A review of the impact of mycotoxins on
Mursal Abdulkadir Hersi1, Dogukan Kaya2 and Ercument Genc1* 1Department of Fisheries and Aquaculture Engineering, Faculty of Agriculture, Ankara University, Ankara, Turkey 2Agricultural Applications and Research Center, Tokat Gaziosmanpasa University, Tokat, Turkey Corresponding author: egenc@ankara.edu.tr
INSIGHTS on MYCOTOXINS in AQUACULTURE
Mainstream fish farmers in tropical and developing regions use home-produced instead of imported fish feed because imported feed is usually expensive.
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.
So far, different methods of both chemical, microbiological and physical mechanisms that can either eliminate or reduce the effect of mycotoxins are available.
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).
Mycotoxins risk in Aquafeed
The fishing industry has also led to the depletion of wild aquatic animals.
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Mycotoxins are toxic and potentially carcinogenic substances produced by different types of fungi. Mycotoxin-induced diseases have severe economic consequences for the aquaculture industry.
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)
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 and Jory, 2000)
Water
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).
(Di Gregorio et al., 2014)
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:
Mycotoxins are toxic and potentially carcinogenic substances produced by different types of fungi (Zain et al., 2012)
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.
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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).
SubstratesmovementpHlevelsFeedstorageconditionsMicrobialabundanceand interactions
The occurrence and toxicity of mycotoxins in aquaculture
Alinezhad et al. (2011)
Ochratoxins
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).
Table 1. Main mycotoxins and their associated toxicity in aquaculture.
Aflatoxin B1, B2, G1 & G2
Tuan et al. (2003)
This type of feed is very vulnerable to fungal contamination, so the occurrence of mycotoxins is inevitable (Marijani et al., 2017).
Zearalenone
Type of mycotoxin
Ochratoxin A
Growth retardation, poor nutrient utilization, and halting of sphingolipid metabolism
Immunosuppression, hepatotoxicity, mutagenicity, carcinogenicity, and negative effects on animal reproduction
Table 1 summarizes the main mycotoxin types and their expected clinical signs.
Protein biosynthesis inhibition, immunosuppression, neurotoxicity, tissue lesions, and shock-like syndrome
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).
Associated toxicity in aquaculture Reference
Trichothecenes
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)
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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).
Teratogenicity, reduction of fertility and spawning frequency Schwartz et al. (2010)
T-2 toxin & deoxynivalenol
Matejovaetal.(2017a);Kumaretal.(2013)
Aflatoxins
Nephrotoxicity, hepatotoxicity, growth retardation, and premature mortality Manningetal.(2003)
Zearalenone
Main representative
Fumonisins B1 & B2
Fumonisins
A study conducted by Alinezhad et al. (2011), investigated the presence of aflatoxins in the ingredients and feed formulated for rainbow trout.
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).
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)
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Aflatoxins
Aflatoxins are water-soluble substances produced by moulds from the genus Aspergillus, particularly Aspergillus parasiticus and Aspergillus flavus (Varga et al., 2009).
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).
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).
Substantially weaken the immune system
The biological effects of aflatoxins are hazardous. The most potent aflatoxin type is AFB1 which can:
Aflatoxin-related toxicity depends on the concentration, life stage, and species of the farmed animal (Hendricks, 1993)
AFLATOXIN
Upon ingestion, aflatoxins are absorbed from the digestive system through passive transport to the liver where they are metabolized into various molecules.
Halt the reproduction process
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).
One of its major metabolites is AFB1 8,9-epoxide which results from metabolization by cytochrome P450 (Corcuera et al., 2012).
Promote cancer
Through this mode of action, the compound interacts with the macromolecules of DNA and proteins, hence promoting the carcinogenic effect of aflatoxins (Chaytor et al., 2011).
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Cause severe liver damage
Induce genetic mutations
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;
AFLATOXICOSISSUBACUTE
Pathological symptoms of subacute aflatoxicosis include:
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.
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.
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.
HepatotoxicityHaemorrhagingPoornutrientutilization(Matejova et al., 2017a)
AFLATOXICOSISACUTE
Failed nutrient adsorption(Santacroce et al., 2008)
Yellowish skin
There are three stages of aflatoxicosis: acute, subacute, and chronic.
