Effects of mycotoxins in aquatic species

Studies on the effects of mycotoxins in aquatic species are scarce, and in most cases the concentrations used are unrealistically high. Nevertheless, in recent years some key publications and reviews have brought some interesting results to light.

The occurrence of mycotoxins in aquatic feeds and their effects is a topic that continues to gain attention due to the general trend of replacing expensive animal protein sources with cheaper plant derived proteins. The chemical and thermal stability of mycotoxins renders their molecules unsusceptible to damage during common feed manufacturing procedures like extrusion.

Aflatoxins

Aflatoxins are highly carcinogenic and their concentration is strictly regulated in many markets worldwide. Several aquatic species are sensitive to these mycotoxins. In 2010, a study conducted on sea bream (Sparus aurata) revealed that hepatocytes are affected by aflatoxin B1 at different lengths  of exposure (24, 48, and 72 hours).1 Weight gain and FCR of Beluga (Huso huso) can be negatively affected by concentrations of aflatoxin B1 ranging from 20 to 100 ppb. Changes in liver tissue, fat deposition and necrosis were also observed in this species after 60 days of exposure.2 In hybrid sturgeon (Acipenser ruthenus x A. baeri) fed a diet containing 80 ppb of aflatoxin B1, mortality increased after 12 days of exposure. Histopathological changes such as necrosis, presence of inflammatory cells and biliary enlargement were observed as well as accumulation of aflatoxin B1 in the muscles and liver.3 Growth rate and FCR of Nile tilapia are affected by dietary aflatoxin at concentrations ranging from 100 to 2500 ppb.4,5,6,7 In tilapia, studies conducted at lower aflatoxin concentrations (50 ppb) revealed alteration of liver parameters (necrosis and vacuolization of hepatocytes).4 Aflatoxin B1 showed immunosuppressive effects on rohu (Labeo rohita) and was able to induce oxidative damage to primary target organs such as the liver, kidneys and brain. Weight gain, survival and feed efficiency were also negatively affected in red drum (Sciaenops occellatus). Pacific blue shrimp is susceptible to aflatoxin B1 at relatively high concentrations (LD50= 100 ppb after 24 hours). Black tiger shrimp is even more sensitive, as 50 ppb aflatoxin B1 was enough to cause a 46-59% decrease in body weight (BW) of the treated group compared to the control.8 

more about Aflatoxins

Fumonisins

Studies investigating the effects of Fumonisins (FUM) are also scarce. These mycotoxins are toxic to channel catfish, as animals exposed to 100 ppb fumonisin B1 (FB1) showed changes in the sphingolipids metabolism.18 Concentrations of FB1 lower than 100 ppb were able to induce cancer in one-month-old trout.19 Concentrations of dietary FB1 ranging from 10 to 150 ppb negatively affected the growth parameters of Nile tilapia fingerlings.6 Toxic effects derived from exposure to dietary FB1 at concentrations up to 10000 ppb was also observed in carp. The latter showed a decrease in body weight and an alteration of hematological parameters in target organs.20 Baltic salmon (Salmon salar) appear to be more resistant to fumonisins. In fact, animals that were exposed to concentrations of FB1 up to 20000 ppb appeared unaffected, although a reduction of appetite was observed during the experimental period Gonçalves et al., 2016).21,22 Studies on shrimps are scarce, however it was shown that some species, such as the pacific white shrimp (Litopenaeus vannamei), are sensitive to concentrations of FB1 up to 200 ppb. Effects include reduction in soluble muscle protein concentration and changes in the myosin thermodynamic proprieties (muscular texture, a parameter that can greatly influence production).22,23 From these studies, it can be concluded that several aquatic species could be affected by fumonisins given the low average FB1 concentrations used in the experiments.

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Deoxynivalenol

Some aquatic species are sensitive to deoxynivalenol (DON). For instance, rainbow trout (Oncorhynchus mykiss) are reported to be sensitive to low levels of this mycotoxin (300-2600 ppb) and show significant decreases in growth, feed intake, feed efficiency, protein and energy utilization.9 Atlantic salmon reacts to DON in a similar way.10 Levels of DON between 300 and 1000 ppb negatively affect growth rate and body weight of pacific white shrimp.11 DON exhibits immunosuppressive effects at low doses in carp.12

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Ochratoxins

The effects of this mycotoxin were studied only in few species including zebrafish (Danio rerio) and rainbow trout. This mycotoxin caused several mutagenic and toxic effects. In zebrafish (Danio rerio), authors reported the occurrence of developmental abnormalities.24 In trout, degeneration of several organs including the liver and kidneys, followed by increased mortality were observed in some experiments.22 Ochratoxin (OTA) is toxic to channel catfish and causes effects such as a reduction in weight gain, poor FCR and histopathological lesions.25 Decreased growth performance and poor FCR were also observed in carp fed OTA at concentrations of 15 ppb.26

