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Perspectives in Phycology Open Access Article
Published online February 2019
© 2019 The authors
DOI: 10.1127/pip/2019/0081 E. Schweizerbart'sche Verlagsbuchhandlung, 70176 Stuttgart, Germany, www.schweizerbart.de
Impacts of harmful algal blooms on the aquaculture industry:
Chile as a case study
Patricio A. Díaz1,*, Gonzalo Álvarez2, Daniel Varela1, Iván Pérez-Santos1,3,
Manuel Díaz4, Carlos Molinet4, Miriam Seguel5, Alejandra Aguilera-Belmonte6,
Leonardo Guzmán7, Eduardo Uribe2, José Rengel2, Cristina Hernández8, Cristian
Segura9 and Rosa I. Figueroa10,11
1 Centro i∼mar & CeBiB, Universidad de Los Lagos, Casilla 557, Puerto Montt, Chile
2 Departamento de Acuicultura, Facultad de Ciencias del Mar, Universidad Católica del Norte, Larrondo 1281,
Coquimbo, Chile
3 CentrodeInvestigaciónOceanográcoCOPASSur-Austral,UniversidaddeConcepción,Campus
Concepción, Concepción, Chile
4 Programa de Investigación Pesquera, Instituto de Acuicultura, Universidad Austral de Chile, Puerto Montt,
Chile
5 Centro Regional de Análisis de Recursos y Medio Ambiente (CERAM), Universidad Austral de Chile, Puerto
Montt, Chile
6 Universidad San Sebastián, Lago Panguipulli 1390, Puerto Montt, Chile
7
Centro de Estudios de Algas Nocivas (CREAN), Instituto de Fomento Pesquero, Padre Harter 574, Puerto
Montt, Chile
8 Laboratorio Salud Pública, Seremi de Salud Región de Los Lagos, Crucero 1915, Puerto Montt, Chile
9 Instituto Tecnológico de la Mitilicultura (INTEMIT), Blanco 324, Castro, Chile
10 CentroOceanográcodeVigo,InstitutoEspañoldeOceanografía(IEO),SubidaaRadioFaro50,36390
Vigo, Spain
11 Aquatic Ecology, Biology Building, Lund University, 22362 Lund, Sweden
* Corresponding author: patricio.diaz@ulagos.cl
With4guresand1table
Abstract: Harmful algal blooms (HABs) of toxin-producing microalgae, mainly Alexandrium catenella, Dinophysis spp., and Pseudo-
nitzschia australis, cause the severe illnesses referred to as paralytic, diarrheic, and amnesic shellsh poisoning. They therefore threaten
the sustainable exploitation of bivalves, including in northern and southern Chile, sites of intensive shellsh aquaculture but also recurrent
HABs. Exceptionally large blooms of the genera Pseudochattonella and Karenia recently occurred in the Patagonian fjords, leading to high
sh mortalities (up to 40 000 t) and thus to very negative impacts on the salmon farming industry. The resulting economic losses were
estimated to be US$800M. Here we examine past, present, and possible future trends of the main HAB-causative species in Chile, with the
objective of improving risk assessments of shellsh poisoning and other hazardous events in the region and elsewhere.
Keywords: HAB-causing species; Shellsh aquaculture; Socio-economic impacts; PSP outbreaks; ASP outbreaks; DSP outbreaks; Chile
1 Introduction
The term harmful algal blooms (HABs) was coined by
the Intergovernmental Oceanographic Commission (IOC)
of UNESCO to describe any proliferation of microalgae,
regardless of the concentration, that is perceived as a nui-
sance because of its negative socio-economic impact on
public health, sheries resources, and coastal commodities.
According to Hallegrae (2003), there are three main types of
HAB-causing microorganisms: i) non-toxin-producing spe-
cies that aect the recreational value of the sites where they
proliferate, by causing discoloration of the water or enor-
mous amounts of foam, or cause high rates of sh mortalities
via the drastic reduction of dissolved oxygen in water, due to
the explosive increase in microalgal cell density; ii) toxin-
producing species that through their uptake by the food chain
can cause a variety of neurological and gastrointestinal dis-
orders in humans, including paralytic, diarrheic, and amne-
2 P.A.Díazetal.
sic shellsh poisoning, and thus pose an important threat to
public health and shellsh exploitations; iii) species that are
not toxic to humans but aect sh in culture, by physically
damaging the sh, e.g., by obstructing their gills, and/or by
the production of ichthyotoxic substances.
Among the vast array of microalgal species with impor-
tant potential socio-economic impacts are ~100 species
identied as toxin-producing, 70% of which belong to the
group Dinophyta (Zingone & Enevoldsen 2000; Moestrup
et al. 2009). The impact of their blooms is directly related
to the potency of the shellsh toxins they produce, many of
which are among the most potent bioactive compounds yet
described (van Egmond 2004). Filter-feeding bivalves accu-
mulate microalgal toxins, which can reach concentrations
(regulatory levels) unsafe for human consumption and thus
force health and sheries authorities to implement manage-
ment measures, including the closure of shellsh harvesting.
This in turn causes dramatic eects on the aquaculture indus-
try and the exploitation of natural shellsh banks. During
extreme toxic events, the consumption of illegally obtained
shellsh has resulted in the deaths of the consumers.
In recent decades, new scientic and technological knowl-
edge in parallel with the rapid development of aquaculture
has resulted in the detection of new HAB species in dier-
ent geographic areas, thus globally increasing the number of
known harmful species (Masó & Garcés 2006). Increases in
the frequency and intensity of toxic events at a global scale
have also become apparent, partly explained by the progres-
sive increase in the exploitation of coastal resources (aquacul-
ture, tourist industry), the exponential growth of monitoring
programs (Hallegrae 1993; Hallegrae 2010), and, perhaps
most importantly, increased microalgal growth and dispersal
due to anthropogenic factors (Anderson et al. 2012; Anderson
2014), in particular water eutrophication and climate change
(Heisler et al. 2008; Glibert et al. 2014; Gobler et al. 2017).
The increased geographic distribution, duration, and intensity
of HABs was pointed out by the FAO in its Food and Nutrition
Paper 80 on Marine Biotoxins (FAO 2004). While the magni-
tude of the problems derived from HAB events varies tremen-
dously, depending on factors such as the geographic region,
the seafood product aected, and the frequency and inten-
sity of the blooms, the losses suered by local and regional
economies, whether directly or indirectly, are often enormous
and include the aquaculture, sheries, and tourism sectors.
According to the UNEP Global Environmental Outlook, the
annual worldwide economic impact of algal biotoxins on
human health from seafood alone is ~US$4.0 billion. This
includes costs related to product marketability, resulting from
limitations on the amount and duration of shellsh harvesting
(see revision by Berdalet et al. 2015 and references therein).
In northern and southern Chile and especially in the
Patagonian fjords, HABs have followed the above-described
global trend of increasing impact, with recurrent problems
over the last four decades (Guzmán & Campodónico 1975;
Guzmán et al. 2002; Díaz et al. 2014). The Chilean economy
is especially vulnerable to the negative impacts of HABs, as
aquaculture and pecteniculture have become two of the most
dynamic and successful economic activities in the country. In
fact, after Norway, Chile is the largest producer worldwide
of salmon and trout. The salmon sector has created a devel-
opmental nucleus in southern Chile, including more than 1
200 enterprises, 500 of which are based on salmon aquacul-
ture while others are service companies (INE 2009). Almost
90% of salmonid production occurs in the Los Lagos region,
where in 2007 there were 53 hatcheries (Pinto 2007) in addi-
tion to several feed companies. Total employment in salmon
aquaculture in 2008 was estimated at 55 000, with 60% of
these jobs being processing related (Hishamunda et al. 2014).
In the following, we provide a closer look at the impacts of
HABs in the northern and southern regions of Chile.
2 HABs and their impact in northern Chile
Historically, bivalve aquaculture in northern Chile has
largely been that of the scallop Argopecten purpuratus
(Lamarck 1819). Although traditionally exploited from natu-
ral populations or banks by artisanal extraction techniques,
over-harvesting has necessitated the implementation of sev-
eral administrative measures by Chilean authorities, to avoid
the total depletion of this valuable resource (Thiel et al.
