Harmful algal blooms in the austral Chilean channels and fjords

Harmful algal blooms in the austral Chilean channels and fjords

Progress in the oceanographic knowledge of Chilean interior waters, from Puerto Montt to Cape Horn.
N. Silva & S. Palma (eds.). 2008
Comité Oceanográfico Nacional - Pontificia Universidad Católica de Valparaíso, Valparaíso, pp. 99-103.
6.3 Harmful algal blooms in the austral Chilean channels and fjords
Georgina Lembeye
Departamento de Acuicultura, Subsecretaría de Pesca.
E-mail: [email protected]
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.,
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).
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
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Lembeye, G.
some filterers (e.g., clams) during winter in the
Aysén Region, when the motile phase was absent
(Lembeye, 1998).
Figure 3: a) Pseudo-nitzschia australis and b) Pseudo-nitzschia
pseudodelicatissima (bar scale: 10 microns).
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
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
were most abundant (> 100 cysts·mL–1) at the
stations located between 49° and 51° S (Fig. 4b).
The cysts of A. catenella were detected in low
concentrations (< 3 cysts·mL–1) 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, confirming the identification 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
cysts·mL–1) 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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Harmful algal blooms in the austral Chilean channels and fjords
76º
75º
74°
73º
76°
72°W
75°
B. San Quintín
Puerto Montt
S. Reloncaví
47°S
G. de Penas
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Pacific Ocean
í
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elon
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E. Comau
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42º
Pacific Ocean
G. de Ancud
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E. Steffen
13 12
E. Mitchel
C. Fallos
90
18
B. del Guafo
C. Messier
A. Inglesa
C. King
E. Falcon
84
C. Trinidad
C. Jacaf
90
76
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C. Pulluche
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B. Pitt
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C. Sarmiento
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79
F. Aysén
C. Costa
E. Quitralco
C. Concepción
E. Las Montañas
58
53
E. Cupquelán
Laguna
San Rafael
51°
68
E. Nelson
46º
50°
S. Penguin
S. Europa
E. Peel
88
C. Darwin
49°
S. Eyre
27
C. Picton
C. Moraleda
37
23
C. Ladrillero
Tictoc
45º
S. Iceberg
Puerto Edén
88
G. Corcovado
48°
C. Baker
9
43º
44º
73°W
74°
41°S
C. Smyth
Str
ai
CIMAR 2 Fiordos
G. Elefantes
t of
Ma
CIMAR 1 Fiordos
52°
Canal Kirke
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63
53°
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CIMAR 3 Fiordos
46º
Golfo Elefantes
CIMAR 4 Fiordos
72°
70°
68°
66°W 75º
74°
45º
Fiordo Aysén
18
31 Estero Quitralco
Estero Cupquelán
56°
74°
Canal Puyuguapi
Isla Meninea
35
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44º
Canal Jacaf
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Figure 4: Geographic position of the sampling stations of water and/or the top layer of sediments for the analysis of algae and/or algal
cysts causing harmful algal blooms, CIMAR 1, 2, 3, and 4 Fiordos cruises (Figures a, b, c, and d, respectively).
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Lembeye, G.
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 (>
100 cysts·mL–1) 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. 294298.
Nixon, S. W. 1995. Coastal marine eutrophication: a
definition, social causes, and future concerns.
Ophelia, 41: 199-219.
— 102 —
Harmful algal blooms in the austral Chilean channels and fjords
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.
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.
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.
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.
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