Current knowledge about fumonisins in aquaculture, report from Biomin

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.

Conclusion

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.