HepatotoxicityImmunosuppression
AnaemiaWhitishor pale gills
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.
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.
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).
AFLATOXICOSISCHRONIC
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.
The chronic stage of aflatoxin exposure is associated with: HaematologicalMutagenicityHepatotoxicityImmunosuppressionCarcinogenicityalterations
9 O O HO H O OH HO
DON
Fusarium moulds produce a variety of potent mycotoxins, but three of them have so far undergone substantial research studies (Placinta et al., 2016):
(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).
Fusarium mycotoxins
ZearalenoneFumonisinsTrichothecenes
T-2
TRICHOTHECENES
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).
Nivalenol (NIV)
TRICHOTHECENES
T-2 TOXIN
Fusarium contamination can happen alone or with other mycotoxins (Placinta et al., 1999).
When ingested, trichothecenes act as inhibitors of protein biosynthesis, disrupting the entire process from initiation to termination.
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)
Diacetoxyscirpenoltoxin (DAS)
They also weaken immunity and impair the function of the nervous system (Kumar et al., 2013). DAS
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.
The two most toxic trichothecenes in aquaculture are T-2 toxin and DON.
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T-2 TOXIN
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.
Animals exposed to trichothecenes for a long time show various clinical signs, such as:
Cessation of feeding
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).
Growth restriction
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).
Sluggish movement
Tissue lesions
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.
Higher doses of this mycotoxin also trigger shock-like syndrome, eventually resulting in mortality (Matejova et al., 2017a).
Significantly reduced growth rate and feed utilization indexes, as well as lesions in the intestine and liver ,were reported in this study.
Growth retardation
Inflammation
(Hooft et al., 2011)
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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.
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.
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).
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.
At the end of this trial, significant growth and growth hormone reduction and poor nutrient utilization were detected.
Pathological signs of vomitoxin ingestion aquaculture species include:
DeoxynivalenolDON
, 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).
Poor nutrient Immunosuppressionutilization
Poor nutrient utilization
Degenerated and sloughed intestine
Fumonisin B1, therefore, acts as an inhibitor of sphingolipid synthesis which is crucial for membrane and lipoprotein structures (Wang et al., 1992).
Growth retardation
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:
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).
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 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).
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 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).
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).
OCHRATOXINS
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.
ZEARALENONE
Significant reduction of growth and feed utilization indices, as well as higher antioxidant enzymes in fish muscles, were reported in this study.
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).
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
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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.
Aflatoxin 1.2 mg/kg- 21 days Brain lesions, blood-brain barrier disruption, and behavioural changes. Baldissera et al. (2018)
C. carpio (Common carp) Zearalenone 0.33, 0.62, 0.78 mg/kg- 4 weeks Increased immunity at lower and significantly reduced immunity at higher toxic levels (dose). Pietsch et al. (2015)
In the second part of this article, we will discuss the variety of mycotoxin adsorbing agents and feed additives used in aquaculture and their efficacy.
Reduction in the antioxidant capacity of the fish, lesions, and injury of gills and their tight junctions. Huangetal.(2020)
O. mykiss (Rainbow trout) Zearalenone 1.81 mg/kg- 70 days Structural liver disorganization, necrosis, damaged hepatocytes, and cytoplasmic vacuolation Woźnyetal.(2015)
Irregular and shrunken gill lamellae, necrotic liver hepatocytes, vascular congestion, damaged liver parenchyma, renal urinary space dilation, abnormal increase in goblet cells, sloughed intestines, and inflammation.
