Fumonisins in aquaculture: The most sensitive species
by Rui A Gonçalves, Biomin Holding, Austria
In aquaculture, fumonisins (FUM) have generally been associated with reduced growth rate, feed consumption and feed efficiency, and impaired sphingolipid metabolism. Fumonisin toxicity
is related to this ability to inhibit sphinganine (sphingosine) N-acyltransferase (ceramide synthase), a key enzyme in lipid metabolism, disrupting this pathway. This is due to the long-chain hydrocarbon unit (similar to that of
sphingosine and sphinganine) in these mycotoxins, which plays a role in their toxicity.
Sensitivity of freshwater species
Little information is available on the effects of fumonisins on aquaculture species, and most research focuses on freshwater species.
The channel catfish (Ictalurus punctatus) is the most widely studied species. These fish can tolerate relatively high levels of FUM, with a sensitivity level of around 10 mg fumonisin B1 (FB1)/kg feed. Adverse effects of fumonisin-contaminated diets have also been reported in carp (Cyprinus carpio L.): various experiments have observed scattered lesions in the exocrine and endocrine pancreas, and interrenal tissue, probably due to ischemia and/or increased endothelial permeability.
In another study by Pepeljnjak et al., 2003, one-year-old carp were fed pellets containing 500, 5,000 or 150,000 μg FB1/
kg body weight, resulting in weight loss and alterations in hematological and biochemical parameters in target organs.
Tuan et al. (2003) demonstrated that feeding FB1 to tropical species at 10, 40, 70 and 150 mg/kg feed for 8 weeks affected growth in Nile tilapia (Oreochromis niloticus) fingerlings. In this experiment, average weight gain in fish fed diets containing 40,000 μg FB1/kg or more were lower. Hematocrit was only reduced in the tilapia given 150,000 μg FB1/kg feed. The ratio of free sphinganine to free sphingosine (Sa:So ratio) in the liver increased at 150,000 μg FB1/kg feed.
Pacific whiteleg shrimp
To the author"s knowledge, the only crustacean species studied to date with respect to sensitivity to FUM is the Pacific whiteleg shrimp (Litopenaeus vannamei). Despite slight variations in testing levels, the few studies available suggest that Litopenaeus vannamei is much more sensitive to FB1 than previously described in freshwater species. García-Morales et al. (2013) have shown that soluble muscle protein concentration was reduced, and changes were observed in the thermodynamic properties of myosin, after 30 days" exposure to FUM in Pacific whiteleg shrimp fed 20 to 200 μg FB1/kg feed.
The same authors reported marked histological changes in the tissues of shrimp fed a diet containing 200 μg FB1/kg feed, and changes in meat quality after 12 days of ice storage in fish fed more than 600 μg FUM/kg feed. The effect of FUM on muscle quality may be of great importance, especially for shrimp- exporting countries, as it directly affects shelf life. The study by Burgos-Hernández et al. in 2005 also confirmed that FB1 causes histological changes in the shrimp hepatopancreas as a result of alterations in trypsin and collagenase activity.
Mexía-Salazar et al. (2008) also observed marked histological changes in the hepatopancreas, as well as necrotic tissue, in shrimp fed 500 μg FB1/kg. These authors also observed changes in both the electrophoretic patterns and the thermodynamic properties of the myosin extracted from shrimp exposed to FB1.
Marine species as more susceptible
All aquaculture species tested for sensitivity to FUM to
date have been omnivorous or herbivorous, and all have been freshwater species, with the exception of whiteleg shrimp. High levels of FUM have been measured in plant meals commonly used for carnivorous marine species, but there have been no studies investigating the possible effect of FUM on marine species. To fill this knowledge gap, two trials were carried out in marine species, where there is potential to use plant meals.
One of the studies was conducted with gilthead seabream (Sparus aurata), one of the most important aquaculture species farmed in Europe and a good model to study the effect of FUM on carnivorous marine species.
In this study, which is still being evaluated, triplicate groups of 35 gilthead seabream (315 fish in total), with a mean initial body weight (IBW) of 28.8 ± 2.1 g were fed one of three experimental diets for 60 days. The experimental diets were: FUM 1, containing 168 μg FUM/kg feed; FUM 2, containing 333 μg FUM/kg; and a control diet, free of mycotoxins.
Preliminary results indicate that the FUM inclusion levels tested affect total growth. Table 1 summarises the effect of FUM at 168 and 333 μg/kg feed on the main growth indicators: final body weight (FBW), specific growth rate (SGR), feed conversion ratio (FCR), feed intake (FI) and protein efficiency ratio (PER), compared to the control diet. The FUM levels tested did not affect survival rates.
