Cig 4

Environmental Research 182 (2020) 109111
Contents lists available at ScienceDirect
Environmental Research
journal homepage: www.elsevier.com/locate/envres
Review article
Global impact of ciguatoxins and ciguatera fish poisoning on fish, fisheries T

and consumers
Lucía Soliñoa,b,∗, Pedro Reis Costaa,b
a
IPMA - Instituto Português do Mar da Atmosfera, Rua Alfredo Magalhães Ramalho, 6, 1495-006, Lisbon, Portugal
b
CCMAR – Centre of Marine Sciences, University of Algarve, Campus of Gambelas, 8005-139, Faro, Portugal
A R T I C LE I N FO A B S T R A C T
Keywords: Ciguatera fish poisoning (CFP) is one of the most devastating food-borne illnesses caused by fish consumption.
Food safety Ciguatoxins (CTXs) are potent neurotoxins synthesized by the benthic microalgae Gambierdiscus spp. and
Harmful algal blooms Fukuyoa spp. that are transmitted to fish by grazing and predation. Despite the high incidence of CFP, affecting
Marine food web an estimated number of 50,000 persons per year in tropical and subtropical latitudes, the factors underlying
Seafood
CTXs occurrence are still not well understood. Toxin transfer and dynamics in fish and food-webs are complex.
Toxic microalgae
Feeding habits and metabolic pathways determine the toxin profile and toxicity of fish, and migratory species
Gambierdiscus
may transport and spread the hazard. Furthermore, CTX effect on fish may be a limiting factor for fish re-
cruitment and toxin prevalence. Recently, new occurrences of Gambierdiscus spp. in temperate areas have been
concomitant with the detection of toxic fish and CFP incidents in non-endemic areas. CFP cases in Europe have
led to implementation of monitoring programs and fisheries restrictions with considerable impact on local
economies. More than 400 species of fish can be vectors of CTXs, and most of them are high-valued commercial
species. Thus, the risk uncertainty and the spread of Gambierdiscus have serious consequences for fisheries and
food safety. Here, we present a critical review of CTXs impacts on fish, fisheries, and humans, based on the
current knowledge on CFP incidence and CTXs prevalence in microalgae and fish.
1. Introduction frequent in the Atlantic endemic regions (Boada et al. 2010; Hossen
et al. 2015). Indian CFP causes typical CFP traits that can be accom-
Ciguatera fish poisoning (CFP) is a human food-borne illness caused panied with hallucinations, mental depression, and nightmares (Quod
by consumption of fisheries products harboring ciguatoxins (CTXs). and Turquet, 1996).
CTXs are natural compounds produced by the epi-benthic dinoflagellate CTXs enter the marine food web via herbivorous fish or benthic
genus Gambierdiscus and Fukuyoa (Bagnis et al. 1980; Litaker et al. invertebrates that feed on macroalgae where Gambierdiscus or Fukuyoa
2009; Gómez et al. 2015). These toxins are heat stable and highly li- cells are settled on. Most of these organisms are important diet com-
pophilic polycyclic ether compounds, which bind competitively to ponents of carnivorous species, and toxins are accumulated and bio-
voltage-gated sodium and potassium channels with different potencies transformed in fish top predators (Mak et al. 2013a, b). A wide range of
(Dechraoui et al. 1999, 2006; Yasumoto et al., 1977; Schlumberger fish species with different feeding habits, substantially differing in size
et al. 2010). This interference causes cell disturbances, with gastric, and in life span, have been implicated in CFP, especially in tropical and
neurological, and cardiovascular disorders in humans, which can last subtropical areas (Chinain et al. 2019). Fish is the dietary basis and
for several months and recur with the consumption of fish, alcohol, or represents an important economic sector in most of these endemic re-
tobacco (Friedman et al. 2008, 2017). Despite of the diversity of gions, where CFP affects more than 50,000 persons per year (Lewis
symptoms, the most characteristic sign of CFP is the inversion of et al. 1986; Lehane and Lewis, 2000). Groupers, snappers, and jacks are
thermal perception (alodynia) together with paresthesia, fatigue, ar- some of the groups of fish under bans or restrictions owing to their
ticular and muscular pain, vomits, and diarrhea (Friedman et al. 2017). elevated CTXs accumulation capability (Prefect de la Région Prefect de
Regional differences have been also observed, with neurological la region de Guadeloupe, 2002; US Department of Health and Human
symptoms being usually predominant and persistent over gastric dis- Services, 2011; Governo Regional da Madeira, 2016; Gobierno de
turbances in the Pacific (Wong et al. 2014), while gastric symptoms are Canarias, 2018). The lack of effective methods to detect CTXs in the
∗
Corresponding author. IPMA - Instituto Português do Mar da Atmosfera, Rua Alfredo Magalhães Ramalho, 6, 1495-006, Lisbon, Portugal.
E-mail address: [email protected] (L. Soliño).
https://doi.org/10.1016/j.envres.2020.109111
Received 1 October 2019; Received in revised form 31 December 2019; Accepted 1 January 2020
Available online 07 January 2020
0013-9351/ © 2020 Elsevier Inc. All rights reserved.
L. Soliño and P.R. Costa Environmental Research 182 (2020) 109111
Fig. 1. Chemical structure of the main ciguatoxins (CTXs): a) CTX1B representative of Pacific CTX I (oxopene group) b) CTX3C representative of Pacific CTX II
(oxocene group) and c) C-CTX-1 representative of Caribbean CTX (adapted from Soliño and Costa, 2018).
field and the uncertainty about the occurrence of toxins cause im- et al. 2018). Although CTX-producing algae have been identified in the
portant economic losses every year around the world (Richlen et al. Mediterranean Sea, no confirmed CFP incidents have been confirmed
2012; Rongo and Van Woesik, 2012; Morin et al. 2016). nor CTX has been detected in fish (Raikhlin-Eisenkraft and Bentur,
Geographical toxin profiles have been recognized and associated 2002; Bentur and Spanier, 2007). Contrastingly, several human out-
with the Pacific and Indian Ocean or the Caribbean Sea, leading to the breaks have been reported in the Canary and Madeira islands. In most
denomination of P-, I-, and C-CTXs, respectively (Vernoux and Lewis, of these cases, amberjacks (Seriola rivoliana and Seriola dumerili) and
1997). Although still in use, this nomenclature does not accurately groupers (Epinephelus spp.) were associated with the outbreaks (Pérez-
describe CTX diversity, which can be structurally divided in three kinds Arellano et al., 2005; Gouveia et al. 2009; Nuñez et al. 2012; Otero
of molecules: the oxopene (CTX1B type), the oxocene (CTX3C type), et al. 2010; Caillaud et al. 2012; Gobierno de Canarias, 2019).
and Caribbean/Indian CTXs structures (Scheuer et al. 1967; Satake Although CFP was well known in endemic European overseas ter-
et al. 1993; Lewis et al. 1998; Hamilton et al. 2002a,b; Soliño and Costa, ritories, such as The French Indies and French Polynesia, the emerging
2018). The first two are usually related to fish and microalgae from the risk of CFP in Europe has led the EU Member States to jointly develop
Pacific Ocean, while C- and I-CTXs have not been confirmed in mi- and validate detection methods and monitoring programs. However,
croalgae. C- and I-CTXs share the same molecular formula, although I- CTXs occurrence in these new areas is still not well assessed, which
CTXs structure has not yet been elucidated. C-CTXs differ from the hinders the establishment of effective regulations that can guarantee
Pacific analogues, having an extra ring in their backbone (Fig. 1). They food safety without compromising fishing industry.
also differ in potency, with a derivative only found in Pacific fish This review intends to provide a general overview of CFP impact to
(CTX1B) being one of the most toxic analogues. Therefore, toxicity fisheries and fish consumption worldwide, with special interest in re-
equivalency factors (TEFs) suggested by the European Food Safety cently affected European regions.
Authority (EFSA) were assigned after CTX1B (TEF = 1). The TEFs for
CTX-2 and -3 are both 0.3. TEF is 0.2 for CTX3C, and 0.1 and 1 for its
analogues 2,3-dihydroxy CTX3C and 51-hydroxy CTX3C, respectively. 2. Brief overview of historical records
C-CTX-1 was assigned a TEF value of 0.1. These values were measured
by acute toxicity tests via intraperitoneal injection in mice (Lewis et al. The first historical records of CFP outbreaks date back to antiquity.
1991; EFSA 2010). CFP was cited in Homer's Odyssey and even Alexander the Great for-
Recently, the spread of CTX-producing organisms has extended to bade his army to eat fish to avoid the harmful effects of this food-borne
temperate areas, including the coasts of Europe. Gambierdiscus and illness (Hokama and Yoshikawa-Ebesu, 2001). CFP could be the cause
Fukuyoa populations have been identified in the Mediterranean Sea of ancient migrations undertaken by Polynesian islanders to conquer
(Cyprus, Crete, Malta, and Balearic islands) and in Atlantic islands of new and safer fishing areas (Rongo et al. 2009). Historical documents
Portugal and Spain, namely Madeira and Canary archipelagos, respec- suggest that expedition crews in the West Indies suffered CFP in-
tively (Aligizaki and Nikolaidis, 2008; Fraga et al. 2011; Kaufmann and toxications since 1606 (de Quiros expedition in 1606 and Captain Cook
Böhm-Beck, 2013; Laza-Martínez et al. 2016; Reverté et al. 2018; Tudó expedition in 1774). Moreover, CFP became a serious problem for
military troops in endemic islands during World War II (Withers, 1982;
2
Hokama and Yoshikawa-Ebesu, 2001). (Lewis, 1986; Skinner et al. 2011).

