mycotoxins in aquaculture feeds: facts and implications

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Digital Re-print - January | February 2007Feature: Feed additives

Feature title: Mycotoxins in Aquaculture feeds: facts & implications

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26 | I nternatIonalAquAFeed | Juy-Fbuy 07 -

Mycotoxins are

s e c o n d a r y

metabolites produced

by fungi, commonly

referred as molds. They are

produced by these organisms when

they grow on agricultural products

before or after harvest or during

transportation or storage.

Most of the mycotoxins that have the

potential to reduce growth and health sta-

tus of fish and other farmed animals con-

suming contaminated feed are produced

by Aspergillus, Penicillium and Fusariumsp. These toxic substances are known to

be either carcinogenic (e.g. aflatoxin B1,

ochratoxin A, fumonisin B1), estrogenic

(zearalenone), neurotoxic (fumonisin B1),

nephrotoxic (ochratoxin), dermatotoxic (tri-

chothecenes) or immunosuppressive (afla-

toxin B1, ochratoxin A and T-2 toxin).

Mould toxins vary in their toxicity toward

different animals species and while the effect

of mycotoxins is relatively well known in

most terrestrial farm animals the effect

of mycotoxins on aquaculture species has

not been studied extensively. Nevertheless,

several studies have reported pathological

signs of mycotoxin poisoning in fish and

shrimp species which can cause economic

losses to the industry. These economic

losses can be caused either by unfavorableeffects on the animal themselves caused

by exposure to high contamination levels,

or by an increase potential for detrimental

health effects in animals consuming low or

moderate contaminated products.

Given the trend and the economical need

to replace expensive animal-derived proteins,

such as fish meal, with less expensive plant

proteins sources, the relevance of mycotoxin

contamination in aquaculture feeds have a

tendency to increase since feed ingredients

of plant origin, have higher susceptibility

for mycotoxin contamination. Mycotoxin

contamination is often an additive process,

beginning in the field and increasing during

harvest, drying, and storage. In tropical and

subtropical conditions the potential for

mycotoxin contamination is further increaseddue to storage under humid and hot conditions,

favorable for fungi contamination of stored feed

and grain (CAST, 2003).

tabe 1: occurrence, average and highes eves f mycxins deeced based n cmmdiy ype and cunry f rigin

Mycxin Sampe Size Percen Psiive Average f Highes leve Cmmdiy fund Cunry f originPsiive (g/kg) Deeced (g/kg)

Aflatoxin sTotal 965 18% 39 381 Peanut Meal AustraliaZearalenone 963 35% 409 6,468 Corn ChinaDeoxynival enol 963 45% 866 18,991 Wheat ChinaFumonisin B1 960 46% 664 10,577 Corn ChinaT-2 toxin 748 1% 273 494 Finished Feed ThailandOchratoxin A 128 18% 11.7 143 Corn Malaysia

Mycotoxins in Aquaculture feeds:

facts and implications

by Pedro Encarnao PhD

Biomin Laboratory Singapore Pte. Ltd3791 Jalan Bukit Merah #08-08

E-Center@RedhillSingapore 159471

Email: [email protected]

Feed additives

Effect of different levels of aflatoxin B1 on tilapia growth performance(Source, Dr Jowaman Khajarern)

- Juy-Fbuy 07 | InternatIonalAquAFeed | 27

A recent survey (Chin & Tan, 2006)

conducted in all Asian region analyzed 970

samples of different feed ingredients and

feed samples to determine contamination

levels of the major mycotoxins of interest;

namely, aflatoxins, zearalenone (ZON),

deoxynivalenol (DON), fumonisin (Fum), T2

toxin and ochratoxin A (OTA). In brief, from

the survey results, aflatoxins and ochratoxin

A, accounted for 18 percent of the sample

contamination; 35 percent were positive for

zearalenone, 45 percent for deoxynivalenol

and 46 percent for fumonisin B1 (Table 1).

