Fusarium mycotoxicoses in broilers

The oral LD₅₀ of DON for broilers has been estimated as 140 mg/kg body weight with no mortality until oral doses reached 70 mg/kg, indicating a relatively low acute toxicity (Huff et al., Reference HUFF, DOERR, HAMILTON and VESONDER1981). Broilers fed naturally contaminated wheat-based diets containing up to 11 mg/kg DON had no significant changes in feed conversion or body weight gain (Awad et al., Reference AWAD, BÖHM, RAZZAZI-FAZELI and ZENTEK2006; Hamilton et al., Reference HAMILTON, TRENHOLM, THOMPSON and GREENHALGH1985b; Hulan and Proudfoot, Reference HULAN and PROUDFOOT1982; Swamy et al., Reference SWAMY, SMITH, COTTER, BOERMANS and SEFTON A.E.2002). Broilers fed diets containing corn inoculated with Fusarium graminearum did not have reduced feed consumption or growth until dietary DON concentrations exceeded 116 mg/kg (Moran et al., 1982). Huff et al. (Reference HUFF, KUBENA, HARVEY, HAGLER, SWANSON, PHILLIPS and CREGER1986), on the other hand, demonstrated reduced growth rate of broilers fed a naturally contaminated wheat-based diet containing 16 mg/kg DON. It was found that all of the effects of DON noted in broilers were comparable to the effects reported in growing Leghorn chicks by Kubena et al. (Reference KUBENA, SWANSON, HARVEY, FLETCHER, ROWE and PHILLIPS1985), with the exception of reduced growth rates. The difference in growth rate of broilers compared to layers may explain why this parameter was more sensitive to change in broilers than layers (Kubena et al., Reference KUBENA, SWANSON, HARVEY, FLETCHER, ROWE and PHILLIPS1985). Dänicke et al. (Reference DÄNICKE, MATTHES, HALLE, UEBERSCHÄR, DÖLL and VALENTA2003) and Swamy et al. (Reference SWAMY, SMITH, KARROW and BOERMANS2004a) observed a linear decrease in feed intake and body weight gain in the grower phase in broilers fed diets naturally contaminated with up to 14 mg/kg DON. When broilers were growing more slowly, growth depression was observed in the finisher phase (Swamy et al., Reference SWAMY, SMITH, COTTER, BOERMANS and SEFTON A.E.2002). This supports the concept that broilers do not exhibit feed refusal in a manner similar to swine when fed Fusarium mycotoxin-contaminated diets (Smith et al., Reference SMITH, MCMILLAN and CASTILLO1997). Such species differences are believed to be due to differences in the effects of Fusarium mycotoxins on brain neurochemistry. Increased concentrations of serotonergic neurotransmitters in pigs fed contaminated grains were suggested as a possible cause of feed refusal. In broilers, adrenergic neurotransmitters also increase, antagonising the effect of serotonin on appetite suppression (Swamy et al., Reference SWAMY, SMITH and MACDONALD2004b). It is likely that mycotoxin-induced growth suppression in broilers is due to gradual alterations in metabolism that occur with chronic exposure to contaminated grains.

Elevated blood uric acid concentrations have often been reported in broilers fed Fusarium mycotoxin-contaminated diets. Blood urea nitrogen concentrations increased in broilers fed diets containing 16 mg/kg DON from contaminated wheat (Kubena et al., Reference KUBENA, HUFF, HARVEY, CORRIER, PHILLIPS and CREGER1988). Serum uric acid concentrations increased in broilers fed diets containing 2.5 mg/kg NIV (Pettersson et al., Reference PETTERSSON, HEDMAN, ENGSTRÖM, ELWINGER and FOSSUM1995). Swamy et al. (Reference SWAMY, SMITH, COTTER, BOERMANS and SEFTON A.E.2002) reported increased serum uric acid concentrations in the finisher phase in broilers fed diets contaminated with multiple Fusarium mycotoxins. Increased plasma uric acid concentration was also reported in layers (Chowdhury and Smith, Reference CHOWDHURY and SMITH2004) and in turkeys (Girish et al., Reference GIRISH, SMITH, BOERMANS and KARROW2008b) fed contaminated diets containing DON, 15-acetyl-DON and ZEN. Inhibitory effects of Fusarium mycotoxins on hepatic protein synthesis may result in elevated hepatic free amino acids which in turn would be used for energy utilization thus increasing serum uric acid concentrations (Chowdhury and Smith, Reference CHOWDHURY and SMITH2005).

