Dinophysis acuta (Fig. 2a), which is probably the main source of the toxic complex DSP; and D. acuminata (Fig. 2b), a widely distributed species throughout Chile that is also associated with the production of DSP (Wright & Cembella, 1998). Pseudo-nitzchia spp. diatoms can cause ASP; in Chile, the species linked to this toxin are P. australis (Fig. 3a) and P. pseudodelicatissima (Fig. 3b) (Guzmán et al.,

2002; Suárez et al., 2002). The diatoms Chaetoceros convolutus and Leptocylindrus minimus and the phytoflagellate Heterosigma akashiwo are among the microalgae responsible for mortality in farmed fish, particularly salmonids (Anderson et al., 2001).

The proliferation of harmful algae has been attributed to particular physical and chemical conditions that favor their reproduction and concentration, including marine currents, nutrients, temperature, and luminosity. The

Figure 1: Alexandrium catenella. a) chain of motile-phase cells, b) cyst (bar scale: 10 microns).

Figure 2: a) Dinophysis acuta, b) Dinophysis acuminata (bar scale: 10 microns).

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reasons for the increased frequency of HABs, their expansion to previously unaffected geographic areas, and the appearance of new species are numerous and mainly attributed to the transport and release of ballast water from other affected oceanic areas (Hallegraeff & Bolch, 1991), anthropogenic activities that cause variations in nutrient availability (Nixon, 1995), and possible alterations in the dynamics of oceanographic parameters attributed to “global climate change”, that might affect the organisms' diversity and abundance (Smayda, 1990; Hallegraeff, 1993). On the other hand, the systematic increase of research centers, regional health laboratories, and private programs that carry out constant monitoring activities has resulted in a greater number of records of these events, which might otherwise have gone unnoticed.

The research carried out between Puerto Montt and Laguna San Rafael (northern zone; Fig. 4a) has focused on detecting the distribution areas and abundance of the toxic species present in the phytoplankton, whereas studies from Golfo de Penas to Strait of Magellan (central zone; Fig. 4b) and from Strait of Magellan to Cape Horn (southern zone; Fig. 4c) have concentrated on the study of dinoflagellate cysts, particularly the distribution and abundance of A. catenella cysts (Lembeye, 2004), which are responsible for PSP. It is especially interesting to learn about the ecological role that the cysts play in dispersal mechanisms, survival, and genetic recombination of the different species (Anderson et al., 1995). In A. catenella, this is very important since the toxicity in cysts may be greater than in vegetative cells (Lirdwitayaprasit et al., 1990). In marine areas where the motile phase was not recorded, the detection of PSP in shellfish was attributed to cysts (Dale et al., 1978; White & Lewis, 1982). Cysts could be one of the causes of toxicity observed in

some filterers (e.g., clams) during winter in the Aysén Region, when the motile phase was absent (Lembeye, 1998).

The results obtained in the northern zone (Clément et al., 1996) show the distribution of the toxic dinoflagellates A. catenella and D. acuta, and the presence of harmful diatoms including C. convolutus and L. minimus. In this area, low concentrations of A. catenella and D. acuta were registered, respectively, at five and three stations in the study area. The toxin analysis for PSP and DSP in mytilid mollusks collected at 11 stations, however, only detected minimum concentrations of PSP at one station located in Canal Costa.

In the central zone, the presence of dinoflagellate cysts has been observed at most of the analyzed stations (Lembeye, 2004). The cysts

–1were most abundant (> 100 cysts·mL ) at the stations located between 49 and 51° S (Fig. 4b). The cysts of A. catenella were detected in low

–1concentrations (< 3 cysts·mL ) only at the stations of Puerto Edén, Punta Entrada in Canal Kirke, Punta Don Pedro in Sarmiento Channel, and Isla Cedomir in Canal Pitt. Along with A. catenella, cysts from 30 other dinoflagellate species were found, conf i rming the ident i f icat ion of Protoperidinium excentricum, P. conicoides, P. conicum, P. claudicans and P. denticulatum.

In the southern zone, cysts were observed in all the samples (Fig. 4c). Both more abundant (> 100

–1cysts·mL ) and more diverse cysts (> 10 distinct forms) were recorded in sediments obtained in Canal Ballenero.

A. catenella cysts were found in Bahía Borja and Canal Ballenero. Moreover, 27 cyst forms were observed, including nine forms that, due to their morphological characteristics, were attributed to the genus Protoperidinium. These were identified as: P. conicoides, P. conicum, P. claudicans, P. denticulum, and P. excentricum. Other species identified through cyst germination were Protoceratium reticulatum, Scrippsiella trochoidea, and S. sweeneyae. The cysts of both Scrippsiella species are morphologically equal; this was confirmed after germinating the cysts in cultures. In the samples from Bahía Parry, Alexandrium ostenfeldii was also detected by germinating the samples from sediments in cultures, but no cysts were detected that could be attributed to this species.

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Figure 3: a) Pseudo-nitzschia australis and b) Pseudo-nitzschia pseudodelicatissima (bar scale: 10 microns).

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During the CIMAR 4 Fiordos cruise in the northern zone, from Boca del Guafo to Estero Elefantes (Fig. 4d), cysts were observed in all the samples, with the greatest concentrations at Melinka, Puerto Harchy, and Estero Quitralco (Lembeye, 2004). The greatest cyst abundance (>

–1100 cysts·mL ) was associated with greater form diversity (> 10).