For centuries, the causes of this food-borne illness remained un- The Cook Islands, with an incidence of 1437 per 100,000 persons-
known and the population of tropical areas relied on traditional year during the period 1998–2008, have also experienced a remarkable
knowledge and remedies to avoid or diminish the symptoms (Bourdy increase of CFP cases compared with previous surveys that estimated a
et al. 1992). Then, the hypothesis of toxin transfer through a vector rate of only one case per 100,000 persons-year. The same trend was
organism was suggested, in which herbivorous fish might accumulate observed in Marshall Islands, Vanuatu Niue, Fiji, Tonga, and Palau in
the toxin through diet and transfer it to their predators (Randall, 1958; the mentioned periods (Fig. 2a and b) (Lewis, 1986; Skinner et al.
Banner, 1976). Almost two decades after this first hypothesis, a dino- 2011).
flagellate was identified as the primary causative organism of CFP. First The total health-related costs for an individual with CFP was esti-
identified as Diplopsalis sp. and later renamed Gambierdiscus toxicus, the mated to be NZD $2090 (USD $1396.62) in Rarotonga (Cook Islands)
highly toxic species from French Polynesia may correspond today to G. and an estimation of approximately NZD $396,000 (USD $264,623.04)
polynesiensis, while other G. toxicus have been reassigned to other was calculated considering the non-reported cases for the year 2011
Gambierdiscus and Fukuyoa species (Adachi and Fukuyo, 1979; Bagnis (Rongo and van Woesik, 2011; Rongo et al. 2012). The increase of CFP
et al. 1980; Litaker et al. 2009). The increasing list of Gambierdiscus and in this island, which is the most populated of the archipelago, certainly
Fukuyoa species includes 24 species and ribotypes up to date (Litaker has tremendous social and economic impact.
et al. 2009; Fraga and Rodríguez, 2014; Murray et al. 2014: Fraga et al. In French Polynesia, a rate of annual incidence ranging from 263 to
2016; Smith et al. 2016; Dai et al. 2017; Kretzschmar et al. 2017; 419 per 100,000 persons-year was estimated in the totality of the
Rhodes et al. 2017; Jang et al. 2018), and 37 CTX analogues have been Polynesian territory over the decade 1992–2001, with similar results
identified in microalgae and fish (Scheuer et al. 1967; Murata et al. for the period between 1998 and 2008 (Chateau-Degat et al. 2007a;
1990; Lewis et al. 1991, 1998; Satake et al. 1993, 1997, 1998; Skinner et al. 2011).
Yasumoto et al. 2000; Hamilton et al. 2002a,b; Diogène et al. 2017), A recent study in Moorea (Society Archipelago) estimated the
although only a few have been successfully synthesized and are com- health-related cost caused by CFP in the island at USD $1613 for each
mercially available as analytical standards (Hirama et al. 2001; Inoue reported case. Taking into account under-reported cases and expenses
et al. 2002). related to loss of productive days, the total cost for the year 2011
reached USD $80,078 (Morin et al. 2016).
3. Geographical distribution of CFP and incidence Kiribati Islands, with an estimate rate of 324 and 313 per 100,000
persons-year in the period 1973–1983 and 1998–2008, respectively, are
Ciguatera is a pervasive food-borne illness that affects fish-con- the next most affected areas, having a constant incidence in time
sumers worldwide and causes enormous expenses in social security and (Fig. 2b) (Lewis, 1986; Skinner et al. 2011). Moreover, North Marianas,
insurance (Todd, 1985; Rongo et al. 2012; Morin et al. 2016). Ciguatera Guam, and Samoa showed a constant incidence along the studied per-
has been reported in the Pacific, Atlantic, and Indian Ocean displaying iods (Fig. 2a and b) (Skinner et al. 2011). Contrastingly, Hawaii, New
a distribution between 35° N and 35° S. Global fish trade and high Caledonia, and Tuvalu have experienced a clear decrease of reported
tourist affluence to tropical areas contribute to increase the risk of CFP cases. The incidence of 203 per 100,000persons-year calculated for
for consumers in temperate countries (Slobbe et al. 2008; Schlaich et al. 1975–1981 for Hawaii (Lewis, 1986) dropped to only 3.24 during
2012; Mattei et al. 2014; Zimmermann et al., 2015; Friedemann, 2016, 1998–2008 (Fig. 2a and b). New Caledonia, with an incidence rate of
2019). around 200 per 100,000 inhabitants-year in 1973–1983, was among the
Furthermore, Gambierdiscus distribution has expanded to higher most ciguateric areas in the Pacific, but a rate of only nine cases was
latitudes (Ishikawa and Kurashima, 2010; Kuno et al. 2010; Jeong et al. calculated in the latest period. In Tuvalu, incidence also decreased from
2012; Nishimura et al. 2013; Kohli et al. 2014; Zhang et al. 2016) and 439 to 84 cases per 100,000 inhabitants-year during the mentioned
into new areas of the East Atlantic (Fraga et al. 2011; Kaufmann and periods (Lewis, 1986; Skinner et al. 2011).
Böhm-Beck, 2013; Reverté et al. 2018), the Mediterranean islands In Australia, poisoning by ciguatera is almost exclusively recorded
(Aligizaki and Nikolaidis, 2008; Laza-Martínez et al. 2016; Tudó et al. in Queensland (Fig. 2b), but surveillance data may represent only a
2018), and the Arabian sea and Gulf of Bengal (Naik et al. 2011; small fraction of the total incidence. The median number of hospitali-
Saburova et al. 2013). This fact may be related to global warming and zations caused by CFP in 2010 accounted at least for 25 cases (Kirk
sea surface temperature increase, and may pose a new issue in terms of et al. 2014). The incidence calculated for the period 1965–1984 was 30
food safety and fisheries management in these areas. (Tosteson et al., cases per 100,000 persons-year (Gillespie et al. 1986). Recent episodes
1988; Hales et al. 1999; Chateau-Degat et al. 2005; Tester et al. 2010). of CFP in New South Wales may point to an expansion of the syndrome
CFP incidence is difficult to estimate and depends on demographical to southern areas (Farrel et al. 2016; 2017; Murray et al. 2016).
and temporal factors. The officially recorded cases are estimated to be In Japan, the most affected area is Okinawa Prefecture (Fig. 2a). In
only 20% of the actual cases of CFP (Lehane and Lewis 2000; Rongo and 1997–2006, the overall annual incidence was 0.77 per 100,000 persons.
van Woesik, 2011; Skinner et al., 2011). Fish consumption habits and Annual incidences of around 1 per 100,000 population were reported
lack of protein source alternatives in coastal areas and small oceanic for Hong Kong (1989–2008) and other regions of East Asia and
islands may increase the risk of poisoning. Moreover, disturbances such Southeast Asia (Chan, 2015a,b).
as hurricanes and human alterations can also favor blooms of Gam- The only report available for the Indian Ocean indicates an annual
bierdiscus and increase the number of CFP incidents (Kohler and Kohler, incidence of 7.8 per 100,000 persons in Réunion Island in 1986–1994
1992; Quod et al. 2000, 2006; Rongo and van Woesik, 2011; Skinner (Quod and Turquet, 1996).
et al. 2011; Morin et al. 2016). Several researchers have employed re- In the Atlantic Ocean, CFP has only been reported in the Northern
cords in medical care systems and surveys to construct the complex hemisphere. An annual impact of 5.6 per 100,000 persons was esti-
picture of CFP in areas of the Pacific Ocean and the Caribbean Sea. mated in Florida (Fig. 2c) (Radke et al. 2015), while in the Caribbean,
In the Pacific, CFP incidence varies greatly among islands. The the highest incidence rates occur in Virgin Islands, Guadeloupe Island,
trends observed in early and recent studies are also diverse, showing a Montserrat, Antigua and Barbuda, and Culebra. In the US Virgin Islands
tendency to decrease in certain islands while others have experienced a a rate of 1200 affected persons per year and 100,000 inhabitants was
clear increase (Fig. 2a and b). CFP case records in 1973–1983 and estimated between 1980 and 2000 (Radke et al. 2013). In Montserrat,
1998–2008 in the Pacific reflected the highest number of victims in the Antigua and Barbuda, and British Virgin Islands these rates per 100,000
isolated Tokelau Island, with an occurrence rate of 653 and 1576 per persons varied between 586 and 199 per year from 1996 to 2006
100,000 persons-year during these periods, respectively (Fig. 2b) (Tester et al. 2010). In Iles Saintes (Guadeloupe), 300 per 100,000
3
Fig. 2. Geographical distribution of ciguatera fish poisoning incidence. The colors reflect the incidence rate (100,000 persons-year). Location names indicate the
spots where Gambierdiscus spp. were reported. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this
article.)
4
persons-year were poisoned in the period 1960–1980 (Czernichow et al. endemic CFP areas usually try to avoid eating it (Darius et al. 2013).
1984), although recent studies have recorded much lower incidence in Nevertheless, this issue has seldom been addressed and more research is
Guadeloupe (Tester et al. 2010; Boucaud-Maitre et al. 2018). In the case needed to confirm if certain species are more prone than others to
of Puerto Rico (Culebra Island), the number of patients per 100,000 differentially accumulate the toxin throughout the body or in different
inhabitants-year was 750 during 2002–2004 (Fig. 2c), which resulted in muscle types (i.e.,red muscle versus white muscle).
an indirect cost of USD $164.80 per episode (Azziz-Baumgartner et al. CTXs concentration is usually higher in viscera (particularly in the
2012). With a population size of 1868 permanent residents on Culebra liver) than in muscle. However, toxin concentration ratios between the
Island, the reported incidence means that around 15 persons would liver or viscera and flesh vary among species, suggesting that toxins are
develop ciguatera every year, which corresponds to almost 1% of the differently stored in different fish species.
population (Azziz-Baumgartner et al. 2012). This percentage is similar The liver of moray eels seems to have the greatest storing capacity,
to that found in the US Virgin Islands (Radke et al. 2013) and is similar reaching more than one hundred times the CTXs concentration found in
or higher than the estimations for certain areas in the Pacific Ocean muscle (Gymnothorax funebris) (Chan, 2017). Groupers (Mycteroperca
(e.g., Tokelau) (Lewis, 1986; Skinner et al. 2011). This fact is surprising venenosa, Epinephelus morio) and great amberjack (Seriola dumerili) from
considering that highly toxic dinoflagellate species, like G. polynesiensis the Caribbean also seem to have great CTXs accumulation capability in
