Current Knowledge about Fumonisins in Aquaculture
What are fumonisins?
Fumonisins (FUM) are a group of mycotoxins discovered in 1988 in South Africa (Gelderblom et al., 1988). The group includes FB1, FB2 and FB3. They are mainly produced by a number of Fusarium species, notably F. verticillioides (formerly F. moniliforme = Gibberella fujikuroi), F. proliferatum, and F. nygamai. The most abundantly produced mycotoxin of the Fusarium family is fumonisin B1 (FB1). Fumonisins are characterized as having a long-chain hydrocarbon unit, similar to that of sphingosine and sphinganine, which plays a role in their toxicity (Wang et al., 1992). Fumonisins inhibit the sphinganine (sphingosine) N-acyltransferase (ceramide synthase), a key enzyme in lipid metabolism, resulting in disruption of this pathway. This enzyme catalyzes the acylation of sphinganine in the biosynthesis of sphingolipids. Sphingolipids are important for the membrane and lipoprotein structure, and also for cell regulations and communications (Berg et al., 2003).
The occurrence, level of contamination and implications of mycotoxins entering the feed chain through cereal grains have gained global attention in recent years. The aquaculture industry is no exception to this rise in awareness. Figure 1 shows the occurrence of fumonisins in corn, one of the major commodities affected by this group of toxin. Since 2015, there has been a global trend towards increasing fumonisin levels in corn. This trend is also reflected in other commodities commonly used for aquafeed production. Table 1 shows the mycotoxin contamination in important commodities and finished feeds sampled worldwide between January and December 2017. Corn, corn gluten meal (CGM), dried distillers with solubles (DDGS) and rice bran samples presented the highest occurrence of FUM. With the exception of rice bran, which had a relatively low level of contamination (161 ppb), corn, CGM and DDGS were contaminated with FUM levels of over 2,900 ppb. As FUM is relatively stable against high temperature and processing conditions, it is expected that FUM will be found in finished feeds, as confirmed by analyses of finished feed samples taken in the same reporting period (Table 1.5). In 2017, FUM was the most predominant mycotoxin, present in 81% of the collected samples with an average contamination level of 1,352 ppb.
An important factor that also negatively affects aquaculture species is the co-occurrence of mycotoxins; the simultaneous presence of more than one mycotoxin in the same sample. 80% of finished feed samples collected in 2017 were contaminated by more than one mycotoxin (Figure 2).
Fumonisin occurrence in Asia: a glimpse at 2018 samples
Table 2 shows the mycotoxin contamination in plant commodities and finished feeds sampled in Asia between January and March 2018. Samples from China and India are shown in Tables 3 and 4, respectively. The trend observed in the first quarter of 2018 continues the 2017 trend. Samples from China showed the highest contamination level for FUM in both plant commodities (2,767 ppb) and finished feeds (1,765 ppb).
Can fumonisin negatively affect aquaculture species?
In aquaculture, FUM has been generally associated with reduced growth rate, lower feed consumption, poor feed efficiency ratios, and impaired sphingolipid metabolism (Goel et al., 1994; Li et al., 1994; Lumlertdacha and Lovell, 1995; Tuan et al., 2003). However, information on the eﬀects of FUM in the most important aquaculture species is scarce, with most of the available research focusing on freshwater species.
Channel catfish (Ictalurus punctatus) is the most studied species (Goel et al., 1994; Li et al., 1994; Lumlertdacha et al., 1995; Lumlertdacha and Lovell, 1995). According to the cited authors, channel catfish can tolerate relatively high levels of FUM, with a sensitivity level of around 10 ppb.
It is known that liver tissue of rainbow trout (Oncorhynchus mykiss) is sensitive to FUM, inducing changes in sphingolipid metabolism at levels lower than 100 µg/kg (Meredith et al., 1998) and inducing cancer in one-month-old trout (Riley et al., 2001). It was observed that animals fed 1,000, 5,000, 10,000 or 20,000 µg/kg FB1 for ten weeks appeared unaffected in terms of growth, feed intake and liver damage (García, 2013). However, the study also reported observations that all fish (including those in the control group) had very poor feed intake and growth, presenting specific growth rate values two to six times lower than the average reported in other studies (Farmer et al., 1983; McCormick et al., 1998).