Though it is impossible to correlate

the occurrence of a specific mycotoxin

to a specific commodity from the data

studied, there is apparent prevalence of

some mycotoxins to some specific sample

types. For instance, 100 percent of the

peanut meal samples analyzed were found

to be contaminated with aflatoxins with the

highest level of 381 g/kg and an average of

202 g/kg (Table 2). For wheat samples, 88

percent were affected by DON with the

highest level found at 18,991 g/kg and an

average contamination level of 1,181 g/kg,

while no aflatoxins were detected in any of

the wheat samples. It was seen that more

than 80 percent of the corn gluten meal

samples were ZON (87 percent) and Fum

(83 percent) positive (Chin & Tan, 2006).

A contaminated ingredient or feed is likely

to contain more than one type of mycotoxin.

Numerous researchers have reported that

mycotoxins act synergistically so that the

negative effects of two mycotoxins are

worse than the effects of each individually

(Manning, 2001). Mycotoxins also appear

to be very heat stable and the pelleting and

extrusion process of fish and shrimp feeds

do not seem to reduce appreciable amounts

of mycotoxins (Manning, 2001).

The contamination of feeds and raw

materials by mycotoxins is a reality and

its increasing on a global basis making it

increasingly likely that any given feedstuff

could contain one or, more likely, several

mycotoxins. They are invisible, odorless and

tasteless toxins with a major impact on

animal health. The awareness on the effect

of mycotoxins in terrestrial livestock is

increasing but still overviewed in aquaculture

species.

Aflatoxins

Aflatoxins are produced by Aspergillus

fungi, which can infect many potential

feedstuffs as corn, peanuts, rice, fish meal,

shrimp and meat meals (Ellis et al., 2000).

Aflatoxin B1 (AFB1) is one of the most

potent, naturally occurring, cancer-causing

agents in animals. Initial findings associated

with aflatoxicosis in fish include pale gills,

impaired blood clotting, anemia, poor growth

rates or lack of weight gain. Prolonged

feeding of low concentrations of AFB1

causes liver tumors, which appear as pale

yellow lesions and which can spread to the

kidney (Manning 2001). These subtle effects

often go unnoticed and profits are lost due

to decreased efficiency in production, such

as slow growth, reduced weights of the

finished product, an increase in the amount

of feed needed to reach market weight, and

increased medical costs.

The extent of disease, caused by

consumption of aflatoxins, depends upon

the age and species of the fish. Fry are more

susceptible to aflatoxicosis than adults and

some species of fish are more sensitive to

aflatoxins than others (Tuan et al., 2002).

Rainbow trout is reported to be one of the

most sensitive animals to aflatoxin poisoning.

In this species, an intake of 1 g AFB1/kg

diet can cause liver tumors and the LD50

(dose causing death in 50 percent of the

subjects) for AFB1 in a 50g trout being 500

1000 ppb (0.51.0 mg/kg) (Lovell, 1989). The

carcinogenic or toxic effects of aflatoxins

in fish seem to be species specific. While

Rainbow trout are extremely sensitive to

AFB1, warm water fish such as channel

catfish (Ictalurus punctatus) are reported

to be less sensitive to aflatoxins (Manning,

2001).