O. mykiss (Rainbow trout) T-2 toxin 1–1.8 mg/kg- Increased leukocyte and lymphocyte and considerably decreased non-specific immunity. Modra et al. (2020)
O. niloticus (Nile tilapia) Aflatoxin 2 mg/kg- 170 days Reduced growth, fecundity, gonad somatic index, and milt quality. Marijanietal.(2019)
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Damaged intestinal mucosal barrier and halted apoptosis, oxidative stress, lesions in gills. Huangetal.(2018a)
O. niloticus (Nile tilapia) Aflatoxin 0.1 mg/kg- 12 weeks Decreased growth, feed utilization, haematological indices, and resistance to A. hydrophila, as well as damaged liver and increased antioxidant enzymes. Mahfouzetal.(2015)
Ochratoxin A 1.2, 1.6, 2.0, 2.4 mg/kg60 days
Fumonisin 10, 20, 40, 80 mg/kg -56 days
Salmo salar (Atlantic salmon) Deoxynivalenol 5.5 mg/kg- 8 weeks Lowered growth, feed and protein efficiency, as well as negatively affected intestinal integrity. Moldal et al. (2018)
Wu et al. (2019)
C. carpio (Common carp) Zearalenone 0.33, 0.62, 0.78 mg/kg- 4 weeks Significantly reduced gene expression of immune, antioxidative, and estrogenic functions. Pietsch (2017)
Ghafarifarsani et al. (2021)
Aflatoxin 0.2 mg/kg- 70 days
Shahafveetal.(2017)
C. idella (Grass carp) Deoxynivalenol 0.03, 0.32, 0.63, 0.92, 1.24 mg/kg -8 weeks
Table 2. Summary of recent studies on the effect of mycotoxins in different aquatic animals. Dose, duration, and toxicity are reviewed.
C. idella (Grass carp) Deoxynivalenol 0.03, 0.32, 0.63, 0.92, 1.24 mg/kg - 60 days
Ochratoxin A 2.4 mg/kg- 35 days Reduction of growth and feed utilization as well as higher antioxidant enzymes. Baldissera et al. (2020)
Heterobranchus longifilis (Catfish)
Litopenaeus vannamei (Pacific white shrimp) Aflatoxin 0.005 mg/kg- 30 days Lower gut microbiota abundance and higher antioxidant enzymes. Wangetal.(2018)
Moniliformin 20, 40, 60, 120 mg/kg- 10 weeks
Dicentrarchus labrax (Sea bass) Ochratoxin A 9.23 mg/kg- 3 days Lethargy, loss of balance, haemorrhaging, vascular dilatation and congestion, and damaged kidney. El-Sayedetal.(2009)
Clarias gariepinus juv. (African catfish) Fumonisin B1 &Aflatoxin B1 0.048 (AB1)+43.0 (FB1), 0.093 (AB1)+83 (FB1) mg/kg
Cyprinus carpio (Common carp) Aflatoxin 0.5, 0.7 and 1.4 mg/kg- 3 weeks
Significant growth reduction. Adeyemoetal.(2016)
Significant reductions in growth, weight gain, feed utilization, erythrocytes, haemoglobin, and haematocrit counts, leukopaenia and anaemia. Adeyemoetal.(2018)
Significantly lower growth performance and mortality (%4). Yildirim et al. (2000)
O. niloticus (Nile tilapia) Moniliformin 70,150 mg/kg- 28 days Significantly decreased growth and red blood cells. Tuan et al. (2003)
Colossoma macropomum (Tambaqui)
Oncorhynchus mykiss (Rainbow trout) Aflatoxin 1.2 mg/kg- 21 days, Premature mortality. Nomura et al. (2011)
Aquatic animal Mycotoxin Dose, duration Toxic effects Reference Bagrus filamentosus (Silver catfish)
O. mykiss (Rainbow trout) zearalenoneAflatoxin& Varies- 60 days Reduced growth, feed utilization, digestive enzymes, immune response, and decreased goblet cells and villi length.
Danio rerio (Zebrafish) Zearalenone 0.01 and 0.03 mg/kg- 3 weeks Reduced fertility and spawning frequency. Schwartzetal.(2010),
Danio rerio larvae (Zebrafish) Aflatoxin 75 ng/mL- unspecified Neurotoxicity; hyperlocomotion.
Ctenopharyngodon idella (Grass carp)
Cyprinus carpio (Common carp) T-2 toxin 5.3 mg/kg -30 days Negatively affected haematological indices such as haemoglobin, red and white blood cells, reduced antioxidant enzymes, and tissue lesions. Matejovaetal.(2017)
Oreochromis niloticus (Nile tilapia)
O.niloticus (Nile tilapia) Fumonisin 20, 40, 60 mg/kg -30 days Significant growth and growth hormone reduction and poor nutrient utilization, Claudino-Silva et al. (2018)
Reduced Red blood cells, white blood cells, haemoglobin, growth and survival rates. Selim et al. (2014)
Ictalurus punctatus (Channel catfish)
Growth retardation, sloughing intestinal lining, poor nutrient utilization, and oxidative stress. Liu et al. (2020)
Escrivá, L., Font, G. and Manyes, L., 2015. In vivo toxicity studies of fusarium mycotoxins in the last decade: A review. Food and Chemical Toxicology, 78, 185-206.