The adverse effects of FUM-contaminated diets have also been reported in carp (Cyprinus carpio L.). One-year-old carp showed signs of toxicity at 10,000 µg FB1/kg feed (Petrinec et al., 2004). The experiments reported the presence of scattered lesions in the exocrine and endocrine pancreas and inter-renal tissue, probably due to ischemia and/or increased endothelial permeability. In another study, one-year-old carp consumed pellets contaminated with 500, 5,000 or 150,000 µg FB1/kg of body weight, resulting in a loss of body weight and alterations of hematological and biochemical parameters in target organs (Pepeljnjak et al., 2003). For tropical species, Tuan et al. (2003) demonstrated that feeding FB1 at 10, 40, 70 or 150 mg/kg feed for eight weeks affected the growth performance of Nile tilapia (Oreochromis niloticus) fingerlings. In the same experiment, fish fed diets containing FB1 at levels of 40,000 µg/kg or higher showed decreased average weight gains.
Hematocrit was only decreased in tilapia fed diets containing 150,000 µg FB1/kg. The ratio between free sphinganine and free sphingosine (Sa:So ratio) in the liver increased when 150,000 µg FB1/kg was present in the fish feed. Fumonisin B1 has not been extensively studied as a shrimp feed contaminant. However, the few studies available suggest that Pacific white leg shrimp (Litopenaeus vannamei) are sensitive to FB1. García-Morales et al. (2013) showed that white leg shrimp fed FB1 at 20 to 200 µg/kg had a reduced soluble muscle protein concentration and reported changes in myosin thermodynamic properties after 30 days of FUM exposure. The same authors reported marked histological changes in tissue samples of shrimp fed a diet containing 200 µg FB1/kg and meat quality changes after 12 days of ice storage when fish were fed diets containing more than 600 µg FUM per kg of feed.
Are marine species sensitive?
All the FUM-sensitive aquaculture species tested so far, are all omnivorous or herbivorous, and all are freshwater species.
In contrast to freshwater species, the liver in marine fish plays an essential role in lipid metabolism. It is a sensitive organ reflecting any lipid metabolism changes, which might influence the essential pathways of n-3 long-chain polyunsaturated fatty acids (EPA and DHA) biosynthesis and metabolism (Li et al., 2018). The known mode of action of FUM is inhibition of ceramide synthase, a key enzyme in lipid metabolism. It is therefore expected that FUM has a negative impact on the lipid metabolism of marine species. Based on this theoretical rationale, BIOMIN performed some ground-breaking studies in marine species. As expected, these studies showed that marine species were highly sensitive to FUM, affecting growth performance and immune status at relatively low FUM levels (< 5,000 μg/kg).
However, according to the European Commission (EC), the guidance values for FUM (fumonisins B1 + B2) in complementary and complete feeding stuffs for fish is 10 ppm (European Commission, 2006). This is a reason for concern, as new BIOMIN data suggests that the guidance values might be too high, at least for marine species.
Synergism: the most important concept
FUM is the most predominant mycotoxin in plant meals and consequently in finished feeds. However, 80% of all finished feed samples tested during 2017 were contaminated with more than one mycotoxin (Figure 2). It is important to know the effects of FUM in addition to its interaction with other mycotoxins present in the feed. Synergism, i.e., the interaction of two or more mycotoxins to produce a combined effect greater than the sum of their separate effects, is not very well described in aquaculture. However, studies have shown that Aflatoxin B1 (AFB1) and FUM have a synergistic effect in fish (Carlson et al., 2001; McKean et al., 2006; Adeyemo et al., 2018) and shrimp (Pérez-Acosta et al., 2016).
The study conducted by McKean et al. (2006) in mosquitoﬁsh (Gambusia aﬃnis) perfectly describes the synergistic effect between AFB1 and FUM. The authors observed that mortality started to increase only above 2,000 ppb of FUM reaching 17%. A similar mortality rate was obtained for AFB1 levels of 215 ppb. However, when combining both mycotoxins, the authors observed that mortality increased to 75% at concentrations of 1,740 ppb of FUM combined with 255.4 ppb of AFB1. The same synergistic effect was also observed in other species as detailed in Table 5.