have not been found in the Caribbean and that the toxic potency of the liver, with CTXs concentrations more than 10 times higher than
Caribbean CTXs found in Atlantic fish is one order of magnitude lower those in muscle (Vernoux et al. 1985).
than those usually found in the Pacific (EFSA 2010). Interestingly, To a lesser extent, mackerels, like Scomberomorus commerson from
Florida, holding a highly toxic Gambierdiscus excentricus producing the Pacific and Scomberomorus cavalla inthe Caribbean showed toxin
around 469 fg CTX3C eq cell−1 (Litaker et al. 2017), maintains a re- levels in the liver around 6 and 9 times higher than that in muscle,
latively low CFP incidence. This suggests that underlying factors other respectively (Vernoux et al. 1985; Kohli et al. 2017). Parrotfish may
than toxicity in microalgae and fish are behind the real impact of CFP in also accumulate CTXs differentially in muscle and liver (Chungue et al.,
an area. These factors may be related to fish consumption frequency, 1977; Satake et al. 1996). In laboratory studies, mullet Mugil cephalus
habits of consumers, population awareness, or the effectiveness of exposed to a single dose of G. polynesiensis spiked meal was found to
fisheries management and monitoring (Goater et al. 2010). contain high CTX-like activity (measured by cell based assay) in muscle,
Despite the relatively low CFP incidence in the US, health costs of liver, and blood after 3 h of exposure (with a ratio liver:muscle of 9.92)
approximately USD $17 million annually have been ranking CFP in the (Ledreux et al. 2014).
top five of the costliest food-borne illnesses in this country (Ralston Blood analysis is an interesting approach, as monitoring living an-
et al. 2011; Minor et al. 2015). imals would give information on the occurrence and dynamics of toxins
In Europe, where CTXs are considered an emerging threat, the in- in the ecosystem in a non-invasive way (O'Toole et al. 2012; Mak et al.
cidence calculated since the year when CFP episodes were first reported 2013a).
(2004), are 0.46 and 2.3 cases per 100,000 inhabitants and year in
Canary Islands and Madeira, respectively (Fig. 2d) (Gobierno de 4.2. Correlation with size
Canarias, 2019; Gouveia, personal communication). Monitoring pro-
grams and epidemiological surveys are in an initial phase and the real The food chain hypothesis, first stated by Randall (1958), led to the
incidence is believed to exceed these official figures. In Madeira, it has general assumption that bigger individuals within the same species are
been observed that the complete banon selling Seriola spp. ≥10 kg has likely to contain higher amounts of CTXs. The need for developing
not decreased the cases of ciguatera but the reported cases of ciguatera strategies to distinguish safer fish by consumers and to manage fisheries
because of the fear of recriminations. by local governments have fostered the spread of this assumption
without a supporting scientific basis. The relationship between toxicity
4. CTX dynamics and accumulation in fish and fish size has been demonstrated for a very limited number of spe-
cies. A nine-year survey in French Polynesia involving 856 fishes be-
Fish frequently exposed to natural toxins such as CTXs, may have longing to 59 species from 12 different families has been the most ex-
developed mechanisms that allow them to tolerate and harbor these tensive study focused on this topic up to date. This investigation found
compounds for long periods of time. Physiological mechanisms, such as no correlation between CTX concentration and fish total length, except
toxin storage in certain organs or rapid depuration to reduce the for one species, Lutjanus bohar, sampled in one of the studied islands,
bioavailability of the toxin may occur in fish to avoid damage (Uno Fakarava Island (Gaboriau et al. 2014). Similarly, the correlation be-
et al. 2012; Luckenbach et al. 2014; Ikehara et al. 2017). Genetic tween the rate of toxic fish and body length was not significant for any
adaptations associated to feeding habits and prey type are another of the 43 studied species. The proportion of toxic individuals even de-
possible explanation, but probably a complex combination of all these creased with increasing size in Epinephelus polyphekadion and Kyphosus
factors models CTXs dynamicsin marine food webs. cinerascens (Gaboriau et al. 2014).Equally, no correlation was found
between toxicity and total length or weight in peacock grouper (Ce-
4.1. Fish tissue distribution phalopholis argus) in Kiribati or between toxicity and weight in the same
species from Hawaii (Bienfang et al. 2012; Mak et al. 2013b). Moreover,
CTXs distribution in fish tissues has been poorly investigated, and no relationship was found between total length and CTX levels in bar-
frequently the only tissues targeted for toxin detection are the muscle racuda (Sphyraena barracuda) or lionfish (Pterois spp.) from the Car-
and the viscera. The few studies separately considering internal organs ibbean (O'Toole et al. 2012; Soliño et al. 2015). This relationship was
detected CTXs in an array of fish organs, i.e., muscle, intestine, gills, not found either for amberjacks S. rivoliana and S. dumerili in the Ma-
stomach, gall bladder, liver, and spleen, as well as blood, gonads, heart, caronesia or S. dumerili from Hawaii (Kimura et al. 1982; Caillaud et al.
skin, and bones (Vernoux et al. 1985; Ledreux et al. 2014). 2012).
According to the available data, CTX concentration is uniform Contrastingly, a positive relationship was observed between CTX
throughout the flesh (Vernoux et al. 1982, 1985; Otero et al. 2010). concentration in the muscle and liver of moray eels (Gymnothorax spp.)
However, poisoning surveys have observed that patients that consumed and their weight in individuals collected in Marakei and Tarawa, South
the fish head or jaw muscle developed more severe illnesses than those Pacific Ocean (Chan et al. 2011). The same relationship was found
who ingested only the body muscle (Oshiro et al. 2010; Chateau-Degat between total length or body weight and CTXs concentrations in giant
et al. 2007b; Copeland et al. 2014). According to popular belief, fish moray (Gymnothorax javanicus) also caught in the Kiribati Islands (Mak
head is more likely to contain CTXs, and native population from et al. 2013b).
5
A weak significant correlation was found in C. argus in Hawaii be- -3, and further oxidized compounds. Furthermore, CTX3 produced 2-
tween toxicity and length but not with fish condition index. However, hydroxyCTX3C, 2,3-dihydroxyCTX3C, and 52-hydroxyCTX3C (Ikehara
mean CTXs concentration differed significantly between sites (Dierking et al. 2017). Although this study was only tested with carnivorous and
and Campora, 2009). omnivorous fish liver, it is expected that herbivorous fish will also have
Contradicting results were obtained in French Polynesia, a positive some biotransformation capabilities.
relationship between the ratio of toxic individuals and fish body weight Contrastingly, Caribbean and Indian CTX oxidized products do not
of Lutjanus bohar, Lutjanus monostigma, Epinephelus fuscoguttatus, and lead to more toxic compounds. These oxidized products are more polar,
Variola louti was found in samples from Okinawa, Japan, (Oshiro et al. which contradicts the bioactivation through foodweb hypothesis
2010). Moreover, higher frequency of toxic specimens was found in (Pottier et al. 2002a,b; Hamilton et al. 2002a,b; Estevez et al. 2019).
heavier individuals of amberjacks (Seriola spp.) and dusky grouper However, while 29 CTX1B and CTX3C congeners have been elucidated
(Epinephelus marginatus) from the Canary Islands (Sanchez-Henao et al. in microalgae and fish, in the case of C-/I-CTXs the list is substantially
2019). shorter, with two and six congeners for Caribbean and Indian toxins,
Therefore, according to the present knowledge, we can only pos- respectively. Many congeners may remain unknown and likely con-
tulate that the relationship between CTXs content or percentage of toxic tribute to the total toxicity. Accordingly, total toxicity arises from the
fish and fish weight/length may be positive for Gymnothorax spp., L. relative amount of each analogue and their relative potency, being
bohar, and C. argus (significant relationship found in more than one these factors highly variable among fish species and CTX-producing
study). This is disturbing considering that many legal regulations and algae species. Metabolism, feeding strategy, and site-fidelity behavior
recommendations apply fish length as a threshold to monitor or avoid eventually model the characteristic toxin profile and toxin contents,
ciguateric fish. Nevertheless, field data reporting higher toxicity in leading to risky ciguateric species. This is in agreement with CTX de-
smaller individuals and data obtained after fish challenging experi- rivatives found in other regions, although with variation in analogue
ments in laboratory suggest CTXs somatic growth dilution (Caillaud ratios (Wong et al. 2014; Yogi et al. 2011, 2013; 2014; Soliño and
et al. 2012; Gaboriau et al. 2014; Clausing et al. 2018). Therefore, slow- Costa, 2018).
growing fish may have higher CTXs concentrations than fast-growing
ones. These results may indicate that the toxin quantity found in certain 5. Impact to fisheries and fish consumption
species may be related with site-fidelity, age, and growth rate rather
than fish weight or length (Sanchez-Henao et al. 2019). Fish are an important nutritional and gastronomic resource and
fishing is an important activity for subsistence and commerce.
4.3. Correlation with trophic level Recreational fishing also represents a common sport and a tourist at-
traction. However, CFP is a double threat for fisheries. First, the risk of
The relationship between CTXs accumulation and trophic level was food-borne illness may lead to customers refraining from eating fish,
suggested by the observation that most toxic and oxidized CTXs com- with the consequent reduction of fish sells. Secondly, the direct effect of
pounds were usually detected in omnivorous and carnivorous fish. CTXs toxins on fish may cause a decrease on larvae recruitment or higher
lipophilic nature and their ability to accumulate in tissues make them mortality rates for adult fish. In coral reef ecosystems, diverse species
easily transferred through marine food webs and bioaccumulated in top are harvested by commercial and small-scale fisheries. The latter often