The effects of feeding Fusarium mycotoxin-contaminated grains on relative organ weights are inconsistent. Relative gizzard weight increased in growing chicks fed contaminated wheat containing up to 18 mg/kg DON (Kubena et al., Reference KUBENA, SWANSON, HARVEY, FLETCHER, ROWE and PHILLIPS1985; Huff et al., Reference HUFF, KUBENA, HARVEY, HAGLER, SWANSON, PHILLIPS and CREGER1986) or 12 mg/kg NIV (Pettersson et al., Reference PETTERSSON, HEDMAN, ENGSTRÖM, ELWINGER and FOSSUM1995). This was probably related to the decreased nutrient density (increased fibre) of DON-contaminated scabby wheat (Harvey et al., Reference HARVEY, KUBENA, ROTTINGHAUS, TURK, CASPER and BUCKLEY1997). Decreased absolute and relative weights of the intestine, associated with decreased duodenal villus height and width, occurred in broilers fed diets containing 5 mg/kg DON (Awad et al., Reference AWAD, BÖHM, RAZZAZI-FAZELI and ZENTEK2006). Discrepancies in relative weights of other internal organs have been observed (Kubena et al., Reference KUBENA, SWANSON, HARVEY, FLETCHER, ROWE and PHILLIPS1985, Reference KUBENA, HUFF, HARVEY, CORRIER, PHILLIPS and CREGER1988, Reference KUBENA, HUFF, HARVEY, PHILLIPS and ROTTINGHAUS1989; Huff et al., Reference HUFF, KUBENA, HARVEY, HAGLER, SWANSON, PHILLIPS and CREGER1986; Swamy et al., Reference SWAMY, SMITH, KARROW and BOERMANS2004a). Organ weights may not always be relevant indicators of toxicity. Time of toxin exposure may be a significant factor as the organ may initially increase in size and subsequently undergo a size reduction (Swamy et al., Reference SWAMY, SMITH, KARROW and BOERMANS2004a).

Reduced antibody titres to Newcastle disease virus (NDV) have been observed in grower birds fed diets naturally contaminated with DON alone or DON combined with other Fusarium mycotoxins (Harvey et al., Reference HARVEY, KUBENA, HUFF, ELISSALDE and PHILLIPS1991; Dänicke et al., Reference DÄNICKE, MATTHES, HALLE, UEBERSCHÄR, DÖLL and VALENTA2003). Broilers fed diets naturally contaminated with DON in addition ZEN and fusaric acid (FA) had decreased biliary IgA concentrations (Swamy et al., Reference SWAMY, SMITH, COTTER, BOERMANS and SEFTON A.E.2002) and decreased percentages of B lymphocytes in the blood (Swamy et al., Reference SWAMY, SMITH, KARROW and BOERMANS2004a).

Reports that poultry can tolerate relatively high concentrations of Fusarium mycotoxins has raised concern that poultry products could be an inconspicuous route of human exposure. No residues of DON or its metabolites could be detected, however, in plasma or edible tissues (muscles, liver and gizzard) of broilers fed, for 48 days, diets containing up to 18 mg/kg DON from naturally contaminated wheat or wheat purposely inoculated with F. culmorum (Dänicke et al., Reference DÄNICKE, VALENTA and MATTHES2007a; El-Banna et al., Reference EL-BANNA, HAMILTON, SCOTT and TRENHOLM1983; Kubena et al., Reference KUBENA, SWANSON, HARVEY, FLETCHER, ROWE and PHILLIPS1985). The risk of human exposure through consumption of chicken meat would appear to be negligible. The possibility of chronic exposure of layers to Fusarium mycotoxins in feed also raised concern about the transmission of these toxins or their metabolites into eggs (discussed below).