Direct mortality, especially in short-term feeding trials (up to four weeks), is an extreme consequence of the combined levels of AFB1 and FB1. Under commercial aquaculture conditions, lower levels of AFB1 and FB1 are expected to generate a decrease in growth performance and an increase in disease vulnerability.
Fumonisins were present in the majority of raw materials sampled in the BIOMIN Mycotoxin Survey in 2017, a trend that is likely to continue based on the analysis of samples gathered in the first quarter of 2018. Although research into fumonisins is scarce, fumonisin contamination has been directly linked to decreased performance levels in aquaculture. The majority of research is focused on freshwater species, but new BIOMIN data that is soon to be published conducted in marine species suggests that sensitivity levels may be lower than previously thought. The majority of finished feed samples are contaminated with more than one mycotoxin, highlighting both the importance of understanding mycotoxin synergisms when diagnosing performance problems and the importance of constructing mycotoxin mitigation strategies.
- Fumonisins are the predominant mycotoxin contaminant in raw materials and finished feed samples worldwide.
- Aquaculture performance indicators are compromised when fumonisins are present in the feed.
- Synergies with other mycotoxins, especially aflatoxin, compound the negative impact of fumonisins in aquaculture feeds.
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 haematology of juvenile Clarias gariepinus catfish. Aquaculture 491: 190-196.
Berg JM, Tymoczko JL, Stryer L. Biochemistry. 5th edition. New York:
W H Freeman; 2002. Available from: https://www.ncbi.nlm.nih.gov/books/NBK21154/.
Carlson, D.B., Williams, D.E., Spitsbergen, J.M., Ross, P.F., Bacon, C.W., Meredith, F.I. and Riley, R.T. (2001). Fumonisin B1 Promotes Aflatoxin B1 and N-Methyl-N´-nitro-nitrosoguanidine-Initiated Liver Tumors in Rainbow Trout. Toxicology and Applied Pharmacology 172(1): 29-36.
European Commission. (2006). Commission Recommendation of 17 August 2006 on the presence of deoxynivalenol, zearalenone, ochratoxin A, T-2 and HT-2 and fumonisins in products intended for animal feeding. [On-line]. Available at: eur-lex.europa.eu/LexUriServ/LexUriServ.do. Accessed 11.09.18.
Farmer, G.J., Ashfield, D. and Goff, T.R. (1983). A feeding guide for juvenile Atlantic salmon. Can. MS. Rep. Fish. Aquat. Sci 1718: 1-13.
García-Morales, M-H., Pérez-Velázquez, M., González-Felix, M.L., Burgos-Hernández, A., Cortez-Rocha, M-O., Bringas-Alvarado, L. and Ezquerra-Brauer, J-M. (2013). Effects of Fumonisin B1-Containing Feed on the Muscle Proteins and Ice-Storage Life of White Shrimp (Litopenaeus vannamei). Journal of Aquatic Food Product Technology 24(4): 340-353.
García, E.C. (2013). Effects of fumonisin B1 on performance of juvenile Baltic salmon (Salmo salar). Department of Biological and Environmental Science, University of Jyväskylä, Faculty of Science MSc.
Gelderblom, W.C., Jaskiewicz, K., Marasas, W.F., Thiel, P.G., Horak, R.M., Vleggaar, R. and Kriek, N.P. (1988). Fumonisins - novel mycotoxins with cancer-promoting activity produced by Fusarium moniliforme. Appl. Environ. Microbiol. 54(7): 1806-1811.
Goel, S., Lenz, S.D., Lumlertdacha, S., Lovell, R.T., Shelby, R.A., Li, M., Riley, R.T. and Kemppainen, B.W. (1994). Sphingolipid levels in catfish consuming Fusarium moniliforme corn culture material containing fumonisins. Aquat. Toxicol 30(4): 285- 294.
Li, M.H., Raverty, S.A. and Robinson, E.H. (1994). Effects of dietary mycotoxins produced by the mold Fusarium moniliforme on channel catfish Ictalurus punctatus. J. World Aquac. Soc. 25(4): 512-516.