Although less sensitive, warm water

species are still affected by aflatoxin

contamination. Feeding a diet containing

10 ppm AFB1/kg diet to channel catfish

caused reduced growth rate and moderate

internal lesions over a 10-week trial period

(Jantrarotai & Lovell, 1990a). In carp, it

was reported that aflatoxins are potential

immunosuppressors (Sahoo et al. 2001). A

recent study (Manning et al., 2005a) indicated

that feeding diets containing aflatoxins from

moldy corn does not seem to affect channel

catfish weight gain, feed consumption, feed

efficiency, and survival. Studies on the Nile

tilapia (Oreochromis niloticus) showed

reduced growth rates when tilapias were fed

diets containing 1880 ppb AFB1 (Chavez-

Sanches et al., 1994). In addition, tissue

abnormality or lesions in the livers of these

tilapias showed the beginnings of cancer

development. In another study, Nile tilapia

fed diets with 100

ppb AFB1 for 10

weeks had reducedgrowth, and fish

fed diet with 200

ppb AFB1 had 17

percent mortality

(El-Banna et al.,

1992). In a more

recent study, Tuan

et al. (2002) showed

that acute and sub-

chronic effects of AFB1 to Nile tilapia are

unlikely if dietary concentrations are 250

ppb or less. However, diets containing levels

of AFB1 higher than 250 ppb had lower

weight gain and haematocrit count compared

to a control diet. Diets containing 100 ppm

AFB1 caused weight loss and severe hepatic

necrosis in Nile tilapia (Tuan, et al., 2002).

In marine s hrimp, several studies showed

that AFB1 can cause abnormalities such

as poor growth, low apparent digestibility,

physiological disorders and histological

changes, principally in the hepatopancreatic

tissue (Wiseman et al., 1982; Ostrowski-

Meissner, et al., 1995 Bintvihok at al.,

2003; Boonyaratpalin et al., 2001; Burgos-

Hernadez et al., 2005, Supamattaya et al.,

2006). Nevertheless, reports on the effect of

AFB1 on shrimp are inconsistent. Bintvihok

et al. (2003) reported that after just 7

or 10 days of consumption of diets with

AFB1 levels below 20 ppb, mortality rate

table 2: Prevalence of mycooxins in differen commodiies

Prevalence 1s 2nd 3rd 4h 5h 6h

Corn FUM (68%) DON (67%) ZON (40%) OTA (20%) AFLA (19%) NASoybean/Meal ZON (14%) DON(7%) FUM(7%) OTA(5%) AFLA(3%) NAWheat/bran DON (85%) ZON (24%) FUM (5%) T2(


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28 | I nternatIonalAquAFeed | Juy-Fbuy 07

was slightly higher in AFB1-treated groups

than in the control group. Histopathological

findings indicated hepatopancreatic damage

by AFB1 with biochemical changes of the

haemolymph.

In another study, AFB1 at 50100 ppb

showed no effect on growth in juvenile

shrimps (Boonyaratpalin et al., 2001).

However, growth was reduced when AFB1

concentrations were elevated to 5002500ppb. Survival dropped to 26.32 percent

when 2500 ppb AFB1 was given, whereas

concentrations of 501000 ppb had no

effect on survival (Boonyaratpalin et al.,

2001). There were marked histological

changes in the hepatopancreas of shrimp

fed diet containing AFB1 at a concentration

of 1002500 ppb for 8 weeks, as noted by

atrophic changes, followed by necrosis of the

tubular epithelial cells. Severe degeneration

of hepatopancreatic tubules was common

in shrimp fed high concentrations of AFB1

(Boonyaratpalin et al., 2001). Abnormal

hepatopancreas and antennal gland tissues

were also reported by Ostrowski-Meissner, et

al., 1995 in shrimp fed 50 ppb AF B1/kg after

only 2 weeks. Feed conversion efficiency andgrowth were significantly affected at AFB1

400 ppb. Apparent digestibility coefficients

decreased significantly at AF B1 900 ppb

(Ostrowski-Meissner, et al., 1995).

According to Burgos-Hernadez et al.

(2005), the effect of AFB1 toxicity to shrimp

results in the modification of digestive

processes and abnormal development of

the hepatopancreas due to exposure to

mycotoxins. These effects might be due

to alterations of trypsin and collagenase

activities, among other factors, such as the

possible adverse effect of these mycotoxins

on other digestive enzymes (e.g. lipases

and amylases) (Burgos-Hernadez et al.,

2005). These results show that aflatoxin

contamination in shrimp feed may cause

economic losses by lowering the production

of shrimp.