2007). Thus, since 1958, successive bans on scallop exploi-
tation within an extensive area, extending from Arica (18°
2′S) to Valparaíso (33°S), have been applied. Following the
frequent market appearance of illegally harvested scallops,
in 1986 Chilean authorities imposed an indenite ban on the
harvesting of A. purpuratus (Avendaño & Cantillanes 1996).
However, the subsequent closure of scallop sheries pro-
vided an incentive to develop and initiate scallop aquacul-
ture, rst experimentally, between 1983 and 1985, and then
commercially, beginning in 1989 (Illanes & Akaboshi 1983;
Disalvo et al. 1984; Uriarte et al. 2001). Since 1990, Chilean
scallop production has grown rapidly, yielding 1,529 met-
ric tons (mt) in 1991 and 26,933 mt in 2004. Consequently,
Chile has become the third largest scallop aquaculture pro-
ducer worldwide, after China and Japan (von Brand et al.
2016).
The development of this prosperous industry was accom-
panied by a large commercial eort, including recognition of
the scallop as coquille Saint Jacques on the French market. In
response to requirements of the Food and Drug Administration
and the European Community, certication systems to ensure
the safety of cultured molluscan shellsh for consumers were
established (Suárez-Isla et al. 2002; von Brand et al. 2016).
Since 1989, the Chilean sheries authority (SERNAPESCA)
has monitored scallops harvested from aquaculture sites, via
the program “Sanidad de Moluscos Bivalvos”. Within the
framework of this program, several toxic outbreaks have been
detected in the main aquaculture sites located in northern
Chile: Bahía Inglesa (27°7′S; 70°52′W, Atacama region), Bahía
Impactsofharmfulalgalbloomsontheaquacultureindustry 3
Guanaqueros (30°11′S; 71°25′W, Coquimbo region), and Bahía
Tongoy (30°15′S; 71°20′W, Coquimbo region) (Fig. 1).
2.1 ASP outbreaks
Due to their high frequency and recurrence, the most impor-
tant toxic episodes have been those caused by the presence
of domoic acid (DA), the toxin responsible for amnesic
shellsh poisoning (ASP). DA is produced by the diatoms
Pseudo-nitzschia australis and Pseudo-nitzschia callian-
tha. At least one event per year in Bahía Guanaqueros and
two events per year in Bahía Inglesa and Bahía Tongoy have
been documented. In some cases, the DA concentration
exceeded the regulatory limit (20 mg kg−1) and the harvest-
ing of scallops from aquaculture sites was therefore banned
(Suárez-Isla et al. 2002; Álvarez et al. 2009a; López-
Rivera et al. 2009). The longest and most intense ASP out-
break detected thus far was in Bahía Inglesa (Fig. 2A), in
the austral spring of 2006. On November 2, 2006, P. aus-
tralis reached a maximum concentration of 1.6 × 106 cells
L−1 (80% of the total phytoplankton biomass), with a toxin
concentration of 103 mg kg−1 wet weight, the maximum
concentration of DA measured in scallops from this area.
However, as the P. australis concentration declined and a
non-toxic phytoplankton became available as food for the
scallop, depuration rapidly occurred. Based on a one-com-
partment model, the estimated depuration rate was 0.49
day−1, which is similar to the rates determined in other rap-
idly detoxifying bivalves, such as the mussels Mytilus edu-
lis (0.5–2 day−1) (Novaczek et al. 1992; Wohlgeschaen
et al. 1992; Kracker 1999; Mafra et al. 2010), M. califor-
Fig. 1. Geographic distribution of the main biotoxins detected along Chilean
coast. The regions most aected by HAB events in northern (Antofagasta,
Atacama and Coquimbo) and southern (Los Lagos, Aysén and Magallanes)
Chile are indicated in gray.
4 P.A.Díazetal.
nianus (0.3–0.5 day−1) (Whyte et al. 1995), M. gallopro-
vincialis (0.4–0.5 day−1) (Blanco et al. 2002), and Perna
canaliculus (2.0 day−1) (MacKenzie et al. 1993), the oys-
ter Crassostrea virginica (0.25–0.88 day−1) (Mafra et al.
2010), and the surf clam Mesodesma donacium (0.4 day−1)
(Álvarez et al. 2015). Therefore, the time in which scallops
are unsafe for consumers is usually very short (1–2 weeks)
and the economic losses caused by ASP outbreaks in the
aquaculture industry accordingly moderate.
2.2 PSP outbreaks
Other groups of toxins detected in scallops are saxitoxins
(STX), which cause paralytic shellsh poisoning (PSP) and
are mainly produced during blooms of Alexandrium species.
The rst known PSP episode at an aquaculture sites in north-
ern Chile occurred in the austral autumn of 2006, at Bahía
Mejillones (23°05′S; 70°29′W). During this event trace con-
centrations of PSP toxins were detected and included C2,
gonyautoxin 2 (GTX2), GTX3, and decarbamoylgonyau-
toxin 2 (dcGTX2). In addition, in the winter of 2006, two
further episodes were recorded, at Bahía Guanaqueros and
Bahía Tongoy. During both, PSP toxin levels were 27–34 µg
STX eq. 100 g−1, below the regulatory limit of 80 µg STX
eq. 100 g−1. The toxin prole was dominated by STX, GTX2,
and GTX3. To date, the causative agent of PSP in northern
Chile has not been conrmed. Indeed, the toxin proles and
environmental conditions at the three aquaculture sites dif-
fered greatly from those determined during Alexandrium
proliferations elsewhere in northern Chile, which were
attributed to the species characterized as A. cf. tamarense by
Álvarez et al. (2009b). The total amount of PSP toxins and
the relative proportions of their isoforms can vary depend-
ing on the Alexandrium strain and its response to a range of
biotic, abiotic, and intrinsic (genetic) factors (Stüken et al.
2015 and references therein). However, the recent recogni-
tion of cryptic Alexandrium species together with the estab-
lishment of new genetic groups and name assignments (John
et al. 2014; Fraga et al. 2015) has revealed that the dier-
ent PST proles could also be produced by dierent species
or genetic groups within the genus Alexandrium. Recently,
Salgado et al. (2012) unveiled some of this hidden diversity,
reporting the presence of Alexandrium ostenfeldii in Bahía
Guanaqueros and Bahía Tongoy, but to date the toxic prole
and toxin content of this species are unknown.
2.3 DSP outbreaks
Another group of toxic compounds found in A. purpuratus are
the lipophilic toxins responsible for diarrhetic shellsh poi-
Fig. 2. A) Density of Pseudo-nitzschia australis (cells L−1) and domoic acid (DA) concentra-
tions (mg kg−1) recorded in scallop samples from Bahía Inglesa (northern Chile) between
August and December 2006. B) DA concentrations (mg kg−1) recorded in Chilean blue mus-
sel samples collected from Vilupulli (southern Chile) between August and December 2000.
Impactsofharmfulalgalbloomsontheaquacultureindustry 5
soning (DSP) and produced by the dinoagellate Dinophysis
acuminata. Until 2015, the presence of these toxins was
monitored by means of a mouse bioassay. Between 2005
and 2006, several prolonged preventive closures of scallop
harvesting were declared due to the detection of D. acumi-
nata and, in a few cases, the positive results of DSP bioas-
says. This imposed serious economic problems in the scallop
industry, as demand could not be met. Moreover, there was
strong market price competition from Peru, which oered
massive production at lower cost (Molina et al. 2012). The
uncertainty of the mouse bioassay, including the possible
interference of other lipohilic toxins, together with the har-
vesting closures led to eorts to study the toxin proles of
both the involved lter feeders and toxic phytoplanktonic
organisms. The study of Blanco et al. (2007) showed that
both the D. acuminata and the shellsh samples analyzed
contained only non-diarrhetic pectenotoxins (PTX), not any
of the toxins of the okadaic acid (OA) group, the causative
agents of severe gastrointestinal intoxications that have
occurred in other places around the world (Reguera et al.
2014).
2.4 YTX-related disease outbreaks
Other lipophilic toxins detected in aquaculture sites
are yessotoxins (YTX). Their rst detection was in
Bahía Mejillones, during a bloom of the dinoagellate
Protoceratium reticulatum. Analyses of phytoplankton
samples dominated by this species revealed a maximum
YTX concentration of 0.4 pg cell−1. This episode was
associated with the massive mortality of cultured scal-
lops, mainly seed scallops (12 ± 2 mm in shell height).