A second study was carried out in turbot (Psetta maxima; formerly Scophthalmus maximus), a benthic carnivorous species, considered to be the most important flatfish species farmed in Europe and one with a great potential for East Asia. In this study, which is still being evaluated, triplicate groups of 30 turbot (450 fish in total) with a mean initial body weight (IBW) of 83.7 ± 2.9 g were fed diets containing 0.5, 1.0, 2.0 or 5.0 mg FUM/kg for 63 days (diets labeled FUM 0.5, FUM 1.0, FUM 2.0 and FUM 5.0, respectively).
Results to date demonstrate that 5 mg FUM/kg feed significantly increased mortality (p < 0.05). Final mean body weight, specific growth rate and protein efficiency ratio were significantly lower in the fish fed the FUM 1.0, FUM 2.0 and FUM 5.0 diets, and feed conversion ratio was higher, than fish fed the control or FUM 0.5 diets. 1–5 mg FUM/kg feed reduced the height of the villi in the distal intestine brush border and reduced hepatic lipid inclusion (p < 0.05).
Results to date from these two trials
are of great potential interest. To our
knowledge, they are the first trials
conducted in marine species, investigating a pelagic and a benthic species. Furthermore, FUM levels tested in previous trials are within the contamination levels often found in commercial aquafeeds, which highlights the importance of screening and preventing FUM in feeds.
Marine fish and shrimp species may be highly sensitive to relatively low fumonisin levels (< 5000 μg FUM/kg feed), affecting growth performance and immune status. This is much lower than the sensitivity levels of most freshwater species, and also lower than livestock species.
This presents additional challenges to the marine aquaculture sector as the European Commission guidance values for
FUM (fumonisins B1 + B2) in complementary and complete feedingstuffs for fish is 10 mg FUM/kg feed (European Commission, 2006), which might be too high, at least for Sparus aurata, Psetta maxima and Litopenaeus vannamei. Further research is required to confirm whether other marine species are as sensitive to FUM, and to better understand the effect of other mycotoxins co-occurring with FUM.
Synergism can reduce sensitivity levels
Although FUM is the predominant mycotoxin in plant meals and the subsequent feed, an average of 80 percent of all finished feed samples are contaminated with more than one mycotoxin.
It is, therefore, important to understand the effects of FUM and its interaction with other mycotoxins that may be present in the feed, especially other Fusarium mycotoxins that are produced alongside FUM. Synergism, i.e. the interaction of two or more mycotoxins to cause a combined effect that is greater than the sum of their separate effects, has not been fully described in aquaculture. However, aflatoxin B1 and fumonisins are known to interact synergistically in fish and shrimp. The study conducted by Mckean et al. (2006) in mosquitofish (Gambusia affinis) describes the synergistic effect of aflatoxin and fumonisins perfectly.
The authors observed that mortality only starts to increase (to 17%) above 2,000 ppb FUM and similar mortality is seen at aflatoxin levels of 215 ppb. However, when both mycotoxins were combined, the authors found that mortality increased to 75 percent at 1,740 ppb FUM plus 255.4 ppb AF.
This synergistic effect was also observed in rainbow trout (Oncorhynchus mykiss) with AFB1 at 100 ppb and FB1 at
3,200 ppb (Carlson et al., 2001); in Pacific white leg shrimp (Litopenaeus vannamei) with 300 ppb AFB1 and 1,400 ppb FB1; and in African catfish (Clarias gariepinus) with AFB1 at 7.3 ppb and FB1 at 15,000 ppb.
Seabream, turbot, and Pacific whiteleg shrimp appear to be highly sensitive to FUM contamination. Sensitivity levels in these species are below the European Commission guidance values
for FUM (fumonisins B1 + B2) in complementary and complete feedingstuffs for fish of 10 mg FUM/kg feed.
We understand that these guidance values are based on the sensitivity of freshwater aquaculture species. The immense diversity of species makes it difficult to produce guidelines for the aquaculture industry. Further evaluation of FUM sensitivity in other marine species is essential to determine the risk that FUM may present to aquaculture feed manufacturers and farmers.
Although freshwater species are less sensitive to FUM, it is important to remember that feeds used in these species contain high levels of a wide range of plant proteins. This significantly increases the probability of mycotoxin co-occurrence in freshwater aquafeeds, increasing sensitivity to these mycotoxins in the feed.