OchratoxinsOchratoxins are a group of secondary

metabolites produced by fungal organisms

belonging to Aspergillus and Penicillium

genera. Ochratoxin A (OA) is the most

abundant of this group and is more toxic

than other ochratoxins. It contaminates

corn, cereal grains and oilseeds. Ochratoxin

A can adversely affect animal performance.

It primarily attacks the kidneys of affected

animals (CAST, 2003).

Very few studies have been conducted

to determine the effect of ochratoxins in

fish species. In juvenile channel catfish, diets

containing levels of 1 to 8 ppm of OA resulted

in the development of toxic responses.

Significant reduction in body weight gain

were observed after only 2 weeks in fish

fed diets containing 2 ppm of ochratoxin

A or above (Manning et al., 2003a). After

8 weeks body weight gain was significantly

reduced for fish fed diets containing 1 ppmOA or above. Additional toxic responses

included poorer FCR for fish fed diets with

4 or 8 ppm OA, and lower survival and

hematocrit count for fish fed the 8 ppm

OA diet. Severe histopathological lesions of

liver and posterior kidney were observed

after 8 weeks for catfish fed diets containing

levels of OA of 4 and 8 ppm (Manning, et

al., 2003a). In growing rainbow trout the

oral LD50 of ochratoxin

A has been determined to

be 4.67 ppm. Pathological

signs of ochratoxicosis in

trout include liver necrosis,

pale, swollen kidneys and

high mortality (Hendricks,

1994).

Cyclopiazonic acid(CPA)

Cyclopiazonic acid (CPA)

is a mould toxin produced

by several species of

Aspergillus and Penicillium

fungi. Jantrarotai and Lovell

(1990b) found that CPA, a neurotoxin

frequently found in association with aflatoxins,

was more toxic to channel catfish than

aflatoxins and is more frequently found

than aflatoxins in feedstuffs in the southern

United States. A dietary level of 100 ppb

CPA significantly reduced growth, and 10,000

ppb caused necrosis of gastric glands. The

minimum dietary concentration that caused

a reduction in growth rate was 100 ppb for

CPA as compared with 10,000 ppb for AFB1

(Jantrarotai and Lovell, 1990b).

FumonisinsThe fumonisins represent a group of

mycotoxins produced predominantly by

Fusarium moniliforme species. Fumonisin

B1 has been found to be the major toxic

component both in corn culture and in

naturally contaminated corn. Some early

investigations associated this toxin with

a variety of animal diseases. Fumonisins

specifically disrupt sphingolipid metabolism

(Wang et al., 1992). Administration of feed

contaminated with F. moniliforme culture

material was related to certain changes in

some hematological parameters and serum

or plasma chemical concentration and

activities in many animal models (Pepeljnjak

et al., 2002).

The importance of fumonisins as

toxic agents in fish remains still poorly

understood. In one study, channel catfish fed

F. moniliforme culture material containing313 ppm of fumonisin B1 (FB1) for 5 weeks

revealed minimal adverse effects (Brown et

al., 1994). Conversely, Lumlertdacha et al.

(1995) reported that dietary levels of FB1

of 20 ppm or above are toxic to year-1

and year-2 channel catfish. After 10 and

14 weeks, respectively, year-1 and year-

2 catfish fed 20 ppm or more of FB1 in

the diet had lower weight gain compared

to the control, and those fish fed diets

with levels of 80 ppm and above showed

significantly lower hematocrits and red

and white blood cells than those fed

lower doses (Lumlertdacha et al., 1995).

Similarly, Yildirim et al. (2000) found that in

channel catfish, diets containing 20 ppm of

moniliformin (MON) or FB1 significantly

reduced body weight gain after 2 weeks.

According to Yildirim et al. (2000), FB1 is

more toxic than MON to channel catfish.

Adverse effects of fumonisin contaminated

diets have also been reported in tilapia.