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Zearalenone

The effects of Zearalenone (ZEN) have not been fully evaluated. The few studies available showed the ability of this mycotoxin to affect reproductive parameters in some aquatic species. In zebrafish (Danio rerio), the presence of ZEN was reported to reduce spawn frequency.13 In another study from the same authors, larvae of zebrafish (Danio rerio) exposed to 500 ppb ZEN showed abnormalities in eye development and curvature of body axis.14 Black tiger shrimp fed ZEN at concentrations ranging from 500-1000 ppb showed histological changes in the liver.15 ZEN had negative effects on the hematological parameters (white cell count) in carp (Cyprinius carpio) and carry-over of both ZEN and the secondary metabolite α-zearalenol was observed in muscles.16 Rainbow trout (Oncorhynchus mykiss) exposed to concentrations of ZEN up to 10000 ppb showed defects  to blood coagulation and iron storage processes.17

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Aquaculture

Synergistic Effects in Aqua

There are a limited number of studies where the issue of synergistic interactions between mycotoxins is addressed. FB1 was observed to produce synergistic effects with Afla in trout, as it was able to promote the onset of afla-initiated liver tumor. The authors suggested a correlation between the disruption of the sphingolipid mechanism exerted by FB1 and the alteration of the sphingolipid signaling pathway.22 The combined effects of Afla B1 and T-2 toxin were studied in Gambusia affinis and additive effects were proven. Effects of Afla B1 and DON were studied on carp (Cyprinius carpio) and it was concluded that the toxic effects of the two mycotoxins together were greater than their effects individually.

Effects of Mycotoxins in Fish

AFB1 – Aflatoxin B1 | AFM1 – Aflatoxin M1 | DON – Deoxynivalenol | FUM – Fumonisins | OTA – Ochratoxin A | T-2 – T-2 Toxin | HT-2 – HT-2 Toxin | ZEN - Zearalenone | Ergots – Ergot, Alkaloids

Effects of Mycotoxins in Shrimp

AFB1 – Aflatoxin B1 | AFM1 – Aflatoxin M1 | DON – Deoxynivalenol | FUM – Fumonisins | OTA – Ochratoxin A | T-2 – T-2 Toxin | HT-2 – HT-2 Toxin | ZEN - Zearalenone | Ergots – Ergot, Alkaloids