predators. Traditional knowledge and several research studies indicate represents the predominant fishery, employing a wide range of tradi-
that omnivorous and piscivorous fish are the most ciguateric species. tional and advanced fishing techniques, and it is important for the li-
A high number of fish and invertebrate samples from different velihoods of millions of people (Salas et al. 2007; Garcia and
trophic levels were collected in Marakei and analyzed for Pacific CTX Rosenberg, 2010). Common fish species landed by artisanal and re-
analogues, namely CTX1B and CTX-2 and 3 (Mak et al. 2013b), recreational fishing include snappers (Lutjanidae), surgeonfishes and
vealing a weak correlation between trophic level and CTX1B content, unicornfishes (Acanthuridae), parrotfishes (Labridae), emperor breams
measured by δ15N isotopes. CTXs were detected in 54%, 72%, and 76% (Lethrinidae), and groupers (Epinephelidae), among others. These fa-
of herbivorous, omnivorous, and carnivorous fishes, respectively (Mak milies include numerous high-risk CFP species. More than 400 species
et al. 2013b). The dominant toxin type in grazers and herbivorous fish of fish can act as vectors of CTXs (Gillespie et al. 1986), and the recent
was CTX-2, and in piscivorous fish CTX1B. For example, the studied spread of CFP-causing dinoflagellates into temperate areas suggests this
species of parrotfish and surgeonfish showed a significantly higher CTX- already long list will increase.
2 and CTX-3 content than that of CTX1B (Mak et al. 2013b). Con-
trastingly, it seems that top predators with a varied diet such as ce- 5.1. Effects of CTX to fish
phalopods and crustaceans have more chances to contain elevated
contents of CTX1B as well as CTX-2/-3 in variable ratios (Anyperodon The issue of whether or not CTXs affect fish behavior or health re-
leucogrammicus, Plectropomus laevis, L. monostigma). Species like C. mains unclear. It has been hypothesized that certain levels of CTXs may
argus, E. fuscoguttatus, E. polyphekadion, G. flavimarginatus, and L. bohar, be lethal to fish as an explanation for the low levels of CTXs found in the
feeding mainly on fish, cephalopods, and crustaceans, contained CTX1B environment (Lewis and Holmes, 1993). This theory is supported by
levels higher than those of other CTX analogues. However, total toxicity several authors that found severe signs of toxicity in adult fish by dis-
may depend on a mixture of different factors, such as feeding rate and solved toxin exposure or toxin intake (Table 1). Exposure to Caribbean
capability of toxin storage and clearance. In fact, high frequency of and Pacific CTXs results in developmental toxicity in finfish embryos
ciguateric specimens and high toxicity were found among several her- and larvae (Colman et al. 2004; Yan et al. 2017; Mak et al. 2017), and
bivorous species in French Polynesia (Gaboriau et al. 2014). CTXs have been shown to link brain receptors in fish with similar af-
finity to that in mammals in laboratory tests (Dechraoui-Bottein et al.
4.4. CTXs biotransformation 2006). A proteomic approach also showed stress-related protein ex-
pression pointing to damage signs in toxic fish (Jiang et al. 2012). This
CTXs are biotransformed in different fish species leading to a suite may represent an important impact on larval and juvenile recruitment
of analogues of diverse toxicity and lipophilic levels. Cytochrome P450 in hatchery areas, like shallow reef-like ecosystems, with the con-
monooxygenase is a multi-enzymatic complex comprising several sub- sequent decrease in fish restocking and sustainability. Surprisingly,
families, and it is by far the most important enzymatic system. Ikehara toxins can be accumulated in certain species at such high levels capable
et al. (2017) found that incubation of a mix of CTX4A/B with fish en- to poison a hundred people (Diogène et al. 2017).
zymatic machinery in vitro (liver S9 fraction) was converted into CTX-2, Adult unicornfish Naso brevirostris exposed for four months to CTX-
6
L. Soliño and P.R. Costa
Table 1
Effects of exposure to ciguatoxins in fish species.
Fish species Fish stage Exposure route Toxin/toxic substrate Dose Study focus Effects Reference
−1
Acanthurus xanthopterus Adult Oral ingestion Toxic flesh of Lutjanus bohar 0.039–0.1 g toxic flesh g of Toxin transference and No signs of poisoning Helfrich and
fish toxicity on fish Banner, 1963
Thalassoma bifasciatum Adult Oral ingestion Gambierdiscus toxicus 0.26–4.88 mg of freeze-dried Toxin transference and Skin color variations, inactivity, loss of Davin et al.
Gambierdiscus cells g−1 of fish toxicity on fish equilibrium, erratic swimming, jerky feeding (1986)
movements, loss of orientation, and loss of net
avoidance ability
Epinephelus fulvus, Lutjanusapodus, Adult Intraperitoneal and Ciguatoxic fish extract and 7−35 mg of toxic fish g−1 of Toxin transference and Skin color variations, inactivity, loss of Davin et al.
Lutjanus mahogoni,and oral ingestion flesh and freeze-dried cells of fish toxicity on fish equilibrium, erratic swimming, jerky feeding (1988)
Micropterus salmoides Gambierdiscus toxicus movements, loss of orientation, and death (at
7.1 mg g−1)
Gambusia affinis Adult Dissolved toxins in Pure CTX1B and CTX-2 LD50 (48 h) 4.7 and Toxic effect on fish Pronounced opercular movement, uncoordinated Lewis (1992)
water 19.4 nmol kg−1 of fish swimming, and death
Oryzias latipes Embryos Microinjection C-CTX-1 5 pg egg−1 Effects of toxins on fish Decrease in heart rate, hyperkinetic twitching and Colman et al.
development spinal deformities. Hatched larvae presented loss (2004)
of orientation, inability to feed, mortality
7
Cephalopholis argus and Adults Naturally P-CTXs 81.8–0.01 ng g−1 CTX1B eq in Identification of Increase of cytoskeleton proteins and proteins Jiang et al.
Gymnothorax undulatus contaminated muscle detoxification proteins by involved in detoxification, antiapoptosis, and (2012)
proteomics approach immune defense
Mugil cephalus Juveniles Oral ingestion Gambierdiscus polynesiensis 0.3 ng CTX3C eq g−1 of fish Toxin transference and Relaxation of jaw,resting at bottom of tank, loss of Ledreux et al.
cells clearance; toxicity on fish equilibrium, bursts of erratic swimming, jerky (2014)
feeding behavior, leaping out of the water,
convulsions, and twitching
Oryzias melastigma Embryos Microinjection CTX1B 1.32–1.71 ng g−1 Effects of toxins on fish Hatching failure, caudal fin and spinal deformities, Yan et al.
development internal damage, immune dysfunction, (2017)
bradycardia, and twitching. Transcription of genes
related to the stress/immune responses, cardiac
and bone development, and apoptosis
Oryzias melastigma Larvae Microinjection CTX1B 0.0303–5.45 ng CTX1B g−1 Physiological and Reduced larval survivability, abnormal locomotion Mak et al.
(0.0303–5.45 pg CTX1B behavioral effects of toxins and response to external stimuli, low heartbeat (2017)
larva−1) on fish larvae rate, damages in the pericardial cavity, backbone
deformities, and failure of the swim bladder
inflation
Naso brevirostris Juveniles Oral ingestion Gambierdiscus polynesiensis 0.4 ng CTX3C eq g−1 fish CTX accumulation/ No signs of poisoning Clausing et al.
cells depuration rates (2018)
contaminated food did not shown any sign of intoxication (Clausing species for routine analysis in specific monitoring programs for CTXs.
et al. 2018). This disparity in results may be related to the species used
for laboratory test. For example, one study used Gambusia affinis as 5.2.2. Moray eels (Muraenidae)
animal model, which is a freshwater fish, and very unlikely to be ex- The broad distribution of moray eels (Gymnothorax spp.) and their
posed to CTXs in the environment (Lewis, 1992). More recently, capability to accumulate high CTXs levels have caused numerous CFP
Ledreux et al. (2014) used mullets caught in Southeast USA for their outbreaks in the Indo-Pacific and Atlantic Ocean (Chan. 2017). Moray
challenging experiment (Table 1). Mullets are not among the most ci- eels consumption is only popular in certain regions of French Polynesia
guateric fish species, and G. polynesiensis has never been reported in the and Papua New Guinea. However, this fishery is becoming more im-
area where these particular fishes were obtained (Ledreux et al. 2014; portant for exportation to China and Taiwan, where eels are used for
Clausing et al. 2018). Contradictory findings are probably caused by traditional medicine (Máñez and Paragay, 2013). In the Atlantic, Brazil,
species-specific strategies of toxin resistance. Some fish species such as Spain, and Portugal hold artisanal fisheries with minor catches of
pufferfish have developed a high degree of resistance to their own moray eels (FAO 2018).
potent neurotoxins (Yamamori et al. 1988). In the case of CTXs, the
threshold above which the toxin may affect the carrier and whether it is 5.2.3. Barracudas (Sphyraenidae)
the result of co-evolution by continuous exposition to the toxicant is not Barracudas are very popular commercial and recreational angling
clear. This issue should be extremely interesting in newly reported CFP species, and are implicated in a large number of CFP cases in Australia
areas where local fish encounter these compounds for the first time. A and the Caribbean Sea (Stewart et al. 2010; Hamilton et al. 2010; Azziz-
global increase in occurrences of harmful species in regions where they Baumgartner et al. 2012) (Fig. 3), e.g.,a sawtooth barracuda (Sphyraena
were previously undetected has been observed. The occurrence of putamae) caused a fatality in Brisbane (Queensland) (Hamilton et al.
Gambierdiscus in European areas of the Macaronesia and the Medi- 2010) and a captured 80-cm specimen contained 167.8 ppb of C-CTX-1
terranean Sea shows that environmental changes, such as global in the Bahamas (O'Toole et al. 2012).
warming and its underlying drivers, are rapidly modifying habitats. Although many of the catches are released because of the threat of
Species changes and adaptations to this new scenario are the inevitable ciguatera, the landed number of great barracuda (Sphyraena barracuda)
consequence for fish populations. Understanding the actual con- in Florida's Biscayne National Park, were 5956 fishes in the year 1991,
sequences of these changes will be imperative to predict the response of according to the sport fishing creel census (1976–1991) (Harper et al.
fish, fisheries, and consumers to the new context. 2000).
5.2. Risk of fish species implicated in CFP 5.2.4. Mackerels (Scombridae)