Results presented by Tuan et al. (2003)

demonstrated that feeding MON and FB1

at 70 and 40 ppm, respectively, adversely

affected growth performance of Nile

tilapia fingerlings. FB1 is slightly more toxic

than MON to tilapia fingerlings as toxic

symptoms appear earlier in fish exposed

to FB1. Nevertheless, neither MON nor

FB1 caused mortality or histopathological

lesions in Nile tilapia fingerlings. Compared

Feed additives

Hemorrhagic liver affected byaflatoxin B1 contamination

(Source, Dr Jowaman Khajarern)

-

to channel catfish, Nile tilapia appears to be

more resistant to these two mycotoxins in

the diet (Tuan et al., 2003).

Although research studies revealed that

FB1 is toxic to tilapia and channel catfish

by suppressing growth and/or causing

histopathological lesions, this fish survived

mycotoxins levels up to 150 ppm. Reduction

on the percentage of survival of channel

catfish was observed for diets containing240 ppm FB1 (Li et al., 1994). Studies on the

effect of FB1 in carp indicated that long-term

exposure to 0.5 and 5.0 mg per kg body

weight is not lethal to young carp, but can

produce adverse physiological effects. The

primary target organs of FB1 in the carp

are kidney and liver (Pepeljnjak et al., 2002).

Other changes subsequent to fumonisin

exposure that have been reported for carp

include scattered lesions in the exocrine and

endocrine pancreas, and inter-renal tissue,

probably due to ischemia and/or increased

endothelial permeability (Petrinec et al.,

2004).

TrichothecenesTrichothecenes are a group of mycotoxins

produced by certain fungi of the genus

Fusarium that infect the grains, wheat by-

products and oilseed meals used in the

production of animal feeds. The type A-

trichothecene T2-toxin produced by the

fungus Fusarium tricintum proved lethal to

rainbow trout at a dietary concentration

near 6 mg/kg body weight (Marasas et al.,

1967). Poston et al. (1983), however, fed

rainbow trout T2-toxin at 15 ppm of diet and

found that the main effects were reduced

feed consumption, reduced growth, lower

hematocrit, and lower blood hemoglobin.

Results from Manning et al. (2003b)

demonstrated that T2-toxin is toxic to

juvenile channel catfish. Reductions in growth

rate were observed after 8 weeks for fish fed

diets containing levels of T2-toxin ranging

from 0.625-5.0 ppm, compared to a control

diet. Significantly poorer feed conversion

ratio was found only for the highest level

of T2-toxin (5 ppm). The survival of fish fed

T2-toxin at 2.5 and 5 ppm was significantly

lower than that of the control fish (Manning

et al., 2003b).

A recent study with channel catfishindicate that disease resistance of juvenile

channel catfish was reduced when fed

feedborne T-2 t oxin, resulting in significantly

greater mortality when challenged with

Edwardsiella ictaluri compared to a control

group (Manning et al., 2005b). In carp, the

injection of T-2 toxin did not significantly

change the activity of enzymes in carp liver,

although a tendency for reduction was noted

(Kravchenko et al., 1989).

In shrimp, Supamattaya et al. (2006)

reported that in white shrimp growth was

significantly reduced by T-2 toxin at 0.1 ppm

while for black tiger shrimp reduced growth

was observed at levels of 2.0 ppm. The

presence of T-2 toxin at 1.0-2.0 ppm produced

atrophic changes and s evere degeneration of

hepatopancreas tissue, inflamation and loose

contact of hemopoietic tissue and lymphoid

organ on black tiger and white shrimp after

feeding for 10 weeks and 8 week respectively.

The same pathology was

found in shrimp received

1.0 ppm zearalenone

(Supamattaya et al., 2006).

It was concluded by the

authors that white tiger

shrimp are more sensitive

to mycotoxins then black

tiger shrimp.