The highest mortality coincided with the hypoxic con-
ditions detected before and after the bloom, suggesting
oxygen depletion as the main cause of mortality (Álvarez
et al. 2011). However, shellsh mass mortality in asso-
ciation with the presence of P. reticulatum were previ-
ously reported by Grindley and Nel (1970) and Horstman
(1981). In addition, Suzuki et al. (2005) demonstrated that
YTX injected into the adductor muscle can kill scallops.
Further research is needed to clarify the negative eects of
YTX on A. purpuratus and aquaculture activities. Álvarez
et al. (2016) reported a dense bloom of Gonyaulax taylorii
in Bahía Mejillones, where densities reached 1.4 × 105
cells L−1. Toxin analyses of phytoplankton net samples
revealed the presence of YTX and homo-YTX, at concen-
trations below 1 pg cell−1. This was the rst report of the
production of these toxins by this species, both in Chilean
waters and possibly worldwide. Despite the low toxin
concentration per cell in P. reticulatum and G. taylorii,
the detection of these YTX-producing species pointed out
the necessity to routinely monitor these species in order
to protect public health as well as the activities of scallop
producers.
Finally, the most recently detected lipophilic toxins in
northern Chile were azaspiracids (AZA). The rst report of
these compounds was in the surf clam Mesodesma donacium
and the clam Mulina edulis from Bahía Coquimbo, where
AZA-1 was present at low levels (Álvarez et al. 2010). In
the same period, López-Rivera et al. (2010) reported AZA-1
and AZA-2 concentrations below the regulatory limit of 160
µg kg−1 from Bahía Inglesa. Currently, Azadinium poporum
is the only known AZA producer, with AZA-1 as the sole
toxin in its prole (Tillmann et al. 2017). However, consider-
ing the dierences in the toxin proles of the aected shell-
sh and A. poporum, more than one species of Azadinium
or Amphidoma may be present in northern Chilean waters.
Additional research is needed to determine the other sources
of AZA and their possible negative impacts on aquaculture
activities.
3 HABs and their impacts in southern Chile
HABs of toxin-producing microalgae are recurrent events in
southern Chile, including in Patagonia (41–55°S), and are
mainly due to A. catenella, the dinoagellate associated with
PSP outbreaks (Guzmán et al. 2002; Molinet et al. 2003;
Díaz et al. 2014; Díaz et al. 2018); Dinophysis spp. (D. acuta
and D. acuminata), associated with lipophilic toxin produc-
tion (OA, dinophysistoxins (DTX), and PTX; (Díaz et al.
2011; Alves de Souza et al. 2014); P. reticulatum, associated
with the production of YTX (Alves de Souza et al. 2014);
and diatoms of the genus Pseudo-nitzschia (mainly P. aus-
tralis), associated with ASP production (Suárez-Isla et al.
2002).
3.1 ASP outbreaks
ASP events are recurrent in the inner sea of the Los Lagos
region, the site of > 95% of the national production of the
Chilean blue mussel Mytilus chilensis (annual mean of
25 × 104 mt). This important aquaculture industry – second
in Chile after salmon farming – is mostly concentrated in
the inland sea of Chiloé Island. Aquaculture of blue mus-
sels generates high value-added products for export, yield-
ing annual revenues close to US$100M. In 2016, production
surpassed 29 × 104 mt (Sernapesca 2016), positioning Chile
as one of the world leaders in mussel farming (FAO 2014).
However, in 2000, natural mussel banks at Chiloé Island
were closed for more than a month due to the detection in
shellsh of ASP toxin concentrations above the regulatory
limit. The presumably responsible species was P. australis,
although P. pseudodelicatissima was also present in some
areas. The intoxication and detoxication of mussels and
oysters with ASP toxins (DAs) is fast (4–6 days) (Suarez-
Isla et al. 2002). As shown in Fig. 2B, in only 5 days the
concentration of ASP toxins in scallops dropped to 30% of
the initial value, with total detoxication occurring in < 20
days. The rapid (1–2 weeks) kinetics of DA detoxication in
scallops from southern Chile resemble those determined dur-
ing ASP outbreaks in northern Chile (Fig. 2A).
6 P.A.Díazetal.
3.2 PSP outbreaks
The dinoagellate genus Alexandrium is one of the most
important plankton genera in the world, in terms of its
diversity, distribution, and impacts on socio-economics and
human health (Anderson et al. 2012). In southern Chile,
PSP outbreaks caused by A. catenella have been a recurring
problem since 1972 (Guzmán et al. 1975). Extremely intense
PSP outbreaks posing a major threat to public health and the
shing industry have been recorded in the Patagonian fjords
of the Magallanes and Aysén regions, while PSP outbreaks
in Los Lagos are only occasional. In the Aysén region, the
earliest records date back to 1992 (Muñoz et al. 1992) and
severe PSP outbreaks have been documented since 1995
(Molinet et al. 2003). However, historic records reveal the
occurrence of PSP events since the late 19th century, as in
1886 the aboriginal inhabitants of Patagonia (living close to
Ushuaia) were poisoned, in some cases lethally, by the con-
sumption of mussels and developed the characteristic symp-
toms of PSP toxin intoxication (Segers 1908). Likewise,
Peric (1985) determined that in 1894 nine aborigines living
on Navarino Island (Chilean Magellan region) died due to
the consumption of intoxicated bivalves. In recent decades,
PSP outbreaks have expanded northwards, consistent with
the northwards spread of A. catenella (Guzmán et al. 2002;
Molinet et al. 2003; Mardones et al. 2010; Hernández et al.
2016). During the 1970s, PSP events were restricted to the
Magallanes region (55°S) but during the last intense bloom
of A. catenella, in the late summer of 2016, PSP-aected
areas included the Valdivian coast (39°S) (Hernández et al.
2016).
The considerable interannual variability of PSP events,
with weak or no events at all in some years (Table 1), has
been attributed to large-scale climate variability (Moore
et al. 2009). The PSP events (max. of 107 × 103 STX eq.
100 g−1) recorded in Southern Chile have been severe
enough to cause signicant socio-economic impacts, due to
the prolonged closure of shellsh harvesting and the result-
ing decrease in bivalve catches in the Aysén region since
1995 (Fig. 3). PSP events of the same magnitude (127 × 103
STX eq. 100 g−1) have also been recorded by Benavides et al.
(1995) in the Beagle Channel, during an exceptional bloom
of A. catenella and by Guzmán et al. (2018) in the Aysén
Region who recorded a toxicity record in mussels (143 x 103
μg STX eq. 100 g−1) associated to intense bloom of the same
dinoagellate.
The most intense PSP events, in 1996, 1998, 2000, 2002,
2006, 2009, and 2016, were generated by intense blooms of
A. catenella that covered most of the northern Patagonian
coast and were characterized by maximum PSP toxin con-
centrations exceeding 105 µg STX eq. kg−1 (Guzmán et al.
2002; Molinet et al. 2003; Mardones et al. 2010; Molinet
et al. 2010; Díaz et al. 2014; Hernández et al. 2016; Díaz
et al. 2018). This situation led health authorities to enforce
shellsh harvesting closures over extensive geographic
areas (up to 500 km) and for very long periods (1–3 years).
Table 1. Maximum recorded levels of PSP (µg STX eq kg−1) in
shellsh in southern Chile (Aysén region) from 1996 to 2011.