Spanish mackerel (Scomberomorus commerson) and king mackerel (S.
Although there are certain fish species considered of extreme CFP cavalla), which are highly appreciated species throughout the Indo-
risk, highly variable levels of toxins can be found within individuals of Pacific and West Atlantic Oceans, respectively, have been recurrently
the same species. This variability has been linked to the predominance involved in CFP (Fig. 3) (Lewis and Endean, 1983; Gillespie et al. 1986;
of toxic Gambierdiscus strains over less or non-toxic ones in ciguateric Farrel et al. 2016; 2017), and S. commerson is the principal species in-
areas. It has been observed that a given Gambierdiscus strain can be 100- volved in cases of ciguatera in subtropical Queensland, NE Australia.
fold more toxic than other strains within the same species (Litaker et al. Mackerels support important commercial and recreational fisheries
2010; Pisapia et al. 2017). This variability may be reflected in herbi- in waters across Australia and in the Caribbean, with total annual catch
vorous fish tissues and, as a result, the toxicity of contaminated fish of all mackerel (Scomberomorus spp.)of 922,493 t in 2016 (FAO 2018).
may vary along with CFP risk in a certain area. In the last instance,
consumer's preferences would determine the risk that certain species 5.2.5. Snappers (Lutjanidae)
may pose for a certain population. In the next sections, a summary of Several Lutjanus species, most frequently L. monostigma (one-spot
the most commonly CFP-involved fish families and their importance to snapper), L. bohar (blacktail snapper), and L. argentimaculatus (man-
fisheries is presented. For conciseness, only those cases showing values grove red snapper) are usually involved in poisoning events in the
above the recommended limit (0.01 ppb of CTX1B or 0.1 ppb for C- Pacific and Indian Ocean. In the Atlantic Ocean, L. jocu (dog snapper),
CTX-1) are detailed in Tables 2–4 for snappers, groupers, and jacks, L. apodus (schoolmaster), L. buccanella (blackfin snapper), or L. griseus
respectively. (gray snapper), although considered risk species in variable degree,
have much less CTX prevalence than their previously mentioned con-
5.2.1. Sharks (Elasmobranchs) geners in the Pacific and Indian Ocean (Fig. 3, Table 2). Recently, it has
Sharks have caused several CFP fatalities in the Indian Ocean. In been evidenced that hybrids of highly ciguateric L. apodus and non-
Madagascar, people died after an event in 1993 (Boisier et al. 1995) and ciguateric Ocyurus chrysurus can accumulate moderate levels of CTXs.
93 people got poisoned, suffering predominantly with neurological This may complicate preventive measures against CTXs and lead to
disorders. Furthermore, 11 people died after consumption of bull shark species misidentifications, increasing the risk of CFP in the areas where
Carcharhinus leucas in 2013 (Diogène et al. 2017). The toxin was in- both species coexist (Loeffler et al. 2019).
itially designated as carchatoxin, but the involvement of CTXs in this The highest percentage of snapper landings occurs mainly in
kind of poisoning was recently evidenced (Diogène et al. 2017). Al- Western Central Pacific, Eastern Indian Ocean, Western Central
though never fully confirmed, other CFP outbreaks involving sharks Atlantic, and Southwest Atlantic. These four regions, which comprise
have occurred in the Pacific and Gulf of Mexico (Meyer et al. 2016). endemic CFP areas, represent almost 85% of the total of landings for
Although liver is the primary sink organ where most fish species snapper (Amorim and Westmeyer, 2016).
accumulate and bioactivate CTXs, elasmobranchs also seem to highly
concentrate CTXs in their stomach. In Madagascar, the local tradition of 5.2.6. Groupers (Serranidae)
eating sharks' salted stomach has been responsible for the fatal cases The assemblage of species enclosed as groupers are among the
reported above. highest priced market reef species for the quality of their flesh.
One may consider that CFP caused by shark consumption are rare, According to Schoelinck et al. (2014), 29 out of 163 grouper species are
but the severity of symptoms and the importance of shark trade in the considered ciguateric. Grouper life history traits are generally char-
Indian Ocean, being about 32% of the global catches, make them a real acterized by long life span, slow growth, late maturation, and epi-
risk (Smale, 2008). Stakeholders and food safety authorities should benthic behavior. These features are common in species that accumu-
foster research on CTXs accumulation in sharks and consider certain late large quantities of CTXs, and Pacific species can bioactivate CTXs,
8
Table 2
Ciguatoxin (CTX) analogues or CTX-like activity quantified and confirmed by LC-MS/MS in the muscle of different species of snappers above the recommended limit of 0.01 of CTX1B equivalents (eq). Only maximum
values for each species and location are reported.
Species Common name Feeding habits Location CTX (ppb) CTX congeners Reference
Aprion virescens Green jobfish Mainly on fishes, crustaceans and cephalopods Coral Sea, Australia, South Pacific 0.036 CTX1B Farrel et al. 2017;
Edwards et al.
(2019)
Lutjanus argentimaculatus Mangrove red Mainly on fishes and crustaceans Hong Kong, North Pacific 0.75/1.10/ CTX1B/CTX-2/CTX-3 Wong et al. (2014)
snapper 0.52
Lutjanus bohar Red snapper Mainly on fishes, also shrimps, crabs, amphipods, stomatopods, Kiribati, South Pacific 4.0/0.84/0.45 CTX1B/CTX-2/CTX-3 Mak et al. (2013b)
gastropods, and urochordates Minamitorishima, North Pacific 2.8 CTX1B eqa (CTX1B confirmed by Yogi et al. (2011)
LC-MS/MS)
Hong Kong, North Pacific 1.35/0.56/ CTX1B/CTX-2/CTX-3 Wong et al. (2014)
0.27
Queensland, Australia, South Pacific 1.1 CTX1B Stewart et al. (2010)
Okinawa, North Pacific 1/0.1 CTX1B/CTX-2 Yogi et al. (2011)
Okinawa, North Pacific 0.35 CTX1B Oshiro et al. (2010)
Lutjanus buccanella Blackfin snapper Mainly on fishes Guadeloupe, Caribbean 0.105 CTX1B eqb (C-CTX-1 confirmed by Hossen et al. (2015)