Deoxynivalenol (DON),

also known as vomitoxin, and

other type B trichothecenes

are produced by Fusarium

sp. and can be an importantcontaminant of wheat.

Deoxynivalenol levels of

0.2, 0.5, and 1.0 ppm in t he diet significantly

reduced body weight and growth rate in

white shrimp Litopenaeus vannamei (Trigo-

Stockli et al., 2000). However, the effects of

0.2 and 0.5 ppm DON were manifested at

later stages of growth, and 0.2 ppm DON

affected only growth rate and not body

weight. Feed conversion ratio and survival of

shrimp fed diets containing 0.2, 0.5, and 1.0

ppm DON were not significantly different

from those of shrimp fed the control diet

(0.0 ppm DON) (Trigo-Stockli et al., 2000).

Reduced weight gain has also been noted

in rainbow trout fed DON-contaminated

feeds and feed refusal has been found to

occur in fish fed with diets containing more

than 20 ppm DON. For rainbow trout,

a dietary level of 112.9 ppm resulted

in reduced growth and feed efficiency

(Hendricks, 1994). Woodward et al. (1983)

showed that rainbow trout had sensitive

taste acuity for DON and reduced theirfeed intake as the concentration of DON

increased from 1 to 13 ppm of diet; the fish

refused to consume the diet with a DON

concentration of 20 ppm.

Combating mycotoxinsAlthough mycotoxin contamination of

feed and feed ingredients represent an

increase threat to aquaculture operations

there are a number of options available to

feed manufacturers and farmers to prevent or

reduce the risk of mycotoxicosis associated

with mycotoxin contamination. These range

from careful selection of raw materials,

maintaining good storage conditions for

feeds and raw materials, and using a good

mycotoxin deactivator to combat the widest

possible range of different mycotoxins thatmay be present.

Binders or adsorbents have been used

to neutralize the effects of mycotoxins

by preventing their absorption from the

animals digestive tract. The most common

binders are clays, bentonites, zeolites silicas

and alumino silicates. Unfortunately, different

mycotoxin groups are completely different

in their chemical structure and therefore

it is impossible to equally deactivate all

mycotoxins by using only one single strategy.

Adsorption works perfectly for aflatoxin

but less- or non-adsorbable mycotoxins

(like ochratoxins, zearalenone and the

whole group of trichothecenes) have to be

deactivated by using a different approach.

MycofixPlus is a mycotoxin deactivatorwhich combines adsorption and bio-

inactivation to break functional groups

of mycotoxins such as trichothecenes,

ochratoxin A and zearalenone, and also

immunostimulation with addition of

selected plant extracts. Biotransformation

is defined as detoxification of mycotoxins

using microorganisms or enzymes which

specifically degrade the toxic structures

to non-toxic metabolites. MycofixPlus

combines different microorganisms, live

bacteria and yeast strains, expressing

specific mycotoxin-degrading enzymes to

successfully counteract all agriculturally

Feed additives

Mold contaminated corn

Juy-Fbuy 07 | InternatIonalAquAFeed | 29NEXT PAGEPREVIOUS PAGE


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relevant mycotoxins in a biological way.

BBSH 797, a Eubacterium species, patented

by Biomin, produces enzymes, so-called de-

epoxidases, which degrade the toxic epoxide

ring of trichothecenes, T. mycotoxinivorans

(vorans lat. degrade, eat), a yeast strain,

successfully counteracts ochratoxin A and

zearalenone by enzymatic cleavage.

Furthermore, all mycotoxins are known

to influence detrimentally toward the liverand cause immunosuppression in animals.

The addition of plant and algae extracts to

the animals diet helps to overcome these

negative influences. Special algae extracts,

tested on their immune enhancing effect,

support the immune system and thus

overcome the immunesuppressive effect of

all mycotoxins. The liver, the main target

organ of mycotoxins, is protected by selected

antiphlogistic plant extracts.

References

Abdelhamid, A.M., Khalil, F.F., Ragab, M.A., (1998).