The A. catenella cyst was detected at 50 % of the studied sites, but the greatest concentrations were recorded at Estero Quitralco and Puerto Archy. Moreover, at least 34 distinct cyst forms were recognized; of these, the following were identified: Protoperidinium conicoides, P. conicum, P. claudicans, P. denticulum, P. excentricum, Protoceratium reticulatum, and Scrippsiella spp. The identity of the last two genera was confirmed through cyst germination.

The study carried out by Córdova et al. (2003) showed that the use of protease inhibitors could cause intracellular damage and death to A. catenella cells and cysts. Protease inhibitors act by disrupting the proteolytic activities at the level of cytoplasmic vacuoles and in proteasomes of the nucleus that affect the structure of the chromosomes. These studies offer options and future possibilities for the application of these compounds in the elimination of cysts from ballast water sediments, thereby preventing the dispersal of cysts and the proliferation of harmful microalgae species.

On the other hand, the study by Villarroel (2004) aimed to detect PSP and DSP, which have often been found in the austral zone and, for the first time, ASP was measured in order to determine its presence in samples from the Aysén Region. Furthermore, a high-resolution, liquid HPLC chromatographic analysis was done for the paralyzing toxin, providing more information about the saxitoxin derivatives that make up the PSP.

All these studies have furthered the knowledge of microalgae biodiversity in the austral channels and fjords and the geographic distribution of the harmful species in this extensive austral region.

References

Anderson, D. M., P. Andersen, V. M. Bricel, J. J. Cullen & J. E. Rensel. 2001. Monitoring and management

strategies for harmful algal blooms in coastal waters. APEC#201-ME-01.1, APEC Program, Singapore, and Intergovernmental Oceanographic Commission. Technical Series, 59: 268 pp.

Anderson, D. M., F. Fukuyo & K. Matsuoka. 1995. Cyst methodologies. In: Manual on harmful marine microalgae. Manual and guides. IOC- UNESCO, 33: 229-249.

Córdova, J. L., M. Pinto & G. Lembeye. 2003. Intracelular damage and death caused by protease inhibitors on Alexandrium catenelle natural cysts and vegetative cells. Harmful Algae 2:173-181.

Clément, A., X. Rojas & G. Lembeye. 1996. Distribución y abundancia de fitoplancton: énfasis en especies nocivas. Resultados Crucero CIMAR-Fiordo 1. Comité Oceanográfico Nacional, Valparaíso, Resúmenes Ampliados, pp. 82-84.

Dale, B., C. M. Yentsch & J. W. Hurst. 1978. Toxicity in resting cysts of the red-tide dinoflagellate Gonyaulax excavata from deeper water coastal sediments. Science, 201: 1223-1225.

Guzmán L., H. Pacheco, G. Pizarro & C. Alarcón. 2002. Alexandrium catenella y veneno paralizante de los mariscos en Chile. In: E. A. Sar, M. E. Ferrario & B. Reguera (eds.). Floraciones algales nocivas en el cono sur americano. Instituto Español de Oceanografía, Madrid, pp. 237-256.

Hallegraeff, G. M. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia, 32: 79-99.

Hallegraeff, G. M. & C. J. Bolch. 1991. Transport of toxic dinoflagellate cysts via ships' ballast water. Mar. Poll. Bull., 22: 27-30.

Lembeye, G. 1998. Seguimiento de la toxicidad en recursos pesqueros de importancia comercial en la X y XI Región. Informe Final Proyecto FIP, 86 pp.

Lembeye, G. 2004. Distribución de quistes de Alexandrium catenella y otros dinoflagelados en sedimentos de la zona sur-austral de Chile. Cienc. Tecnol. Mar 27(2): 21-31.

Lirdwitayaprasit, T., S. Nishio, S. Montani & T. Okaichi. 1990. The biochemical processes during cyst formation in Alexandrium catenella. In: E. Graneli, B. Sundstrom, R. Edler & D. M. Anderson (eds.). Toxic marine phytoplankton. Elsevier, New York, pp. 294-298.

Nixon, S. W. 1995. Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia, 41: 199-219.

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Smayda, T. J. 1990. Novel and nuisance phytoplankton blooms in the sea: evidence for global epidemic. In: E. Graneli, B. Sundstrom, R. Edler & D. M. Anderson (eds.). Toxic marine phytoplankton. Elsevier, New York, pp. 29-40.

Suárez, B., A. López, C. Hernández, A. Clément & L. Guzmán. 2002. Impacto económico de las floraciones de microalgas nocivas en Chile y datos recientes sobre la ocurrencia de Veneno Amnésico de los mariscos. In: E. A. Sar, M. E Ferrario & B. Reguera (eds.). Floraciones algales nocivas en el cono sur americano. Instituto Español de Oceanografía, Madrid, pp. 259-268.

Villarroel, O. 2004. Detección de toxinas paralizante, diarreica y amnésica en moluscos de la XI Región por Cromatografía Líquida de Alta Resolución (HPLC) y bioensayo en ratones. Cienc. Tecnol. Mar, 27(2): 33-42.

White, A. W. & C. M. Lewis. l982. Resting cysts of the toxic, red tide dinoflagellate Gonyaulax excavata in Bay of Fundy sediments. Can. J. Fish. Aquat. Sci., 39: 1185-1194.

Wright, J. L. C. & A. D. Cenbella. 1998. Ecophysiology and biosintesis of polyether marine biotoxins. In: D. M. Anderson, A. D. Cembella & G. M. Hallegraeff (eds.). Physiological Ecology of Hamful Algal Bloom. NATO ASI Ser., 41: 427-451.