Li, Y., Jia, Z., Liang, X., Matulic, D., Hussein, M. and Gao, J. (2018). Growth performance, fatty-acid composition, lipid deposition and hepatic-lipid metabolism-related gene expression in juvenile pond loach Misgurnus anguillicaudatus fed diets with different dietary soybean oil levels. Journal of Fish Biology 92(1): 17-33.
Lumlertdacha, S. and Lovell, R. (1995). Fumonisin-contaminated dietary corn reduced survival and antibody production by channel catfish challenged with Edwardsiella ictaluri. J Aquatic Anim Health 7(1): 1 - 8.
Lumlertdacha, S., Lovell, R.T., Shelby, R.A., Lenz, S.D. and Kemppainen, B.W. (1995). Growth, hematology, and histopathology of channel catfish, Ictalurus punctatus, fed toxins from Fusarium moniliforme. Aquaculture 130(2): 201- 218.
McCormick, S.D., Shrimpton, J.M., Carey, J.B., O’Dea, M.F., Sloan, K.E., Moriyama, S. and Björnsson, B.Th. (1998). Repeated acute stress reduces growth rate of Atlantic salmon parr and alters plasma levels of growth hormone, insulin-like growth I and cortisol. Aquaculture 168: 221-235.
McKean, C., Tang, L., Tang, M., Billam, M., Wang, Z., Theodorakis, C.W., Kendall, R.J. and Wang, J-S. (2006). Comparative acute and combinative toxicity of aflatoxin B1 and fumonisin B1 in animals and human cells. Food and Chemical Toxicology 44(6): 868-876.
Meredith, F.I., Riley, R.T., Bacon, C.W., Williams, D.E. and Carlson, D.B. (1998). Extraction, quantification, and biological availability of fumonisin B1
incorporated into the Oregon test diet and fed to rainbow trout. J Food Prot 61(8): 1034-1038.
Pepeljnjak, S., Petrinec, Z., Kovacic, S. and Klarić, M. (2003). “Screening toxicity study in young carp (Cyprinus carpio L.) on feed amended with fumonisin B1.” Mycopathologia 156: 139-145.
Pérez-Acosta, J.A., Burgos-Hernandez, A., Velázquez-Contreras, C.A., Márquez-Ríos, E., Torres-Arreola, W., Arvizu-Flores, A.A. and Ezquerra-Brauer, J.M. (2016). An in vitro study of alkaline phosphatase sensitivity to mixture of aflatoxin B1 and fumonisin B1 in the hepatopancreas of coastal lagoon wild and farmed shrimp Litopenaeus vannamei. Mycotoxin Research 32(3): 117-25.
Petrinec, Z., Pepeljnjak, S., Kovacic, S. and Krznaric, A. (2004). Fumonisin B1 causes multiple lesions in common carp (Cyprinus carpio). Dtsch. Tierarztl. Wochenschr: 358-363.
Riley, R.T., Enongene, E., Voss, K.A., Norred, W.P., Meredith, F.I., Sharma, R.P., Spitsbergen, J., Williams, D.E., Carlson, D.B. and Merrill, A.H.Jr. (2001). Sphingolipid perturbations as mechanisms for fumonisin carcinogenesis. Environmental Health Perspectives 109 (Suppl 2): 301-308.
Tuan, N.A., Manning, B.B., Lovell, R.T. and Rottinghaus, G.E. (2003). Responses of Nile tilapia (Oreochromis niloticus) fed diets containing different concentrations of moniliformin or fumonisin B1. Aquaculture 217(1): 515-528.
Wang, E., Norred, W.P., Bacon, C.W., Riley, R.T. and Merrill, A.H.Jr. (1991). Inhibition of sphingolipid biosynthesis by fumonisins. Implications for diseases associated with Fusarium moniliforme. The Journal of Biological Chemistry 266(22): 14486-14490.
Wang, E., Ross, F.P., Wilson, T.M., Riley, R.T. and Merrill, A.H.Jr. (1992). Increases in serum sphingosine and sphinganine and decreases in complex sphingolipids in ponies given feed containing fumonisins, mycotoxins produced by Fusarium moniliforme. J. Nutr. 122(8): 1706-1716.