Impacts of harmful algal blooms on the aquaculture industry: Chile as a case study

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 shellfish poisoning. They therefore threaten the sustainable exploitation of bivalves, including in northern and southern Chile, sites of intensive shellfish aquaculture but also recurrent HABs. Exceptionally large blooms of the genera Pseudochattonella and Karenia recently occurred in the Patagonian fjords, leading to high fish 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 shellfish poisoning and other hazardous events in the region and elsewhere.

Full text

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 CentrodeInvestigaciónOceanográcoCOPASSur-Austral,UniversidaddeConcepción,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 CentroOceanográcodeVigo,InstitutoEspañoldeOceanografía(IEO),SubidaaRadioFaro50,36390
Vigo, Spain
11 Aquatic Ecology, Biology Building, Lund University, 22362 Lund, Sweden
* Corresponding author: patricio.diaz@ulagos.cl
With4guresand1table
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 shellsh poisoning. They therefore threaten
the sustainable exploitation of bivalves, including in northern and southern Chile, sites of intensive shellsh 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 shellsh poisoning and other hazardous events in the region and elsewhere.
Keywords: HAB-causing species; Shellsh 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 aect 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.Díazetal.
sic shellsh poisoning, and thus pose an important threat to
public health and shellsh exploitations; iii) species that are
not toxic to humans but aect 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
identied 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 shellsh 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 shellsh harvesting.
This in turn causes dramatic eects on the aquaculture indus-
try and the exploitation of natural shellsh banks. During
extreme toxic events, the consumption of illegally obtained
shellsh has resulted in the deaths of the consumers.
In recent decades, new scientic and technological knowl-
edge in parallel with the rapid development of aquaculture
has resulted in the detection of new HAB species in dier-
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 aected, and the frequency and inten-
sity of the blooms, the losses suered 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 shellsh 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 indenite 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 eort, 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, certication systems to ensure
the safety of cultured molluscan shellsh 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

Impactsofharmfulalgalbloomsontheaquacultureindustry 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
shellsh 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; Wohlgeschaen
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 aected by HAB events in northern (Antofagasta,
Atacama and Coquimbo) and southern (Los Lagos, Aysén and Magallanes)
Chile are indicated in gray.

4 P.A.Díazetal.
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 shellsh 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 prole was dominated by STX, GTX2,
and GTX3. To date, the causative agent of PSP in northern
Chile has not been conrmed. Indeed, the toxin proles 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 dier-
ent PST proles could also be produced by dierent 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 prole
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 shellsh 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.

Impactsofharmfulalgalbloomsontheaquacultureindustry 5
soning (DSP) and produced by the dinoagellate 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 oered
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 eorts to study the toxin proles 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 shellsh 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 dinoagellate
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, shellsh 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 eects 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 prole (Tillmann et al. 2017). However, consider-
ing the dierences in the toxin proles of the aected 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 dinoagellate 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
shellsh 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 detoxication 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 detoxication occurring in < 20
days. The rapid (1–2 weeks) kinetics of DA detoxication in
scallops from southern Chile resemble those determined dur-
ing ASP outbreaks in northern Chile (Fig. 2A).

6 P.A.Díazetal.
3.2 PSP outbreaks
The dinoagellate 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-aected
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 signicant socio-economic impacts, due to
the prolonged closure of shellsh 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
dinoagellate.
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
shellsh 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
shellsh 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/detoxication
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 detoxied (dened 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 aected 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 aected. 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.

Impactsofharmfulalgalbloomsontheaquacultureindustry 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/detoxication 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 shellsh production, mainly of the Chilean blue
mussel M. chilensis but also other shellsh 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 shellsh (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 prole of shellsh 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),
misidentied 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 identied.
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.Díazetal.
tively with a moderate to high concentrations of YTX in
shellsh (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 dinoagellate 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 eects 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 dinoagel-
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 dinoagellate 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 aected the salmon industry to dierent 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 dinoagellate 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$800M. Moreover, the decline in the supply of
Chilean salmon led to a globally signicant 25% increase in
salmon prices (FAO 2016), which in the US reached US$ 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 eects and mechanisms of
action on sh. During the March 2016 event, 5 000 tons of
dead salmon had to be dumped oshore. 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 oshore, 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 signicant 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.

Impactsofharmfulalgalbloomsontheaquacultureindustry 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 proles, as current knowledge of the dierent
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 (shellsh culture and sh farming) in Chile,
where the number of HAB events associated with the
dinoagellates A. catenella and D. acuta and the diatom
P. australis, has increased during last decade. Of particu-
lar interest are PSP outbreaks, which have intensied
and moved northwards. These trends have had a serious
impact both in northern Chile, where shellsh, especially
scallops, is the most highly exploited resource, and in the
south, the home of Chile’s salmon farming and aquacul-
ture mussel industries.
• Ecient management strategies should be aimed at
minimizing the related socio-economic costs. Thus, they
should be accurate, appropriate for the aected 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 Scientic 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.
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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