Year PSP
(µg STX eq. 100−1)Sector Specie
1996 107.129 Puerto Aguirre Mytilus
chilensis
1997 1.080 Punta Lynch Aulacomya
ater
1998 99.742 Estero Quitralco Mytilus
chilensis
1999 1.428 Colonia grande Venus antiqua
2000 22.170 Punta Lynch Aulacomya
ater
2001 1.575 Colonia grande Venus antiqua
2002 22.698 Puerto Gala Mytilus
chilensis
2003 4.355 Melinka Gari solida
2004 840 Isla Vergara Gari solida
2005 776 Isla Ovalada Aulacomya
ater
2006 10.476 Canal Puquitin Aulacomya
ater
2007 4.611 Puerto Bonito Aulacomya
ater
2008 2.072 Isla San Andrés Aulacomya
ater
2009 21.541 Canal
Chacabuco
Aulacomya
ater
2010 2.607 Canal vicuña Aulacomya
ater
2011 1.088 Canal vicuña Aulacomya
ater
The socio-economic impacts on the local economies have
been severe. Figure 4 shows the accumulation/detoxication
time of PSP toxins in the ribbed mussel (Aulacomya atra) in
the Aysén region during the intense outbreaks of 1996 and
1998. The high concentrations reached during 1996 (28 000
µg/100 g) could not be detoxied (dened as declining to
< 80 µg/100 g) before the next event in 1998, suggesting
that the higher the toxicity values reached, the greater the
delay in re-opening the aected area for harvesting. During
2002, losses of US$ 100,000 per month, related to the ban
on artisan extraction, were reported, with sherman, divers,
and processing plants among the most strongly aected. In
2016, 1700 people were left unemployed because of HAB
events, due to the inactivity of the processing plants and the
ban on the harvesting of mussels (Cristian Segura, unpub-
lished data). In that year, the estimated economic losses were
close to US$2M, largely deriving from the decline in exports
as 190 mt of the highly economically valuable M. chilensis
could not be harvested.
Impactsofharmfulalgalbloomsontheaquacultureindustry 7
Fig. 3. Total annual artisanal catches (tonnes) of three bivalves species in the A) Aysén and
B) Los Lagos regions from 1980 to 2016. Asterisks indicate the occurrence of intense PSP
outbreaks in both regions; vertical dashed line shows the start of the PSP events in the
Aysén region.
Fig. 4. Accumulation/detoxication time of PSP in the ribbed
mussel (Aulacomya atra) in the Aysén region during the intense
HABs of 1996 and 1998.
3.3 DSP outbreaks
DSP outbreaks have been especially relevant in southern
Chile (Los Lagos, Aysén y Magallanes) since the 1990s,
with DSP events caused by endemic species of the genus
Dinophysis. Both D. acuta and D. acuminata pose important
threats to shellsh production, mainly of the Chilean blue
mussel M. chilensis but also other shellsh species. Records
of DSP events date back to 1970, when over 100 people suf-
fered severe gastrointestinal disorders after eating ribbed
mussels (Aulacomya atra) from Reloncaví Sound (Los Lagos
region). Contamination of the mussels was associated with
an intense bloom of D. acuta (Guzmán & Campodónico,
1975; Guzmán & Campodonico, 1978; Lembeye et al. 1993).
While the lipophilic toxins OA, DTX1, and PTX2 have been
detected in shellsh (mainly mytilids) from the Aysén region
(Lembeye et al. 1993; Zhao et al. 1993; Villarroel 2004),
the contribution of the respective toxin-producing species
to the toxin prole of shellsh from Aysén still needs to be
elucidated in single-cell toxin analyses. By contrast, only
PTX2 was detected in concentrates of a D. acuminata com-
plex from Reloncaví fjord (Goto et al. 2000) and in isolated
cells of D. cf. ovum (Blanco et al. 2007; Fux et al. 2011),
misidentied as D. acuminata (Reguera et al. 2014). DTX1
and PTX2 were detected in “passive samples” (SPATT res-
ins, MacKenzie et al. 2004) from Calbuco and Chiloé Island
(Pizarro et al. 2011) but the responsible toxin-producing spe-
cies were not identied.
3.4 YTX-related disease outbreaks
In recent years, blooms of YTX producers, such as the dino-
agellate P. reticulatum, have been an important source of
concern to the mussel industry in the Los Lagos region.
However, whether YTX pose a health threat is controversial
because they are toxic to mice via intraperitoneal injection
but not through oral administration. In fact, in some coun-
tries (e.g., Australia) YTX levels are no longer a matter of
regulatory interest. During the summer of 2009, a moder-
ate P. reticulatum bloom (2.2 × 103 cell L−1) correlated posi-
8 P.A.Díazetal.
tively with a moderate to high concentrations of YTX in
shellsh (51–496 ng g−1) and with plankton concentrates (3.2
ng L−1) in Reloncaví fjord, Los Lagos (Alves de Souza et al.
2014). More recently, in the summer of 2015, P. reticulatum
densities close to 12 × 103 cell L−1 were reported from
Bahía Huelmo, an important mussel cultivation area within
Reloncaví Sound. The presence of the dinoagellate was
associated with YTX concentrations above the regula-
tory level of 1 mg YTX eq. kg−1) and harvesting closures
were enforced (Miriam Seguel, unpublished data). Unlike
Dinophysis species, P. reticulatum has a benthic resting
stage that enables it to alternate between pelagic and benthic
habitats in response to environmental conditions. Finally, it
should also be noted that, given the detection of Gonyaulax
taylorii as a new YTX producer in northern Chile (Álvarez
et al. 2016), the presence of this species in the Los Lagos
inland sea cannot be ruled out.
3.5 Effects on salmon farming
In southern Chile, HABs have had serious eects on salmon
farming. This industry is located mainly in the regions of
Los Lagos, Aysén, and Magallanes, with resources worth
approximately US$4 billion (SalmonChile 2016).
HABs threaten the viability of cultured sh by sev-
eral mechanisms: i) respiratory dysfunction due either to
mechanical damage to the gill epithelium (Jones & Rhodes
1994) caused by the microalgae themselves, as demonstrated
in Leptocylindrus danicus and Chaetoceros convolutus, or
to the depletion of dissolved oxygen in the water column
following bacterial degradation; ii) the toxicity of dinoagel-
late neurotoxins (Van Deventer et al. 2012); iii) the oxidation
of cell membranes by ROS and PUFA produced by the sh
in response to the toxins (Marshall et al. 2003; Mardones
et al. 2015); and iv) the toxin-mediated disruption of osmo-
regulatory capacity (Aguilera et al. 2016) by Heterosigma
akashiwo, Chattonella spp., Pseudochattonella verruculosa,
A. catenella, and Karenia sp., among others.
In Chile, Lembeye and Campodónico (1984) were able
to attribute the presence of the dinoagellate Prorocentrum
micans to the death of farmed salmonids. However, the rst
HAB event with dramatic economic consequences occurred
in September 1988 and was caused by the microalga H.
akashiwo (Raphidophyceae). Since then, several HAB events
have aected the salmon industry to dierent degrees. During
an important outbreak in the summer of 2002, the presence
of A. catenella caused major losses for the salmon industry
(Clément et al. 2002; Molinet et al. 2003; Fuentes et al. 2008).
However, the most intense A. catenella event, in terms of cell
abundance and geographic coverage, was that at the end of
the spring of 2009, when dinoagellate concentrations of up
to 6,000 cells mL−1 were recorded over an area ranging from
the Aysén region (46°S) to the south of Chiloé Island (42°S) in
the Los Lagos region (Mardones et al. 2010). This HAB event
caused millions of dollars in losses to the regional aquaculture
industry and a serious public health problem.