LC-MS/MS)
Lutjanus cyanopterus Cubera snapper Mainly on fishes, shrimps and crabs Fuerteventura, Macaronesia, East 0.49 C-CTX-1 Estevez et al. (2019)
Atlantic
9
b
Lutjanus griseus Gray snapper Small fishes, shrimps, crabs, gastropods, cephalopods, and some Guadeloupe, Caribbean 0.042 CTX1B eq (C-CTX-1 confirmed by Hossen et al. (2015)
planktonic items LC-MS/MS)
0.24 CTX1B eqb (C-CTX-1 confirmed by Pottier et al. (2002b)
LC-MS/MS)
Lutjanus fulvus Blacktail snapper Fishes, shrimps, crabs, holothurians, and cephalopods Kiribati, South Pacific 0.046/0.02/0 CTX1B/CTX-2/CTX-3 Mak et al. (2013b)
Lutjanus jocu Dog snapper Mainly on fishes and benthic invertebrates, including shrimps, Guadeloupe, Caribbean 0.110 CTX1B eqb (C-CTX-1 confirmed by Hossen et al. (2015)
crabs, gastropods, and cephalopods LC-MS/MS)
Lutjanus malabaricus Malabar blood Mainly on fishes and small amounts of benthic crustaceans, Hong Kong, North Pacific 0.052/0.34/ CTX1B/CTX-2/CTX-3 Wong et al. (2014)
snapper cephalopods, and other invertebrates 0.29
Lutjanus monostigma One-spot snapper Mainly on fishes and benthic crustaceans, primarily crabs Okinawa, North Pacific 5.6 CTX1B Oshiro et al. (2010)
1.9/0.2 CTX1B/CTX-2 Yogi et al. (2011)
Okinawa, North Pacific 0.181 CTX1B Yogi et al. (2014)
Lutjanus sp. Snapper Carnivorous Okinawa, North Pacific 2.03 CTX1B Oshiro et al. (2010)
Guadeloupe, Caribbean 0.470 CTX1B eqb (C-CTX-1 confirmed by Hossen et al. (2015)
LC-MS/MS)
Lutjanus stellatus Star snapper Small crustaceans and fishes Hong Kong, North Pacific 0.021/0.09/ CTX1B/CTX-2/CTX -3 Wong et al. (2014)
0.09
Pagrus pagrus Red Porgy Crustaceans, fishes, and mollusks Selvagens Islands, Macaronesia, East 0.76 C-CTX-1 Estevez et al. (2019)
Atlantic
a
Equivalents of CTX1B by mouse bioassay (MBA) (1MU = 7 ng of CTX1B).
b
Equivalents of CTX1B by Cell Based Assay.
Table 3
Ciguatoxin (CTX) analogues or CTX-like activity quantified and confirmed by LC-MS/MS in the muscle of different species of groupers, above the recommended limit of 0.01 of CTX1B equivalents (eq). Only maximum
values for each species and location are reported.
Species Common name Feeding habits Location CTX (ppb) CTX congeners Reference
Anyperodon leucogrammicus Slender grouper Mainly on fishes and probably on crustaceans Okinawa, North Pacific 1/0.7 CTX1B/CTX-2 Yogi et al. (2011)
Cephalopholis argus Blue-spotted grouper Mainly on fishes and occasionally crustaceans Kiribati, South Pacific 2.92 CTX1B Wu et al. (2011)
Kiribati, South Pacific 1.71/0.67/0.71 CTX1B/CTX-2/CTX-3 Mak et al. (2013b)
Cephalopolis miniata Coral cod fishes and crustaceans Bremer Island, Australia, South 3.9 CTX1B eqa CTX1B (CTX1B Lucas et al. (1997)
Pacific confirmed by LC-MS)
Epinephelus coeruleopunctatus White-spotted grouper Fish and crustaceans Kiribati, South Pacific 0.29/0.75/0.21 CTX1B/CTX-2/CTX-3 Mak et al. (2013b)
Epinephelus cyanopodus Purple rock cod Mainly on sand-dwelling fishes and crustaceans such as Coral Sea, Australia, South Pacific 0.069 CTX1B Farrel et al. 2017;
snake eels and box crabs Edwards et al.
(2019)
Epinephelus fuscoguttatus Brown-marbled grouper Fishes, crabs, and cephalopods Okinawa, North Pacific 3.5/0.1 CTX1B/CTX-2 Yogi et al. (2011)
Kiribati, South Pacific 1.68/0.88/0.53 CTX1B/CTX-2/CTX-3 Mak et al. (2013a),b
Kiribati, South Pacific 1.4 CTX1B Wu et al. (2011)
Okinawa, North Pacific 0.25 CTX1B Oshiro et al. (2010)
Epinephelus lanceolatus Giant grouper Spiny lobsters, fishes, (small sharks and batoids), juvenile Hong Kong, North Pacific 0.019/0.25/ CTX1B/CTX-2/CTX-3 Wong et al. (2014)
sea turtles, and crustaceans 0.215
Epinephelus marginatus Dusky grouper Crabs and octopuses Tenerife, Macaronesia, East Atlantic 0.12 C-CTX-1 Estevez et al. (2019)
10
Epinephelus multinotatus White-blotched grouper Small fishes and crabs Kiribati, South Pacific 0.37/0.41/0.31 CTX1B/CTX-2/CTX-3 Mak et al. (2013b)
Epinephelus polyphekadion Camouflage grouper Mainly crustaceans (portunid crabs) and fishes, sometimes Kiribati, South Pacific 2.8/1.03/0.47 CTX1B/CTX-2/CTX-3 Mak et al. (2013b)
cephalopods and gastropods Hong Kong, North Pacific 0.023/0.18/ CTX1B/CTX-2/CTX-3 Wong et al. (2014)
0.18
Epinephelus sp. Undefined grouper Fish and invertebrates Hong Kong, North Pacific 0.5/0.4/0.4 CTX1B/CTX-2/CTX-3 Wong et al. (2014)
Epinephelus spilotoceps Foursaddle grouper Carnivorous Kiribati, South Pacific 2.73 CTX1B Wu et al. (2011)
Kiribati, South Pacific 0.19/0.03/0.02 CTX1B/CTX-2/CTX-3 Mak et al. (2013b)
Epinephelus tauvina Greasy grouper Mainly fishes and occasionally crustaceans Kiribati, South Pacific 0.24/0.10/0.05 CTX1B/CTX-2/CTX-3 Mak et al. (2013b)
Mycteroperca fusca Island grouper Crustaceans cephalopods, and fishes Selvagens Islands, Macaronesia, East 0.25 C-CTX-1 Costa et al. (2018)
Atlantic
Mycteroperca venenosa Yellowfin grouper Mainly on fishes (mostly on coral reef species) and squids Guadeloupe, Caribbean 0.171 C-CTX-1 Hossen et al. (2015)
Plectropomus laevis Blacksaddled Fishes (including groupers), occasionally crustaceans Okinawa, North Pacific 0.1/0.1 CTX1B/CTX-2 Yogi et al. (2011)
coralgrouper Hong Kong, North Pacific 0.04/0.15/0.15 CTX1B/CTX-2/CTX-3 Wong et al. (2014)
Plectropomus leopardus Leopard coralgrouper Mainly on fishes Hong Kong, North Pacific 0.16/0.92/0.24 CTX1B/CTX-2/CTX-3 Wong et al. (2014)
Variola albimarginata White-edged lyretail Fishes Hong Kong, North Pacific 0.23/0.44/0.30 CTX1B/CTX-2/CTX-3 Wong et al. (2014)
Variola louti Yellow-edged lyretail Mainly on fishes, crabs, shrimps, stomatopods, and other Okinawa, North Pacific 3.8/1.6 CTX1B/CTX-2 Yogi et al. (2011)
crustaceans Okinawa, North Pacific 2.8 CTX1B Oshiro et al. (2010)
Okinawa, North Pacific 0.079 CTX1B Yogi et al. (2014)
a
Equivalents of CTX1B by mouse bioassay (MBA).
Ciguatoxin (CTX) analogues or CTX-like activity quantified and confirmed by LC-MS/MS in the muscle of different species of jacks above the recommended limit of 0.01 of CTX1B equivalents (eq). Only maximum values
Pérez-Arellano et al., 2005