References
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  2. Sepahdari A, Ebrahimzadeh Mosavi HA, Sharifpour I, Khosravi A, Motallebi AA, Mohseni M et al. (2010) Effects of different dietary levels of AFB1 on survival rate and growth factors of Beluga (Huso huso). Iranian Journal of Fisheries Sciences 9: 141–150.
  3. Rajeev Raghavan P, Zhu X, Lei W, Han D, Yang Y, Xie S (2011) Low levels of Aflatoxin B1 could cause mortalities in juvenile hybrid sturgeon, Acipenser ruthenus ♂ A. baeri♀. Aquaculture Nutrition 17: e39–e47.
  4. El-Banna R, Teleb HM, Hadi MM, Fakhry FM (1992) Performance and tissue residue of tilapias fed dietary aflatoxin. Veterinary Medical Journal 40: 17–23.
  5. Chávez-Sanchez MC, Martınez Palacios CA, Osorio MI (1994) Pathological effects of feeding young Oreochromis niloticus diets supplemented with different levels of aflatoxin B1. Aquaculture 127: 49–60.
  6. Tuan NA, Manning BB, Lovell RT, Rottinghaus GE (2003) Responses of Nile tilapia (Oreochromis niloticus) fed diets containing different concentrations of moniliformin or fumonisin B1. Aquaculture 217: 515–528.
  7. Oliveira STLD, Veneroni-Gouveia G, Santurio JM, Costa MMD (2013) Aeromonas hydrophila in tilapia (Oreochromis niloticus) after the intake of aflatoxins. Arquivos do Instituto Biologico 80: 400–406.
  8. Bintvihok A, Ponpornpisit A, Tangtrongpiros J, Panichkriangkrai W, Rattanapanee R, Doi K et al. (2003) Aflatoxin contamination in shrimp feed and effects of aflatoxin addition to feed on shrimp production. Journal of Food Protection 66: 882–885.
  9. Hooft JM, Elmor A, Ibraheem EH, Encarnaçao P, Bureau DP (2011) Rainbow trout (Oncorhynchus mykiss) is extremely sensitive to the feed-borne Fusarium mycotoxin deoxynivalenol (DON). Aquaculture 311: 224–232.
  10. Döll S, Baardsen G, Koppe W, Stubhaug I, Dänicke S (2010) Effects of increasing concentrations of the mycotoxins deoxynivalenol, zearalenone or ochratoxin A in diets for Atlantic salmon (Salmo salar) on growth performance and health. In The 14th International Symposium on Fish Nutrition and Feeding (Qingdao, China,), pp. 120.
  11. Trigo-Stockli DM, Obaldo LG, Dominy WG, Behnke KC (2000) Utilization of deoxynivalenol-contaminated hard red winter wheat for shrimp feeds. Journal of the World Aquaculture Society 31: 247–254.
  12. Pietsch C, Michel C, Kersten S, Valenta H, Dänicke S, Schulz C et al. (2014) In vivo effects of deoxynivalenol (DON) on innate immune responses of carp (Cyprinus carpio L.). Food and Chemical Toxicology 68: 44–52.
  13. Schwartz P, Thorpe KL, Bucheli TD, Wettstein FE, Burkhardt-Holm P (2010) Short-term exposure to the environmentally relevant estrogenic mycotoxin zearalenone impairs reproduction in fish. Science of The Total Environment 409: 326–333.
  14. Schwartz P, Bucheli TD, Wettstein FE, Burkhardt-Holm P (2013) Life-cycle exposure to the estrogenic mycotoxin zearalenone affects zebrafish (Danio rerio) development and reproduction. Environmental Toxicology 28: 276–289.
  15. Supamattaya K, Bundit O, Boonyarapatlin M, Schatzmayr G, Chittiwan V (2005) Effects of mycotoxin T-2 and zearalenone on histopathological changes in black tiger shrimp (Penaeus monodon Fabricius). Songklanakarin Journal of Science and Technology 27: 91–99.
  16. Pietsch C, Kersten S, Valenta H, Dänicke S, Schulz C, Burkhardt-Holm P et al. (2015) Effects of dietary exposure to zearalenone (ZEN) on carp (Cyprinus carpio L.). Toxins 7: 3465.
  17. Wózny M, Brzuzan P, Gusiatin M, Jakimiuk E, Dobosz S, Kuzminski H (2012) Influence of zearalenone on selected biochemical parameters in juvenile rainbow trout (Oncorhynchus mykiss). Polish Journal of Veterinary Sciences 15: 221–225.
  18. Lumlertdacha S, Lovell RT (1995) Fumonisin-contaminated dietary corn reduced survival and antibody production by channel catfish challenged with Edwardsiella ictaluri. Journal of Aquatic Animal Health 7: 1–8.
  19. Riley RT, Enongene E, Voss KA, Norred WP, Meredith FI, Sharma RP et al. (2001) Sphingolipid perturbation as mechanisms for fumonisin carcinogenesis. Environmental Health Perspectives 109:301-308.
  20. Petrinec Z, Pepeljnjak S, Kovacic S, Krznaric A (2004) Fumonisin B1 causes multiple lesions in common carp (Cyprinus carpio). DTW. Deutsche Tierarztliche Wochenschrift, 111: 358–363.
  21. Garcıa EC, (2013) Effects of Fumonisin B1 on Performance of Juvenile Baltic Salmon (Salmo salar). Faculty of Science, University of Jyväskylä, Finland.
  22. Gonçalves RA, Naehrer K and Santos GA (2016)Occurrence of mycotoxins in commercial aquafeeds in Asia and Europe: a real risk to aquaculture? Reviews in Aquaculture (2016) 0, 1–18.
  23. García-Morales M-H, Pérez-Velázquez M, González-Felix ML, Burgos-Hernández A, Cortez-Rocha M-O, Bringas-Alvarado L et al. (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: 340–353.
  24. Debeaupuis JP, Marche C, Lafont P (1984) Embryotoxicity and teratogenicity of ochratoxin A in the zebra-fish (Brachydanio rerio). Microbiologie, Aliments, Nutrition 2: 257–269.
  25. Manning BB, Ulloa RM, Li MH, Robinson EH, Rottinghaus GE (2003) Ochratoxin A fed to channel catfish (Ictalurus punctatus) causes reduced growth and lesions of hepatopancreatic tissue. Aquaculture 219: 739–750.
  26. Agouz HM, Anwer W (2011) Effect of Biogen® and Myco-Ad® on the growth performance of common Carp (Cyprinus carpid) fed a mycotoxin contaminated aquafeed. Journal of Fisheries and Aquatic Science 6: 334–345.