An outbreak of Pseudochattonella cf. verruculosa
(Dictyochophyceae) in the summer of 2016 imposed impor-
tant economic losses at 45 Chilean salmon farms (Paredes
et al. 2016), with the death of 39,942 mt of sh (∼27 mil-
lion sh) (Clément et al. 2016). According to the Norwegian
Bank, the losses due to the 2016 HAB amounted to 18–20%
of the Chilean salmon production estimated for that year,
worth US$800M. Moreover, the decline in the supply of
Chilean salmon led to a globally signicant 25% increase in
salmon prices (FAO 2016), which in the US reached US$ 10
per kg by March 2016 (Miami). The sh losses could be
explained by the extreme climate conditions, the resulting
increment in radiative forcing, the occurrence in that year
of an El Niño event and its coincidence with the positive
phase of the Southern Annular Mode, and wind upwelling,
which together provided highly favourable conditions for
the proliferation of HAB species (Garreaud 2018; León-
Muñoz et al. 2018). The highest concentration of P. verrucu-
losa was recorded at Reloncaví fjord (Los Lagos), where
up to 29.9 × 106 cells L−1 were measured in March 2016
(Clément et al. 2016; Villanueva et al. 2016; León-Muñoz
et al. 2018). The scarce information on HABs of P. verrucu-
losa and other ichthyotoxie microalgal species that occur
in Chile highlights the need for studies on their ecophysio-
logical dynamics as well as their eects and mechanisms of
action on sh. During the March 2016 event, 5 000 tons of
dead salmon had to be dumped oshore. A short time later,
another intense HAB, in this case of the species A. catenella,
occurred in the area, which gave rise to a debate about a
possible link between the salmon discharge and the second
microalgal bloom. A study performed to answer this ques-
tion (Buschmann et al. 2016) concluded that the movement
of water and suspended material during and after the salmon
discharge was oriented oshore, not at Chiloé Island, where
the bloom occurred, and that the episodes were therefore not
linked. However, the report also advised the development
of alternative sh-disposal solutions or at least the design
of dumping sites spatially arranged so as to maximize dilu-
tion while minimizing the risk of the inshore transport of
the sh remains, given that the ammonium resulting from
sh decomposition may be used by microalgae to enhance
their own growth (Buschmann et al. 2016). The A. catenella
bloom was instead attributed to the same environmental
conditions described above for the P. verruculosa bloom:
the unusual simultaneous occurrence of conditions optimal
for algal growth, i.e., inorganic nutrient inputs from upwell-
ing conditions and heightened solar radiation (Garreaud
2018).
Recently, Villanueva et al. (2017) reported signicant mor-
talities of farmed salmon within well-boats in transit through
a Karenia bloom in the Golfo de Penas (47°S), the same area
where in the summer of 2015 the largest mass mortality of
baleen whales had occurred (Häussermann et al. 2017). The
deaths of at least 343 whales were attributed to the HABs that
developed during a build-up of an El Niño event.
Impactsofharmfulalgalbloomsontheaquacultureindustry 9
4. Future perspectives on Chilean HABs
Against a background of global climate change, the northern
expansion of PSP events related to the species A. catenella
will probably continue, with increases in both the geographic
extent and the intensity of the outbreaks. The predicted trend
is consistent with the trends at other latitudes. In fact, the
environmental cascade provoked by climate change in con-
junction with other related and non-related factors, such as
occasional drought, could induce a general upsurge in HAB
events, as suggested, for example, by the increasingly intense
blooms of Dinophysis in Chile during the last several years
(Díaz et al. 2018). Additionally, further studies may reveal
new toxin proles, as current knowledge of the dierent
microalgal populations blooming in the area is incomplete at
both the genetic and the physiological level. Consequently,
“toxicity maps” of northern and southern Chile remain to be
completed and correctly interpreted.
Conclusions
• HAB events are increasingly causing serious harm to
economic sectors related to the exploitation of coastal
resources (shellsh culture and sh farming) in Chile,
where the number of HAB events associated with the
dinoagellates A. catenella and D. acuta and the diatom
P. australis, has increased during last decade. Of particu-
lar interest are PSP outbreaks, which have intensied
and moved northwards. These trends have had a serious
impact both in northern Chile, where shellsh, especially
scallops, is the most highly exploited resource, and in the
south, the home of Chile’s salmon farming and aquacul-
ture mussel industries.
• Ecient management strategies should be aimed at
minimizing the related socio-economic costs. Thus, they
should be accurate, appropriate for the aected area, and
fast-acting. Moreover, they must be based on detailed
knowledge of the biology of the causative species and of
the means by which it negatively impacts the exploited
resources. The ability to forecast HABs requires elucida-
tion of the mechanisms that trigger these events in areas
where they were previously absent. These mechanisms
likely include the movement of resting stages by ballast
waters, coastal eutrophication, and the local conditions
induced by climate change.
• The continuous emergence of new information on caus-
ative species (such as P. verruculosa in southern Chile)
but the lack of understanding of the relationship between
the detection of some toxins and the mass mortalities of
aquaculture species urges for more research into how
HAB events impact aquaculture. This will allow for more
accurate predictions of HABs and the management of
their consequences.
Acknowledgements: Gonzalo Álvarez and Patricio A. Díaz were
funded by the Chilean National Commission for Scientic and
Technological Research (CONICYT + PAI/CONCURSO
NACIONAL INSERCION EN LA ACADEMIA CONVOCATORIA
2015, 79150008 (G. Álvarez), CONVOCATORIA 2016, 79160065
(P.A. Díaz)). Rosa I. Figueroa is funded by FORMAS (Sweden).
Iván Pérez-Santos is funded by COPAS Sur-Austral AFB170006.
This work was funded by the CONICYT – FONDECYT Grant
11170682 and supported by REDI170575 from the International
Cooperation Programme of the CONICYT.
References
Aguilera, A., Gutiérrez, X., Mayorga, J., Villanueva, F. & Varela, D.
(2016): Eects of Alexandrium catenella on Atlantic salmon
post smolt. Abstract book 17th International Conference on
Harmful Algae, Brazil, p. 145.
Álvarez, G., Uribe, E., Ávalos, P., Mariño, C. & Blanco, J. (2010):
First identication of azaspiracid and spirolides in Mesodesma
donacium and Mulinia edulis from Northern Chile. − Toxicon
55: 638–641.
Álvarez, G., Uribe, E., Díaz, R., Braun, M., Mariño, C. & Blanco,
J. (2011): Bloom of the yessotoxin producing dinoagellate
Protoceratium reticulatum (Dinophyceae) in northern Chile. −
J. Sea Res. 65: 427–434.
Álvarez, G., Uribe, E., Quijano-Scheggia, S., López-Rivera, A.,
Mariño, C., Blanco, J., Gonzalo, A., Blanco, J. & Marin, C.
(2009a): Domoic acid production by Pseudo-nitzschia australis
and Pseudo-nitzschia calliantha isolated from North Chile. −
Harmful Algae 8: 938–945.
Álvarez, G., Uribe, E., Regueiro, J., Blanco, J. & Fraga, S. (2016):
Gonyaulax taylorii, a new yessotoxins-producer dinoagellate
species from Chilean waters. − Harmful Algae 58: 8–15.
Álvarez, G., Uribe, E., Regueiro, J., Martin, H., Gajardo, T., Jara, L.
& Blanco, J. (2015): Depuration and anatomical distribution of
domoic acid in the surf clam Mesodesma donacium. − Toxicon
102: 1–7.
Álvarez, G., Uribe, E., Vidal, A., Ávalos, P., González, F., Mariño,
C. & Blanco, J. (2009b): Paralytic shellsh toxins in Argopecten
purpuratus and Semimytilus algosus from northern Chile. −
Aquat. Living Resour. 22: 341–347.
Alves de Souza, C., Varela, D., Contreras, C., de la Iglesia, P.,
Fernández, P., Hipp, B., Hernández, C., Riobó, P., Reguera, B.,
Franco, J.M., Diogene, J., García, C. & Lagos, N. (2014):
Seasonal variability of Dinophysis spp. and Protoceratium retic-
ulatum associated to lipophilic shellsh toxins in a strongly
stratied Chilean fjord. − Deep Sea Res. II 101: 152–162.
Anderson, D.M. (2014): HABs in a changing world: a perspective
on harmful algal blooms, their impacts, and research and man-
agement in a dynamic era of climactic and environmental
change. − In H. G. Kim, Reguera B., Hallegrae G., Lee C. K.,
Han M. S., Choi J. K. (eds.), Harmful Algae 2012, Proceedings
of the 15th International Conference on Harmful Algae,
International Society for the Study of Harmful Algae (2014).
ISBN 978-87-990827-4-2, 16 pp.
Anderson, D.M., Alpermann, T.J., Cembella, A., Collos, Y.,
Masseret, E. & Montresor, M. (2012): The globally distributed
genus Alexandrium: Multifaceted roles in marine ecosystems
and impacts on human health. − Harmful Algae 14: 10–35.
10 P.A.Díazetal.
Avendaño, R. & Cantillanes, M. (1996): Efectos de la pesca clan-
destina, sobre Argopecten purpuratus (Lamarck, 1819) en el
banco de la Rinconada, II Región, Chile. − Cienc. Tecnol. Mar.
19: 57–65.
