Insights on mycotoxins in aquaculture
A review of the impact of mycotoxins on aquatic species

Mycotoxins are toxic and potentially carcinogenic substances produced by different types of fungi. Mycotoxin-induced diseases have severe economic consequences for the aquaculture industry.

So far, different methods of both chemical, microbiological and physical mechanisms that can either eliminate or reduce the effect of mycotoxins are available.

In the first part of this review, we review the main mycotoxins that pose a threat to the aquaculture industry and their effects on aquatic species.

Micotoxins risk in Aquafeed

The world food supply system is expected to be under massive pressure by the end of 2050, when the human population is projected to reach up to 10 billion (Millington and Cleland, 2017). This increasing human population will represent a tremendous demand for animal protein and fish products (Tilman and Clark, 2014).

The fishing industry has also led to the depletion of wild aquatic animals.

Capture fisheries are no longer seen as a sustainable source for supplying our ever-increasing protein demand. Therefore, aquaculture is considered the best candidate to meet our animal protein needs (Subasinghe et al., 2009).

With the expansion of the aquaculture sector, the demand for aquafeed, which is an integral part of the production cost accounting for approximately 60% of the total fish production cost in intensive and super-intensive farming systems, is increasing (Alceste y Jory, 2000).

Mainstream fish farmers in tropical and developing regions use home-produced instead of imported fish feed because imported feed is usually expensive.

To manufacture local feed pellets, the farmers utilize animal waste and local plants such as soybeans, maize, rice, and many other grains (Liti et al. 2005). Since no vital biosecurity measurements are taken during the feed formulation process, such feeds are usually susceptible to contamination with moulds before and after storage (Almeida et al., 2012) and some of them can produce mycotoxins.

Mycotoxins are toxic and potentially carcinogenic substances produced by different types of fungi (Zain et al., 2012).

The formation and concentration of mycotoxins in aquaculture are primarily affected by temperature and humidity. Still, many other elements also affect the growth of moulds, such as:

• Water movement
• Substrates
• pH levels
• Feed storage conditions
• Microbial abundance and interactions

(Di Gregorio et al., 2014)

Infections triggered by mycotoxins are known as mycotoxicosis and are influenced by the dose, species, age, and duration of intoxication.

Depending on the type of mycotoxin, different pathological symptoms can be observed in the affected species, such as anaemia, liver and kidney lesions, hemorrhaging, increased susceptibility to other diseases, and even death (Jaynes et al., 2007).

Mycotoxin-induced diseases cause severe economic reductions in the aquaculture industry (Di Gregorio et al. 2014).

For this reason, in recent years, researchers have made an effort to examine possible strategies for decontamination of mycotoxins in aquaculture (Bovo et al., 2012). To prevent the occurrence of mycotoxins, strong biosecurity measures before and after aquafeed storage are recommended (Di Gregorio et al. 2014). However, the occurrence of mycotoxins is challenging to avoid (Kendra and Dyer, 2007).

The occurrence and toxicity of mycotoxins in aquaculture

Studies on the negative impact of mycotoxins in animals have focused mainly on terrestrial livestock rather than aquatic farmed animals (Pestka, 2007). It was not until the outbreak of aflatoxins in the rainbow trout industry in the 1960s that researchers started to make an effort to study the effects of mycotoxins in aquaculture (Gonçalves et al., 2018).

Due to the higher cost of aquaculture feed ingredients and fish oil, in particular, researchers have sought to identify potential protein source alternatives. Plant proteins can serve as an excellent substitute for fish oil in aquatic feeds, as they are cost-effective and available on a large scale (Anater et al. 2016).

Currently, plant proteins such as oilseeds and grains are included in most aquatic feeds formulated for warm water finfish such as tilapia, carp, and catfish (Marijani et al., 2019).

This type of feed is very vulnerable to fungal contamination, so the occurrence of mycotoxins is inevitable (Marijani et al., 2017).

According to Berthiller et al. (2007), over 400 mycotoxin types are known worldwide and, among them, aflatoxins are the best known due to their frequency of incidence, followed by ochratoxins and Fusarium mycotoxins. Apart from these main mycotoxins, others with low frequency of occurrences, such as nivalenol, alternariol, and roquefortine C, are detected in fish feed (Marijani et al., 2017).

Aflatoxins

Aflatoxins are water-soluble substances produced by moulds from the genus Aspergillus, particularly Aspergillus parasiticus and Aspergillus flavus (Varga et al., 2009).

There are approximately 20 aflatoxins detected worldwide, but only four of them (AFB₁, AFB₂, AFG₁ and AFG₂) have been studied much more than others simply because they are the most toxic aflatoxin molecules (Santacroce et al., 2008).

A. parasiticus can produce all of the earlier mentioned compounds, whereas A. flavus can only produce aflatoxins B₁ and B₂. However, both species can contaminate pre- and post-storage conditions of aquafeeds (Bryden, 2012).

Aflatoxins mainly occur in humid climates but they have also been reported in tropical and subtropical regions (Ostrowski-Meissner et al. 1995; Marin et al. 2013).