Caillaud et al. (2012)
Hossen et al. (2015)
Hossen et al. (2015)
Boada et al. (2010)

Boada et al. (2010)
Otero et al. (2010)
Otero et al. (2010)

Pottier et al.2002b
Reference
CTX1B eq (C-CTX-1 confirmed by LC-MS/MS)
CTX1B eqa (C-CTX-1 confirmed by LC-MS/MS)
CTX1B eqa (C-CTX-1 confirmed by LC-MS/MS)
Fig. 3. Representation of the risk of main ciguateric groups of fish from the
C-CTX-1/CTX3C/CTX1B
C-CTX-1/CTX3C/CTX1B
Atlantic regarding their toxicity and fish catches.

CTX congeners
leading to CTX1B (Ikehara et al. 2017). Although several ciguateric

a
species are banned and advisory recommendations have been released

C-CTX-1
C-CTX-1
C-CTX-1
C-CTX-1
to the population in endemic areas, misidentification of species may

occur, especially in places with high affluence of sparse fishing tourism
(Stewart et al. 2010).
5.8/0.778/0.125
4.37/1.075/1.02
According to the Food and Agricultural Organization of the United

Nations (FAO), groupers contributed more than 461,545 t to global
capture fisheries production in 2016 (FAO 2018). The Florida finfish
0.022
13.79
0.054
62.3
0.17
0.08
CTX
fishery generates over USD $37.5 million in annual dockside value from
1.0
the snapper-grouper complex (Stevens et al. 2017).

Selvagens Islands, Macaronesia, East Atlantic
Selvagens islands, Macaronesia, East Atlantic

Canary Islands, Macaronesia, East Atlantic
Canary Islands, Macaronesia, East Atlantic
5.2.7. Jacks (Carangidae)

Jacks usually refer to the group of fish belonging to the Carangidae
family, and are one of the fish most frequently involved in ciguateric
episodes in the Atlantic (Pottier et al. 2001). The most ciguateric spe-
cies include amberjacks, jacks, and pompanos. Among them, great
Guadeloupe, Caribbean
amberjack (Seriola dumerili), lesser amberjack (S. fasciata), and longfin

yellowtail (S. rivoliana) are highly appreciated by anglers and hold an
important artisanal and commercial fishery in the Caribbean
(Mohammed, 2012).
Location
Amberjacks are also considered a risk species in the Pacific Ocean,

and have been reported to accumulate different congeners of P-CTX and
C-CTX, depending on the catch site (Otero et al. 2010; Yogi et al. 2011;
Estevez et al. 2018).
Mainly on fish, shrimps and other invertebrates
Mainly on fishes and occasionally invertebrates
In the South Atlantic region of the US, the total landings (recrea-
tional and commercial) of great amberjack accounted for more than
Fishes and occasionally invertebrates
576 t in 2006 (SEDAR, 2008). In the Gulf of Mexico, recreational

fisheries landed an average around 680 tof great amberjack per year
between 1992 and 2016 (Crabtree, 2017). In Japan, yellowtail am-
berjack capture fishery landed 66,345 t in 2004 (Nakada, 2008). The
recently CFP-affected areas of the Macaronesia hold an important local
fishery of great and longfin yellowtail amberjacks, that summed a total
Equivalents of CTX1B by Cell Based Assay (CBA).
Squids and fishes
of 10.6 tduring 2017 in the Canary Islands (Spain) (Gobierno de

Fishes at night
Feeding habits
Carnivorous
Canarias, 2017). Moreover, Madeira Islands (Portugal) have a re-

markable amberjack fishery with an average of 7.17 t annual catches
for each species and location are reported.
between 2000 and 2016 (FAO 2018).

Longfin yellowtail
5.2.8. Parrotfish (Scaridae) and surgeonfish (Acanthuridae)

Lesser amberjack
Great amberjack
Common name
Horse-eye jack
Parrotfishes include the genus Scarus, Chlorurus, and Sparisoma

pertaining to the Labridae family. Parrotfishes, together with surgeon-
Black jack
fishes (the genus Acanthurus), are among the most reported CFP-im-
Jack
plicated fish in French Polynesia (Laurent et al. 2005; Darius et al.