Benavides, H., Prado, L., Díaz, S. & Carreto, J.I. (1995): An excep-
tional bloom of Alexandrium catenella in the Beagle Channel,
Argentina. – In: P. Lassus, Arzul G., Erard E., Gentien P.,
Marcailloe C. (eds.), Harmful Marine Algal Blooms. Lavoisier
Publishers, Paris, pp. 113–119.
Berdalet, E., Fleming, L.E., Gowen, R., Davidson, K., Hess, P.,
Backer, L.C., Moore, S.K., Hoagland, P. & Enevoldsen, H.
(2015): Marine harmful algal blooms, human health and wellbe-
ing: challenges and opportunities in the 21st century. − J. Mar.
Biol. Ass. U.K. 96: 61–91.
Blanco, J., Álvarez, G. & Uribe, E. (2007): Identication of pec-
tenotoxins in plankton, lter feeders, and isolated cells of a
Dinophysis acuminata with an atypical toxin prole, from
Chile. − Toxicon 49: 710–716.
Blanco, J., Bermúdez de la Puente, M., Arévalo, F., Salgado, C. &
Moroño, A. (2002): Depuration of mussels (Mytilus gallopro-
vincialis) contaminated with domoic acid. − Aquat. Living
Resour. 15: 53–60.
Buschmann, A., Farías, L., Tapia, F., Varela, D. & Vásquez, M.
(2016): Scientic report on the 2016 southern Chile red tide.
Chilean Department of Economy. p. 66.
Clément, A., Aguilera, A. & Fuentes, C. (2002): Análisis de la
Marea Roja en el Archipiélago de Chiloé, Contingencia verano
2002. − Edition ed. Universidad Austral de Chile.
Clément, A., Lincoqueo, L., Saldivia, M., Brito, C.G., Muñoz, F.,
Fernández, C., Pérez, F., Maluje, C.P., Correa, N., Mondaca, V.
& Contreras, G. (2016): Exceptional summer conditions and
HABs of Pseudochattonella in southern Chile create record
impacts on salmon farm. − Harmful Algae News 53: 1–3.
Díaz, P., Molinet, C., Cáceres, M. & Valle-Levinson, A. (2011):
Seasonal and intratidal distribution of Dinophysis spp in a
Chilean fjord. − Harmful Algae 10: 155–164.
Díaz, P.A., Molinet, C., Seguel, M., Díaz, M., Labra, G. & Figueroa,
R. (2014): Coupling planktonic and benthic shifts during a
bloom of Alexandrium catenella in southern Chile: Implications
for bloom dynamics and recurrence. − Harmful Algae 40: 9–22.
Díaz, P.A., Molinet, C., Seguel, M., Díaz, M., Labra, G. & Figueroa,
R.I. (2018): Species diversity and abundance of dinoagellate
resting cysts seven months after a bloom of Alexandrium
catenella in two contrasting coastal systems of the Chilean
Inland Sea. − Eur. J. Phycol.: DOI: 10.1080/09670262.0967201
8.01455111.
Díaz, P.A., Pérez-Santos, I., Baldrich, A., Montero, P., Igor, G.,
Daneri, G., Seguel, M., Álvarez, G., Guzmán, L., Pizarro, G.,
Norambuena, L., Mardones, J.I., Carbonell, P., Rodríguez, F.,
Reguera, B. (2018): An exceptional summer bloom of
Dinophysis acuta in a Chilean fjord. The 18th International
Conference on Harmful Algae, 21–26 October, Nantes, France.
Disalvo, L., Alarcón, E., Martínez, E. & Uribe, E. (1984): Progress
in mass culture of Chlamys (Argopecten) purpurata Lamarck
(1819) with notes on its natural history. − Rev. Chil. Hist. Nat.
57: 35–45.
FAO (2004): Marine Biotoxin. Food and Agriculture Organization
of the United Nations, Rome, Italy.
FAO (2014): The state of world sheries and aquaculture. FAO
Fisheries and Aquaculture Department, Rome, Italy.
FAO (2016): GLOBEFISH – Analysis and information on world
sh trade.
Fraga, S., Sampedro, N., Larsen, J., Moestrup, Ø. & Calado, A.J.
(2015): Arguments against the proposal 2302 by John et al. to
reject the name Gonyaulax catenella (Alexandrium catenella). −
Taxon 64: 634–635.
Fuentes, C., Clement, A. & Aguilera, A. (2008): Summer
Alexandrium catenella bloom and the impact on sh farming, in
the XI Aysén region, Chile. – In: O. Moustrup, Doucette G.,
Enevoldsen H., Godhe A., Hallegrae G., Luckas B., Lundholm
N., Lewis J., Rengefors K., Sellner K., Steidinger K., Tester P. &
Zingone A. (eds.), Book Summer Alexandrium catenella bloom
and the impact on sh farming en the XI Aysén region, Chile.
pp. 183–186.
Fux, E., Smith, J.L., Tong, M., Guzmán, L. & Anderson, D.M.
(2011): Toxin proles of ve geographical isolates of Dinophysis
spp. from North and South America. − Toxicon 57: 275–287.
Garreaud, R. (2018): Record-breaking climate anomalies lead to
severe drought and environmental disruption in western
Patagonia in 2016. − Climate Research 74: 217–229.
Glibert, P.M., Allen, J.I., Artioli, Y., Beusen, A., Bouwman, L.,
Harle, J., Holmes, R. & Holt, J. (2014): Vulnerability of coastal
ecosystems to changes in harmful algal blooms distribution in
response e to climate change: projections based on model analy-
sis. − Glob. Change Biol. 20: 3845–3858.
Gobler, C.J., Doherty, O.M., Hattenrath-Lehmann, T.K., Grith,
A.W., Kang, Y. & Litaker, R.W. (2017): Ocean warming since
1982 has expanded the niche of toxic algal blooms in the North
Atlantic and North Pacic oceans. − Proc. Natl. Acad. Sci. USA
114: 4975–4980.
Goto, H., Igarashi, T., Watai, M., Yasumoto, T., Villarroel, O.,
Lembeye, G., Noren, F., Gisselson, G. & Graneli, E. (2001):
Worldwide occurrence of Pectenotoxins and Yessotoxins in
shellsh and phytoplankton. – In: Hallegrae, G.M., Blackburn,
S.I., Bolch, C.J. & Lewis, R.J. (eds.), Proceedings of the IX
International Conference on Harmful Alga Blooms, Hobart,
Tasmania, Australia, 7–11 February 2000. Intergovernmental
Oceanographic Commission. UNESCO, Paris, 49 pp.
Grindley, J.R. & Nel, E.A. (1970): Red water and mussel poisoning
at Elands Bay, December 1966. − Fish. Bull. South Africa:
36–55.
Guzmán, L. & Campodonico, I. (1978): Mareas rojas en Chile. −
Interciencia 3: 144–151.
Guzmán, L. & Campodónico, I. (1975): Marea roja en la región de
Magallanes. − Publ. Inst. Pat. Ser. Mon. 9: 44.
Guzmán, L., Campodonico, I. & Antunovic, M. (1975): Estudios
sobre un orecimiento toxico causado por Gonyaulax catenella
en Magallanes. IV. Distribución y niveles de veneno paralítico
de los mariscos (noviembre de 1972 – noviembre de 1973). −
An. Inst. Patagon. 6: 209–223.
Guzmán, L., Espinoza–González, O., Pinilla, E., Besoaín, V.,
Calderón, M.J., Cáceres, J., Iriarte, L., Muñoz, V., Martínez, R.,
Hernández, C., Tocornal, M.A., Carbonell, P. (2018):
Atmospheric and oceanographic processes on the distribution
and abundance of Alexandrium catenella in the North of Chilean
fjords. The 18th International Conference on Harmful Algae,
Nantes – France 21–26 October 2018, p. 37.
Guzmán, L., Pacheco, H., Pizarro, G. & Alárcon, C. (2002):
Alexandrium catenella y veneno paralizante de los mariscos en
Chile. – In: Sar, E.A., Ferrario, M.E. & Reguera, B. (eds.),
Impactsofharmfulalgalbloomsontheaquacultureindustry 11
Floraciones Algales Nocivas en el Cono Sur Americano.
Instituto Español de Oceanografía, Madrid, pp. 235–255.