A study conducted by Alinezhad et al. (2011), investigated the presence of aflatoxins in the ingredients and feed formulated for rainbow trout.

At the end of the experiment, higher contamination rates of AFB₁ were detected (average toxic presence of 0.067, 0.031, 0.012, and 0.009 mg/kg in fishmeal, soybean, wheat, and pallet feed, respectively).

The biological effects of aflatoxins are hazardous. The most potent aflatoxin type is AFB₁ which can:

• Cause severe liver damage
• Promote cancer
• Induce genetic mutations
• Halt the reproduction process
• Substantially weaken the immune system

Aflatoxin-related toxicity depends on the concentration, life stage, and species of the farmed animal (Hendricks, 1993).

In aquaculture, aflatoxins were first identified in 1963 during a hepatoma epizootic in the trout industry when fish were fed aflatoxin-contaminated feed (Ashley and Halver, 1963). Similar aflatoxin poisoning events in different fish species have been reported since then (Ashley et al., 1965; Cagauan et al., 2004; Zhang et al., 2022).

There are three stages of aflatoxicosis: acute, subacute, and chronic.

ACUTE AFLATOXICOSIS

The acute phase occurs when an aquatic animal consumes a moderate or elevated dose of aflatoxins in a short time, resulting in health consequences such as;

• Anaemia
• Whitish or pale gills
• Haemorrhaging
• Poor nutrient utilization
• Hepatotoxicity

(Matejova et al., 2017a)

A 10-day experiment conducted by Sahoo et al. (2001) with carp revealed that the ingestion of aflatoxin B₁ by Labeo rohita at a dose of 11.25 mg/kg caused significantly reduced appetite, lethargy, and loss of balance.

When tissue histomorphology was analysed, they also found seriously damaged kidneys and gills, necrotic liver with vascular dilatation and congestion, as well as sloughed intestines.

Subacute and chronic forms occur when animals are exposed to low doses of aflatoxin over a relatively long period, typically about three and six months, respectively.

SUBACUTE AFLATOXICOSIS

Pathological symptoms of subacute aflatoxicosis include:

• Immunosuppression
• Hepatotoxicity
• Yellowish skin
• Failed nutrient adsorption

(Santacroce et al., 2008)

Symptoms such as liver necrosis, vascular dilation, occlusion, and significant reduction of immune response and antioxidant enzymes were reported in the study by Sahoo et al. (2001) when a 2.5 mg/kg dose of aflatoxin B₁ was given to Labeo rohita for 90 days.

CHRONIC AFLATOXICOSIS

The chronic stage of aflatoxin exposure is associated with:

• Carcinogenicity
• Immunosuppression
• Hepatotoxicity
• Mutagenicity
• Haematological alterations

The main chronic histopathological symptoms observed in different fish species include liver failure, cessation of feed intake, weakened immune system, and death (Santacroce et al., 2008).

Moreover, a study conducted by Shahafve et al. (2017) evaluated the effects of diets containing different doses of aflatoxins (0.5, 0.7, and 1.4 mg/ kg) on common carp (Cyprinus carpio) tissue histomorphology for 3 weeks.

Pathological examinations revealed irregular and shrunken gill lamellae, necrotic and swollen liver hepatocytes, vascular congestion, damaged liver parenchyma, renal urinary space dilation, abnormal increase in goblet cells, sloughed intestines, and inflammation.

Fusarium mycotoxins

Fusarium moulds produce a variety of potent mycotoxins, but three of them have so far undergone substantial research studies (Placinta et al., 2016):

• ⇰ Trichothecenes
• ⇰ Fumonisins
• ⇰ Zearalenone

Globally, many reports show the incidence of Fusarium mycotoxin in grains and aquatic animal feed, especially when they are under humid conditions (Pinotti et al., 2016; Bryden, 2012).

TRICHOTHECENES

Trichothecenes are mycotoxins produced by fungi species belonging to different genera such as Fusarium, Myrothecium, and Trichothecium (Tamm & Breitenstein, 1984). There are four well-known trichothecenes:

• ⇰ Deoxynivalenol (DON)
• ⇰ T-2 toxin
• ⇰ Diacetoxyscirpenol (DAS)
• ⇰ Nivalenol (NIV)

(Escrivá et al., 2015)

These compounds contaminate cereals, for instance, maize, soybeans, wheat, and similar grains, all of which are significant components of aquafeeds (Meronuck and Xie, 1999).

Animals exposed to trichothecenes for a long time show various clinical signs, such as:

• Cessation of feeding
• Sluggish movement
• Growth restriction
• Tissue lesions

Higher doses of this mycotoxin also trigger shock-like syndrome, eventually resulting in mortality (Matejova et al., 2017a).

The two most toxic trichothecenes in aquaculture are T-2 toxin and DON.

T-2 TOXIN

An experiment carried out by Poston et al. (1982) assessed the adverse effects of higher and lower doses (2.5 and 15 mg/kg) of T-2 toxin on trout (Oncorhynchus mykiss).

The results indicated reduced growth rate and feed utilization parameters in the groups ingested lower toxic levels, while those exposed to higher doses showed sloughed intestines, haemorrhaging, and significantly damaged spleens.