2007; Chinain et al. 2010; Clausing and Bottein, 2016; Morin et al.
Seriola rivoliana
2016) and Hawaii (Copeland et al. 2014). These fish are mainly her-
Caranx lugubris
Seriola dumerili
Seriola fasciata
Caranx latus
Caranx spp.
bivorous grazers and have been reported to accumulate less toxic CTX
analogues, such as CTX4A/B, than those of top predators. Although
Species
Table 4
CTX1B is 10-fold more toxic than the precursors CTX4A/B, the elevated
a
feeding rates and specific home range observed in these genera will
11
result in high total toxicity content (Soliño and Costa, 2018). Caribbean species or those caught in traditionally ciguateric reefs, tourist or new
and Pacific Scarus/Acanthurus fisheries are mainly artisanal. This kind residents are less informed (Chinain et al. 2010; Morin et al. 2016). This
of fishery is particularly important in developing countries and highly is also a restrain for tourism, causing millionaire losses from bad pub-
fish-dependent areas, such as islands (Page, 1998). In the tropics, ar- licity, insurance and litigation costs, and hospitalization (Farrel et al.
tisanal fisheries land around 6 million t per year, with a trade value of 2017).
USD $2.4 billion (Hawkins and Roberts, 2004). Although reef-herbi- An important part of tourism in coastal countries is recreational
vorous fish were traditionally destined to local market and subsistence, fishery. Globally, this industry was estimated to trade between USD $65
they are increasing in importance for the economy of communities in to 79 billion in 2015, and represents a direct employment of around
the Pacific and Caribbean islands (Salas et al. 2007; Rassweiler et al. 16.8 to 20.7 million people (FAO, 2018). Sport fishers are among the
2019). As population and tourism rise in the most developed regions, most exposed sectors in coastal population (Radke et al. 2015). Anglers
the rising demand for local fish in these areas is an increasing concern. usually consume their own catches and non-locals are more prone to
ignore the laws and traditional knowledge on CFP. Occasionally, CFP
5.2.9. Marine organisms other than fish has frustrated the intention of establishing prolific recreational and
The origin of the word ciguatera has been attributed to a gastropod commercial fisheries. The grouper C. argus was introduced to Hawaii in
called cigua by natives in the Caribbean (Hokama and Yoshikawa- the 1950s. Since groupers, snappers, and other species with high eco-
Ebesu, 2001). Although ciguatera is commonly associated with fish nomical value were not frequent in Hawaiian Islands, a new fishery of
consumption, it has been found in several invertebrates, namely gas- C. argus was planned, with the aim of creating new economic niches for
tropods like turban shell (Turbo argyrostomus) (Yasumoto and Kano, the islanders. Despite released individuals proliferating and reaching
1976) and trochus (Tectus niloticus) (Darius et al. 2018a; Gatti et al. high biomass in the new territory, the fishery got frustrated after sev-
2018), bivalves like giant clams (Tridacna maxima) (Laurent et al. 2008, eral cases of CFP outbreaks (Bienfang et al. 2012). As a consequence of
2012; Roué et al. 2013, 2016), and echinoderms like the purple sea star refusal by consumers, C. argus became a potential threat to native fishes
(Ophidiaster ophidianus), spiny starfish (Marthasterias glacialis) (Silva and fisheries (Dierking and Campora, 2009). A similar case occurred
et al. 2015), and the sea urchin Tripneustes gratilla (Darius et al. 2018b). with lionfish (Pterois spp.), accidently introduced in the Caribbean. The
CTX1B was found as well in octopus, spiny lobster (Panulirus peni- absence of predators and voracity of this species is a threat for coral
cillatus), and the crab Charybdis paucidentata (Mak et al. 2013b). Al- reefs and native fauna. However, lionfish is a highly appreciated dish,
though invertebrates are not usually involved in CFP events, they may and the establishment of a new lionfish fishery was suggested as an
have a key role in CTXs transfer through the food web. Recently, CTX3C alternative to control their populations. Great efforts were made to
has been found in the marine mammal Hawaiian monk seal (Monachus promote their consumption, until several studies proved the risk of
schauinslandi), pointing that the pervasiveness of CTXs may be higher lionfish as a ciguateric species in the Lesser Antilles (Robertson et al.
than previously expected (Dechraoui-Bottein et al. 2011). 2014; Soliño et al. 2015; Hardison et al. 2018).
The lack of routine analyses for CTX determination in fish and the
5.3. Impact to fish consumption and fishing industry regulation of fisheries based on fish size have been shown to be detri-
mental for fishery profits and for consumers. The experimental appli-
The uncertainty of Gambierdiscus blooms and the variability of CTX cation of regular analyses to S. dumerili allowed for the sale of 1316
accumulation in fish are two of the main reasons why CFP is extremely large fish that would otherwise not have been sold owing to the ban on
difficult to predict and avoid. While high density of Gambierdiscus has selling amberjacks over 9 kg in Hawaii, i.e., more than 83% of all tested
been related to coral reef disturbances and sea surface temperatures in S. dumerili weighing over 9 kg tested negative. Furthermore, no re-
some regions (Kohler and Kohler, 1992; Hales et al. 1999; Quod et al. ported cases of CFP were registered during the period when this control
2000; Villareal et al. 2007; Chinain et al. 2010; Skinner et al. 2011; was employed (Kimura et al. 1982).
Rongo and van Woesik 2012; Morin et al. 2016), other studies did not Similar strategies are likely to be applied in the newly reported CFP
find a clear pattern on seasonality of Gambierdiscus blooms (Parson areas. After the occurrence of the first CFP episodes, the ban on selling
et al. 2010). CTXs occurrence in herbivorous fish has been shown to lag amberjacks of 10 kg or heavier was established in Madeira (Portugal)
after the increase of dinoflagellates. However, movement patterns of without any monitoring control for the actual presence of the toxin. In
carnivorous fish frustrate monitoring and identification of toxic catches. the nearby Canary Islands, the ban is restricted to amberjacks over
For example, several intoxications in North Florida have been related to 14 kg, which are frozen until CTX analyses results are obtained
migrating fish from southern latitudes (Radke et al. 2015). (Sanchez-Henao et al. 2019). This method allows for the trade of safe
The development of fishing industry has increased CFP uncertainty fish over the considered "risk" size, although with the inherent loss of
to some extent. In the Caribbean, islanders have dealt with ciguatera for quality and market price owing to the freezing procedure. Size-based
centuries. Knowing and identifying the riskiest ciguateric areas and the regulations do not only affect amberjacks species but also other im-
direct introduction of fish in the markets contributed to an easy tra- portant commercial species like groupers and snappers. The difficulty of
ceability of fishery products. As fisheries developed, fishing boats developing easy to handle analyses to be applied in-situ is one of the
started operating in further areas and fish were sold in further markets, main obstacles for CFP effective management. After withdrawing the
leading to the “anonymity” of ciguateric fish and spreading risk to “cigua-check” tests (Bienfang et al. 2011), the only true methods for
broader areas (Tosteson, 2004). The same might be true for the Pacific CTXs detection have to be performed in specialized laboratories. In new
islands (Copeland et al. 2014; Farrel et al. 2016). CFP-affected areas and developing regions with limited know-how and
CFP is a debilitating syndrome with high probability of recurrence resources for CTXs monitoring and management, the size-based reg-
after fish consumption, which is one of the main causes of fish con- ulations are still applied as a general rule. This is a risky strategy as
sumption avoidance after suffering the poisoning. In Rarotonga, 71% of there is no scientific evidence of their effectiveness to guarantee sea-
residents exclude fish from their diet because of the risk of CFP food safety and they have been proved to result in important profit loss
(Hajkowicz, 2006). As a consequence of CFP, the gross value of harvest for the fishery market. In Rarotonga, the estimated costs of CFP mon-
loss for reef fish was estimated to be NZD $123,091 in 2001 (USD itoring and management for 2001 were NZD $18,100, while the costs
$82,327.57) in this island (Rongo et al. 2012). In Tahiti, sell losses of associated to health-care and loss of reef fish harvests surpassed NZD
3000 t of reef fish were estimated to cost one million USD dollars $1,000,000, for the same year (Rongo et al. 2012). Therefore, the ap-
(Bagnis et al. 1992). plication of effective monitoring programs would be certainly worthy
Population awareness is another important factor. Although people for fishing industries and public administrations and would improve the
from endemic areas usually avoid consuming the most ciguateric-prone socio-economic status of endemic CFP regions.
12
6. Concluding remarks West Africa coast: an emerging risk in the canary islands (Spain). Toxicon 56 (8),
1516–1519.
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teric territories have been coping with CFP for years, they still face old of ciguatoxins in Hawaiian monk seals Monachus schauinslandi from the northwestern
challenges and are dealing with new ones, such as: and main Hawaiian islands. Environmental science & technology 45 (12),
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Declaration of competing interest poisoning in French Polynesia. Harmful Algae 4 (6), 1053–1062.
Chateau-Degat, M.L., Dewailly, E., Cerf, N., Nguyen, N.L., Huin‐Blondey, M.O., Hubert,
The authors declare no conflicts of interest. B., Laudon, F., Chansin, R., 2007a. Temporal trends and epidemiological aspects of
ciguatera in French Polynesia: a 10-year analysis. Trop. Med. Int. Health 12 (4),
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Environmental Research 182 (2020) 109111

Contents lists available at ScienceDirect

Global impact of ciguatoxins and ciguatera fish poisoning on fish, fisheries T

Hokama and Yoshikawa-Ebesu, 2001). (Lewis, 1986; Skinner et al. 2011).

5.2. Risk of ﬁsh species implicated in CFP 5.2.4. Mackerels (Scombridae)

Pérez-Arellano et al., 2005

Hossen et al. (2015)

Boada et al. (2010)

Otero et al. (2010)

CTX1B eq (C-CTX-1 conﬁrmed by LC-MS/MS)

CTX1B eqa (C-CTX-1 conﬁrmed by LC-MS/MS)

CTX1B eqa (C-CTX-1 conﬁrmed by LC-MS/MS)

Atlantic regarding their toxicity and ﬁsh catches.

leading to CTX1B (Ikehara et al. 2017). Although several ciguateric

species are banned and advisory recommendations have been released

to the population in endemic areas, misidentiﬁcation of species may

According to the Food and Agricultural Organization of the United

the snapper-grouper complex (Stevens et al. 2017).

Selvagens islands, Macaronesia, East Atlantic

Canary Islands, Macaronesia, East Atlantic

5.2.7. Jacks (Carangidae)

amberjack (Seriola dumerili), lesser amberjack (S. fasciata), and longﬁn

Amberjacks are also considered a risk species in the Paciﬁc Ocean,

Mainly on ﬁshes and occasionally invertebrates

576 t in 2006 (SEDAR, 2008). In the Gulf of Mexico, recreational

of 10.6 tduring 2017 in the Canary Islands (Spain) (Gobierno de

Canarias, 2017). Moreover, Madeira Islands (Portugal) have a re-

between 2000 and 2016 (FAO 2018).

5.2.8. Parrotﬁsh (Scaridae) and surgeonﬁsh (Acanthuridae)

Parrotﬁshes include the genus Scarus, Chlorurus, and Sparisoma

plicated ﬁsh in French Polynesia (Laurent et al. 2005; Darius et al.

283–297. morphology of Gambierdiscus yasumotoi from tropical eastern Australia. Harmful

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