Hallegrae, G. (2003): Harmful algal bloom: a global overview. –
In: Hallegrae, G., Anderson, D.M. & Cembella, A.D. (eds.),
Manual on Harmful Marine Microalgae. Monographs on
Oceanographic Methodology. UNESCO Publishing., France,
pp. 25–50.
Hallegrae, G. (2010): Ocean climate change, phytoplankton com-
munity responses, and harmful algal blooms: a formidable pre-
dictive challenge. − J. Phycol. 46: 220–235.
Hallegrae, G.M. (1993): A review of harmful algal blooms and
their apparent global increase. − Phycologia 32: 79–99.
Häussermann, V., Gutstein, C.S., Bedington, M., Cassis, D.,
Olavarria, C., Dale, A.C., Valenzuela-Toro, A.M., Perez-
Alvarez, M.J., Sepúlveda, H.H., McConnell, K.M., Horwitz,
F.E. & Försterra, G. (2017): Largest baleen whale mass mortal-
ity during strong El Niño event is likely related to harmful toxic
algal bloom. − PeerJ 5: e3123 https://doi.org/10.7717/peerj.
3123.
Heisler, J., Glibert, P.M., Burkholder, J.M., Anderson, D.M.,
Cochlan, W., Dennison, W.C., Dortch, Q., Gobler, C.J., Heil,
C.A., Humphries, E., Lewitus, A., Magnien, R., Marshall, H.G.,
Sellner, K., Stockwell, D.A., Soecker, D.K. & Suddleson, M.
(2008): Eutrophication and harmful algal blooms: A scientic
consensus. − Harmful Algae 8: 3–13.
Hernández, C., Díaz, P.A., Molinet, C. & Seguel, M. (2016):
Exceptional climate anomalies and northwards expansion of
Paralytic Shellsh Poisoning outbreaks in Southern Chile. −
Harmful Algae News 54: 1–2.
Hishamunda, N., Bueno, P., Menezes, A.M., Ridler, N., Wattage, P.
& Martone, E. (2014): Improving governance in aquaculture
employment: a global assessment. FAO Fisheries and
Aquaculture Technical Paper No. 575, Rome, FAO.
Horstman, D.A. (1981): Reported red-water outbreaks and their
eects on fauna of the west and south coasts of South Africa,
1959–1980. − Fish. Bull. South Africa 15: 71–88.
Illanes, J.E. & Akaboshi, S. (1983): Estudio experimental sobre la
captación, precultivo y cultivo en ambiente natural de Chlamys
(Argopecten) purpurata, Lamarck 1819, en Bahía Tongoy, IV
Región,Coquimbo. – In: Symposium Internacional: Avances y
perspectivas de la acuacultura en Chile. pp. 233–254.
INE 2009. Instituto Nacional de Estadísticas (INE). Estadísticas de
Remuneraciones.
John, U., Litaker, R.W., Montresor, M., Murray, S., Brosnahan,
M.L. & Anderson, D.M. (2014): Formal Revision of the
Alexandrium tamarense Species Complex (Dinophyceae)
Taxonomy: The Introduction of Five Species with Emphasis on
Molecular-based (rDNA) Classication. − Protist 165:
799–804.
Jones, B. & Rhodes, L. (1994): Suocation of pilchards (Sardinops
sagax) by a green microalgal bloom in Wellington Harbour,
New Zealand. − N.Z.J. Mar. Freshwater Res. 28: 379–383.
Kracker, L. (1999): The Geography of Fish: the use of remote sens-
ing and spatial analysis tools in sheries research. − The
Professional Geographer 51: 440–450.
Lembeye, G. & Campodónico, I. (1984): First record bloom of the
dinofagellate Prorocentrum micans Ehr. in South-Central
Chile. − Bot. Mar. 27: 491–493.
Lembeye, G., Yasumoto, T., Zhao, J. & Fernández, R. (1993): DSP
outbreak in Chilean ords. – In: Smayda, T.J. & Shimizu, Y.
(eds.), Toxic Phytoplankton Blooms in the Sea. Elsevier,
Amsterdam, pp. 525–529.
León-Muñoz, J., Urbina, M.A., Garreaud, R. & Iriarte, J.L. (2018):
Hydroclimatic conditions trigger record harmful algal bloom in
western Patagonia (summer 2016). − Scientic Reports 8:
1330.
López-Rivera, A., O’Callaghan, K., Moriarty, M., O’Driscoll, D.,
Hamilton, B., Lehane, M., James, K.J.J., Furey, A., O’Callaghan,
K., Moriarty, M., O’Driscoll, D., Hamilton, B., Lehane, M.,
James, K.J.J. & Furey, A. (2010): First evidence of azaspiracids
(AZAs): A family of lipophilic polyether marine toxins in scal-
lops (Argopecten purpuratus) and mussels (Mytilus chilensis)
collected in two regions of Chile. − Toxicon 55: 692–701.
López-Rivera, A., Pinto, M., Insinilla, A., Suarez-Isla, B.A., Uribe,
E., Álvarez, G., Lehane, M., Furey, A. & James, K.J. (2009):
The occurrence of domoic acid linked to a toxic diatom bloom
in a new potential vector: The tunicate Pyura chilensis (piure). −
Toxicon 54: 754–762.
MacKenzie, L., Beuzenberg, V., Holland, P., McNabb, P. &
Selwood, A.I. (2004): Solid phase adsorption toxin tracking
(sPATT): a new monitoring tool that simulates the biotoxin con-
tamination of lter feeding bivalves. − Toxicon 44: 901–918.
MacKenzie, L., White, D.A., Sim, P.G., Holland, A.J., MacKenzie,
A., White, D.A., Sim, P.G. & Holland, A.J. (1993): Domoic acid
and the New Zealand greenshell mussel (Perna canaliculus). –
In: Smayda, T.J. & Shimizu, Y. (eds.), Toxic Phytoplankton
Blooms in the Sea. Elsevier, Amsterdam, pp. 607–612.
Mafra, L.L., Bricelj, V.M. & Fennel, K. (2010): Domoic acid uptake
and elimination kinetics in oysters and mussels in relation to
body size and anatomical distribution of toxin. − Aquat. Toxicol.:
17–29.
Mardones, J., Clément, A., Rojas, X. & Aparicio, C. (2010):
Alexandrium catenella during 2009 in Chilean waters, and
recent expansion to coastal ocean. − Harmful Algae News 41:
8–9.
Mardones, J.I., Dorantes-Aranda, J.J., Nichols, P.D. & Hallegrae,
G.M. (2015): Fish gill damage by the dinoagellate Alexandrium
catenella from Chilean fjords: Synergistic action of ROS and
PUFA. − Harmful Algae 49: 40–49.
Marshall, J., Nichols, P., Hamilton, B., Lewis, R. & Hallegrae, G.
(2003): Ichthyotoxicity of Chattonella marina (Raphidophyceae)
to damselsh (Acanthochromis polycanthus): the synergistic
role of reactive oxygen species and free fatty acids. − Harmful
Algae 2: 273–281.
Masó, M., Garcés, E. (2006): Harmful microalgae blooms (HAB);
problematic and conditions that induce them. − Mar. Pollut.
Bull. 53: 620–660.
Moestrup, Ø., Akselman, R., Cronberg, G., Elbraechter, M., Fraga,
S., Halim, Y., Hansen, G., Hoppenrath, M., Larsen, J., Lundholm,
N., Nguyen, L.N. & Zingone, A. (2009): IOC-UNESCO
Taxonomic Reference List of Harmful Micro Algae. Accessed at
http://www.marinespecies.org/hab on 2015-04-20
Molina, R., Cerda, R., González, E. & Hurtado, F. (2012):
Simulation model of the scallop (Argopecten purpuratus) farm-
ing in northern Chile: Some applications in the decision making
process. − Latin Am. J. Aquat. Res. 40: 679–693.
Molinet, C., Lafón A., Lembeye, G., Moreno, C.A. (2003): Patrones
de distribución espacial y temporal de oraciones de
Alexandrium catenella (Whedon & Kofoid) Balech 1985, en
aguas interiores de la Patagonia noroccidental de Chile. − Rev.
Chil. Hist. Nat. 76: 681–698.