Another study carried out by Manning et al. (2003) examined the biological effect of four different T-2 toxin dosages (0.63, 1.3, 2.5, & 5 mg/kg) on the growth and tissue histomorphology of channel catfish (Ictalurus punctatus).

Significantly reduced growth rate and feed utilization indexes, as well as lesions in the intestine and liver, were reported in this study.

A more recent study by Matejova et al. (2017) evaluated the effect of 5.3 mg/kg T-2 toxin in diet on the growth, immune and haematological indices of common carp (Cyprinus carpio) for 30 days.

Negatively affected haematological parameters such as haemoglobin, red and white blood cells, and reduced antioxidant enzymes, as well as tissue lesions, were noted in this study.

DON

Deoxynivalenol, also called vomitoxin, is generally less toxic but more common than T-2 toxin. Like other trichothecenes, it occurs in grains, particularly wheat and maize, contaminating aquafeed containing any of these grains (Marin et al., 2013).

Pathological signs of vomitoxin ingestion aquaculture species include:

• Growth retardation
• Degenerated and sloughed intestine
• Inflammation
• Poor nutrient utilization
• Immunosuppression

(Hooft et al., 2011)

Huang et al. (2020) evaluated how deoxynivalenol at five different doses (0.03, 0.32, 0.63, 0.92 and 1.24 mg/kg) affected the gill histomorphology of grass carp (Ctenopharyngodan idella) over 2 months.

The results of this study depicted a considerable reduction in the antioxidant capacity of the fish, as well as lesions and injury of both the gills and their tight junctions.

FUMONISINS

Fumonisins are mainly produced by Fusarium verticillioides and F. proliferatum, which are species that are frequently found contaminating maize. Among the different types of this mycotoxin, the most well-known is Fumonisin B₁ (Scott, 2012).

In aquaculture, fumonisins are linked to:

• Growth retardation
• Poor nutrient utilization
• Halted sphingolipid metabolism

(Tuan et al., 2003)

Fumonisins have a long hydrocarbon chain resembling sphingosine, an enzyme that helps catalyze the alkylation and diacylation of sphingolipids during lipid metabolism.

⇰ Fumonisin B₁, therefore, acts as an inhibitor of sphingolipid synthesis which is crucial for membrane and lipoprotein structures (Wang et al., 1992).

Claudino-Silva et al. (2018) examined the toxicity of diets containing Fumonisin B₁ and B₂ at various doses (20, 40, and 60 mg/kg) on the growth and feed utilization of tilapia (Oreochromis niloticus).

At the end of this trial, significant growth and growth hormone reduction and poor nutrient utilization were detected.

ZEARALENONE

Zearalenone is another Fusarium mycotoxin mainly produced by Fusarium culmorum and Fusarium graminearum, appearing in different grains such as maize and wheat (Henderson y Smith, 1991).

The production of ZEN is associated with high moisture and lower temperature conditions, and it is linked to reproductive alterations in the exposed animals (Placinta et al., 1999).

⇰ The metabolites produced by zearalenone are structurally similar to natural estrogens and, by mimicking these hormones, they bind with estrogen receptors halting the reproduction of the animal (Kumar et al., 2013).

A three-week experiment conducted by Schwartz et al. (2010) investigating the effects of zearalenone on zebrafish (Danio rerio) reproduction found that it reduced both the fish’s fertility and spawning frequency. Similar results were reported in a study conducted by Woźny et al. (2015) with rainbow trout.

OCHRATOXINS

Ochratoxins are toxic secondary metabolites produced by fungi belonging to the genera Aspergillus and Penicillium. Among the Ochratoxin groups, ochratoxin A (OTA) is the most prevalent and is known for its toxicity for kidney and liver in domesticated animals (Manning and Wyatt, 1984) and residues in the exposed animal’s meat (Guillamont et al., 2005).

⇰ Significantly lower feed utilization rate, growth retardation, premature mortality, and necrotic kidney and liver are among the clinical signs reported in aquaculture species exposed to OTA (Manning et al., 2003).

A study carried out by Hagelberg et al. (1989) assessed how three different doses of OTA (4, 6, and 8 mg/kg) affected the liver and kidney histomorphology of rainbow trout.

Results depicted that the groups fed diets containing 4 mg/kg OTA had moderate kidney and liver damage while those with 8 mg/kg showed severe hepatotoxicity and nephrotoxicity.

Similarly, El-Sayed et al. (2009) examined the sensitivity and clinical symptoms of sea bass (Dicentrarchus labrax) fed with diets supplemented with OTA at a dose of 9.23 mg/kg.

Lethargy, loss of balance, and haemorrhaging dorsal and eroded ventral surfaces were among the observed clinical signs before death. At the same time, necropsy revealed necrotic liver with severe vascular dilatation and congestion, as well as damaged kidneys.

A more recent study by Baldissera et al. (2020) investigated the effects of OTA (2.4 mg/kg in feed) on the growth, feed utilization, and antioxidant enzymes of tambaqui (Colossoma macropomum).

Significant reduction of growth and feed utilization indices, as well as higher antioxidant enzymes in fish muscles, were reported in this study.

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