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Baldissera, M.D., Souza, C.F., Zeppenfeld, C.C., Descovi, S.N., Moreira, K.L.S., da Rocha, M.I.U., da Veiga, M.L., da Silva, A.S. and Baldisserotto, B., 2018. Aflatoxin B1-contaminated diet disrupts the blood–brain barrier and affects fish behavior: involvement of neurotransmitters in brain synaptosomes. Environmental Toxicology and Pharmacology, 60, 45-51.
Alceste, C. and Jory, D.E., 2000. Tilapia alternative protein sources in tilapia feed formulation. Aquaculture Magazine-Arkansas, 26(4), 70-75. Alinezhad, S., Tolouee, M., Kamalzadeh, A., Motalebi, A.A., Nazeri, M., Yasemi, M., Shams, G.M., Tolouei, R. and Razzaghi, A.M., 2011. Mycobiota and aflatoxin B1 contamination of rainbow trout (Oncorhynchus mykiss) feed with emphasis to Aspergillus section Flavi. Iranian Journal of Fisheries, 10(3), 363-374.
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Di Gregorio, M.C., Neeff, D.V.D., Jager, A.V., Corassin, C.H., Carão, Á.C.D.P., Albuquerque, R.D., Azevedo, A.C.D. and Oliveira, C.A.F., 2014. Mineral adsorbents for prevention of mycotoxins in animal feeds. Toxin Reviews, 33(3), 125-135.
Baldissera, M.D., Souza, C.F., da Silva, J.A., Barroso, D.C., Glória, E.M., Mesadri, J., Wagner, R., Baldisserotto, B. and Val, A.L., 2020. Dietary ochratoxin A (OTA) decreases growth performance and impairs the muscle antioxidant system and meat fatty acid profiles in juvenile tambaqui (Colossoma macropomum). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 236, 108803.
Anater, A., Manyes, L., Meca, G., Ferrer, E., Luciano, F.B., Pimpao, C.T. and Font, G., 2016. Mycotoxins and their consequences in aquaculture: A review. Aquaculture, 451, 1-10.
Corcuera, L.A., Vettorazzi, A., Arbillaga, L., Gonzalez-Peñas, E. and De Cerain, A.L., 2012. An approach to the toxicity and toxicokinetics of aflatoxin B1 and ochratoxin A after simultaneous oral administration to fasted F344 rats. Food and Chemical Toxicology, 50(10), 3440-3446.
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Adeyemo, B.T., Tiamiyu, L.O., Ayuba, V.O. and Cheikyula, J.O., 2016. Effects of dietary fumonisin B1 on hematology and growth performance of the clariid fish Heterobranchus longifilis. J. Agric. Vet. Sci, 9, 26-33.
Almeida, I.F.M., Martins, H.M.L., Santos, S.M.O., Freitas, M.S., da Costa, J.M.G.N. and d´ Almeida Bernardo, F.M., 2011. Mycobiota and aflatoxin B1 in feed for farmed sea bass (Dicentrarchus labrax). Toxins, 3(3), 163-171.
Adeyemo, B.T., Tiamiyu, L.O., Ayuba, V.O., Musa, S. and Odo, J., 2018. Effects of dietary mixed aflatoxin B1 and fumonisin B1 on growth performance and hematology of juvenile Clarias gariepinus catfish. Aquaculture, 491, 190-196.
Cagauan, A.G., Tayaban, R.H., Somga, J.R. and Bartolome, R.M., 2004, September. Effect of aflatoxin-contaminated feeds in Nile tilapia (Oreochromis niloticus L.). In: Abstract of the 6th International Symposium on Tilapia in Aquaculture (ISTA 6) Section: Health Management and Diseases, Manila, Philippines (Vol. 12, pp. 16).
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