Problem of mycotoxins in fish production. Egyptian

Journal of Nutrition and Feeds. 1 (1), 63-71.

Bintvihok, A., Ponpornpisit, A., Tangtrongpiros, J.,

Panichkriangkrai, W., Rattanapanee, R., Doi, K.,Kumagai, S., (2003). Aflotoxin contamination in

Shrimp feed and effects of aflotoxin addition to feed

on shrimp production. J. Food Prot. 66, 882-885.

Boonyaratpalin, M., Supamattaya, K., Verakunpiriya,

V., Suprasert, D., (2001). Effects of aflotoxin B1 on

growth performance, blood components, immune

function and histopatological changes in black tiger

shrimp (Paneus monodon Fabricius). Aquac. Res.

32 (suppl. 1), 388-398.

Brown, D.W., McCoy, C.P., Rottinghaus, G.E., (1994).

Experimental feeding of Fusarium moniliforme

culture material containing fumonisin B1 to channel

catfish, (Ictalurus punctatus). Journal of Veterinary

Diagnostic Investiation. 6(1), 123-124.

Burgos-Hernandez, A., Farias, S.I., Torres-Arreola,

W., Ezquerra-Brauer, J.M., (2005). In Vitro studies

of the effects of aflotoxin B1 and fumonisin B1

on trypsin-like and collagenase-like activity from

the hepatopancreas of white shrimp (Litopanaeus

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Chavez-Sanches, Ma.C, Martinez, C.A., Moreno,

I.O., (1994). Pathological effects of feeding youg

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different levels of aflotoxin B1. Aquaculture 127:49-60.

El-Banna, R., Teleb, H.M., Fakhry, F.M., (1992).

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Janrarotai, W. and Lovell, R.T., (1990a). Subchronic

toxicity of dietary aflatoxin B1 to Channel catfish.

Journal of Aquatic Animal Health. 2(4), 248-254.

Janrarotai, W. and Lovell, R.T., (1990b). Acute and

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catfish. Journal of Aquatic Animal Health. 2(4), 255-260.

Lee, B.C., Hendrix, J.D., Bailey, G.S., (19 91). Toxicity

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Li, M.H., Raverty, S.A., Robinson, E.H., (1994). Effects

of dietary mycotoxins produced by the mold

Fusarium moniliforme on channel catfish (Ictalurus

punctatus) J. World Aquacult. Soc. 25(4), 512-516.

Lumlertdacha, S. and Lovell, R.T., (1995). Fumonisin-

contaminated dietary corn reduced survival and

antibody production by channel catfish challenged with

Edwardsiella ictaluri. J. Aquat. Anim. Health. 7(1), 1-8.

Lumlertdacha, S., Lovell, R.T Shelby, R.A., Lenz, S.D.,

Kemppainen, B.W., (1995). Growth, hematology,

and histopathology of channel catfish (Ictalurus

punctatus), fed toxins from Fusarium moniliforme.

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Manning, B.B., (2001). Mycotoxins in fish feeds. In

Nutrition and Fish Health. Lim, C. & Webster, C.D.

Eds). Food Prod ucts Press. New York. 365 p.

Manning, B.B., Ulloa, R.M., Li, M.H., Robinson, E.H.,

Rottinghaus, G.E., (2003a). Ochratoxin A fed

to channel catfish (Ictalurus punctatus) causes

reduced growth and lesions of hepatopancreatic

tissue. Aquaculture. 219, 739-750.

Manning, B.B., Li, M.H., Robinson, E.H., Gaunt, P.S.,

Camus, A.C., Rottinghaus, G.E., (2003). Response

of catfish to diets containing T-2 toxin. Journal of

Aquatic Animal Health. 15(3), 229-238.

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Grass Carpproductionin cages

Mycotoxins inAquaculture feeds:factsand implications

Organicaquaculture:closer to being areality?

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