12 P.A.Díazetal.
Molinet, C., Niklitschek, E., Seguel, M. & Díaz, P. (2010): Trends
of natural accumulation and detoxifcation of paralytic shellsh
poison in two bivalves from the Northwest Patagonian inland
sea. − Rev. Biol. Mar. Ocenog. 45: 195–204.
Moore, S., Mantua, N., Hickey, B. & Trainer, V. (2009): Recent
trends in paralytic shellsh toxins in Puget Sound, relationships
to climate, and capacity for prediction of toxic events. − Harmful
Algae 8: 463–477.
Muñoz, P., Avaria, S., Sievers, H. & Prado, R. (1992): Presencia de
dinoagelados toxicos del genero Dinophysis en el seno Aysén,
Chile. − Rev. Biol. Mar. 27: 187–212.
Novaczek, I., Madhyastha, M.S., Ablett, R.F., Anderson, D.M.,
Johnson, G., Nijjar, M.S. & Sims, D.E. (1992): Depuration of
domoic acid from live blue mussels (Mytilus edulis). − Can. J.
Fish. Aquat. Sci. 49: 312–318.
Paredes, J., Aguilera-Belmonte, A., Olivares, B., Uribe, C., Urrutia,
G., Seguel, M., Villanueva, F., Vargas, M. & Varela, D.
(2016): Morphological variability and genetic identication of
ichthyotoxic species Pseudochattonella sp. isolated from severe
outbreak in 2016 at the Northern Patagonian Fjord, southern
Chile. – Conference Poster.
Peric, J. (1985): Extinción indígena en la Patagonia. Hersaprint,
Punta Arenas.
Pinto, F. (2007): Salmonicultura Chilena: Entre el éxito comercial y
la insustentabilidad. RPP 23. Santiago, Terram. 93 p.
Pizarro, G., Alarcón, C., Franco, J.M., Palma, M., Escalera, L.,
Reguera, B., Vidal, G. & Guzmán, L. (2011): Distribución espa-
cial de Dinophysis spp. y detección de toxinas DSP en el agua
mediante resinas DIAION (verano 2006, Región de Los Lagos,
Chile). − Cienc. Tecnol. Mar. 34: 31–48.
Reguera, B., Riobó, P., Rodríguez, F., Díaz, P.A., Pizarro, G., Paz,
B., Franco, J.M. & Blanco, J. (2014): Dinophysis toxins: caus-
ative organisms, distribution and fate in shellsh. − Mar. Drugs
12: 394–461.
Salgado, P., Díaz, L., Pesse, N., Vivanco, X. & Guzmán, L. (2012):
Monitoreo de Alexandrium catenella en zona no declarada de la
región de Atacama y Coquimbo. Informe Final Convenio –
Asesoria Integral para la toma de decisiones en pesca y acuicul-
tura. 41 p.
Segers, P.A. (1908): Primera observación de una causa nueva de
enfermedad del hígado causando una hipertroa y cirrosis con-
secutivas por excesividad funcional, debido a absorción de toxi-
nas, y primera observación de esplenomegalia concomitante con
hipertroa de bazo en estas afecciones. − La Semana Médica
(Buenos Aires) 20: 117–119.
Sernapesca (2016): Anuario Estadistico de Pesca.
Stüken, A., Riobó, P., Franco, J., Jakobsen, K.S., Guillou, L. &
Figueroa, R.I. (2015): Paralytic shellsh toxin content is related
to genomic sxtA4 copy number in Alexandrium minutum
strains. − Frontiers in Microbiology 6: 404.
Suárez-Isla, B.A., López-Rivera, A., Hernández, C., Clément, A.,
Guzmán, L., 2002. Impacto económico de las oraciones de
microalgas nocivas en Chile y datos recientes sobre la ocurren-
cia de veneno amnésico de los mariscos. – In: Sar, E., Ferrario,
M.E., Reguera, B. (eds.), Floraciones Algales Nocivas En El
Cono Sur Americano. Instituto Español de Oceanografía, pp.
257–268.
Suzuki, T., Igarashi, T., Ichimi, K., Watai, M., Suzuki, M., Ogiso, E.
& Yasumoto, T. (2005): Kinetics of diarrhetic shellsh poison-
ing toxins, Okadaic acid, Dinophysistoxin-1, Pectenotoxin-6
and Yessotoxin in scallops Patinopecten yessoensis. − Fish. Sci.
71: 948–955.
Thiel, M., Macaya, E.C., Acuña, E., Arntz, W.E., Bastias, H.,
Brokordt, K. (....) et al. (2007): The Humboldt Current System
of northern and central Chile. − Oceanogr. Mar. Biol. Annu.
Rev. 45: 195–344.
Tillmann, U., Trefault, N., Krock, B., Parada-Pozo, G., De la
Iglesia, R. & Vásquez, M. (2017): Identication of Azadinium
poporum (Dinophyceae) in the Southeast Pacic: Morphology,
molecular phylogeny, and azaspiracid prole characterization. −
J. Plankton Res. 39: 350–367.
Uriarte, I., Rupp, G. & Abarca, A. (2001): Producción de juveniles
de pectínidos iberoamericanos bajo condiciones controladas. –
In: Maeda-Martínez, A.N. (ed.), Los Moluscos Pectínidos de
Iberoamérica: Ciencia y Acuicultura. McGraw-Hill Inter-
americana Editores S.A, La Paz, Mexico, pp. 147–171.
Van Deventer, M., Atwood, K., Vargo, G.A., Flewelling, L.J.,
Landsberg, J.H., Naar, J.P. & Stanek, D. (2012): Karenia brevis
red tides and brevetoxin-contaminated sh: a high risk factor for
Florida’s scavenging shorebirds? − Bot. Mar. 55: 31–37.
van Egmond, H.P. (2004): Natural toxins: risks, regulations and the
analytical situation in Europe. − Anal. Bioanal. Chem. 378:
1152–1160.
Villanueva, F., Cortez, H., Uribe, C., Peña, P. & Cassis, D. (2017):
Mortality of Chilean farmed salmon in wellboats in transit
through a Karenia bloom. − Harmful Algae News 57: 4–5.
Villanueva, F., Urrutia, G., Uribe, C., Seguel, M., Aguilera-
Belmonte, A., Olivares, B., Varela, D. & Paredes, J. (2016):
Harmful Algal Bloom of Pseudochattonella verruculosa
(Dictyochophyceae, Florenciellales) associated with salmon
farm mortalities in the South of Chile. – Conference poster.
Villarroel, O. (2004): Detección de toxina paralizante, diarreica y
amnésica en mariscos de la XI región por Cromatografía de Alta
Resolución (HPLC) y bioensayo de ratón. − Cienc. Tecnol. Mar.
27: 33–42.
von Brand, E., Abarca, A., Merino, G.E.G.E. & Stotz, W. (2016):
Scallop shery and aquaculture in Chile: A history of develop-
ments and declines. − Dev. Aquac. Fish. Sci. 40: 1047–1072.
Whyte, J.N.C., Ginther, N.G., Townsend, T.D. (1995): Accumulation
and depuration of domoic acid by the mussel, Mytilus califor-
nianus. – In: Lassus, P., Arzul, G., Erard, E., Gentien, P.,
Marcaillou, C. (eds.), Harmful Marine Algal Blooms. Lavoisier
Sci. Publ., París, France, pp. 531–537.
Wohlgeschaen, G.D., Mann, K.H., Subba Rao, D.V. & Pocklington,
R. (1992): Dynamics of the phycotoxin domoic acid: accumula-
tion and excretion in two commercially important bivalves. − J.
Appl. Physiol. 4: 297–310.
Zhao, J., Lembeye, G., Cenci, G., Wall, B. & Yasumoto, T. (1993):
Determination of okadaic acid and dinophysistoxin-1 in mussels
from Chile, Italy and Ireland. – In: Smayda, T.J. & Shimizu, Y.
(eds.), Toxic Phytoplankton Blooms in the Sea. Elsevier,
Amsterdam, pp. 587–592.
Zingone, A. & Enevoldsen, H.O. (2000): The diversity of harmful
algal blooms: a challenge for science and management. − Ocean
Coast. Manag. 43: 725–748.
Manuscript received: 01.12.2017
Revisions required: 29.01.2018
Revised version received: 15.06.2018
Accepted for publication: 09.01.2019
Handling editor: Alejandro H. Buschman