Combinations of mycotoxins likely have a greater impact on birds than the additive effect of individual mycotoxins. Quantities of 0.7 mg/kg T-2 toxin, 0.5 mg/kg DAS with traces of DON in a blend of grains accidentally fed to Brahma chickens caused depression, loss of appetite and dramatic lesions (Konjević et al., Reference KONJEVIĆ, SREBOČAN, GUDAN, LOJKIĆ, SEVERIN and SOKOLOVIĆ2004). Haemorrhages in the proventriculus and bursa of Fabricius as well as pale swollen livers were reported although mycotoxin levels were much lower than the estimated LD₅₀ of T-2 toxin. Additive interactions have been observed between DON and ochratoxin A (OA), where body weight gain and efficiency of feed utilization were reduced in broiler chicks fed diets containing 16 mg/kg of DON from naturally contaminated wheat and 2 mg/kg OA (Kubena et al., Reference KUBENA, HUFF, HARVEY, CORRIER, PHILLIPS and CREGER1988). Less-than-additive toxicity was observed in broilers fed 15 mg/kg DON from naturally contaminated wheat and 300 mg/kg FB₁ (Kubena et al., Reference KUBENA, EDRINGTON, HARVEY, BUCKLEY, PHILLIPS, ROTTINGHAUS and CASPER1997). Broilers fed 16 mg/kg DON, in a naturally contaminated wheat-based diet, combined with 4 mg/kg T-2 toxin also had reduced body weight gains and final body weights, a finding that was not observed in broilers exposed to either toxin singly (Kubena et al., Reference KUBENA, HUFF, HARVEY, PHILLIPS and ROTTINGHAUS1989). Broilers receiving diets containing corn inoculated with F. graminearum exhibited plaques in the mouth and gizzard erosion proportional to the level of DON that ranged from 1.7 to 210 mg/kg. These diets contained up to 1.75 mg/kg ZEN and less than 1 mg/kg of DAS and T-2 toxin (Moran et al., 1982). The incidence and severity of oral lesions induced by T-2 toxin increased when the diets contained a combination of both T-2 toxin (4 mg/kg) and DON (16 mg/kg) from naturally contaminated wheat (Kubena et al., Reference KUBENA, HUFF, HARVEY, PHILLIPS and ROTTINGHAUS1989). The effects observed in the combination of DON and aflatoxin were also more pronounced than the individual effects of either toxin alone. The interaction between 16 mg/kg DON in naturally contaminated wheat and 2.5 mg/kg aflatoxin fed to broilers was characterised by inefficient feed conversion, reduced growth rate, increased relative weight of the gizzard, proventriculus, spleen and liver, anaemia, and decreased serum levels of lactic dehydrogenase, alkaline phosphatase, albumin, uric acid, cholesterol and triglycerides (Huff et al., Reference HUFF, KUBENA, HARVEY, HAGLER, SWANSON, PHILLIPS and CREGER1986). Harvey et al. (Reference HARVEY, KUBENA, ROTTINGHAUS, TURK, CASPER and BUCKLEY1997) reported additive effects of 100 mg/kg moniliformin and 16 mg/kg DON from naturally contaminated wheat when fed to broilers (Table 1).

Fusarium mycotoxicoses in layers

Layers, like broilers, have been thought to tolerate relatively high concentrations of feed-borne Fusarium mycotoxins. Lun et al. (Reference LUN, YOUNG, MORAN, HUNTER and RODRIGUEZ1986) fed laying hens for 27 days a diet containing 82.8 mg/kg DON and 10.7 mg/kg ZEN from corn inoculated with F. graminearum and found no adverse effect of diet on feed consumption, body weight, egg production or external and internal egg quality. Hens fed corn-based diets containing 38 mg/kg DON did not exhibit any changes in feed consumption, weight gain or egg production (Moran et al., 1987). In a large scale experiment conducted by Keshavarz (Reference KESHAVARZ1993) with laying hens fed naturally contaminated corn-based diets, it was found that incremental concentrations of up to 2.1 mg/kg DON and 0.42 mg/kg ZEN did not have any effect on body weight, body weight gain, feed consumption, egg production or egg quality. Kubena et al. (Reference KUBENA, HARVEY, CORRIER, HUFF and PHILLIPS1987a) reported no effects of naturally contaminated wheat-based diets containing 18 mg/kg DON fed from day one through laying phase on body weight of Leghorn chickens. There was no effect on the age of chickens at the onset of lay or egg albumen height. Hen-day egg production, egg weights, eggshell weight and eggshell thickness were higher in hens receiving DON-contaminated diets. Layers fed the same contaminated grains for 112 days, however, exhibited decreased eggshell weight without alteration in egg production or eggshell thickness (Kubena et al., Reference KUBENA, HARVEY, PHILLIPS, HOLMAN and CREGER1987b). In another study, naturally contaminated wheat-based diets containing up to 10 mg/kg DON and 0.27 mg/kg ZEN did not have any adverse effect on egg production in terms of yield, egg weight and eggshell thickness (Sypecka et al., Reference SYPECKA, KELLY and BRERETON2004). Hamilton et al. (Reference HAMILTON, THOMPSON, TRENHOLM, FISER. P.S. and GREENHALGH1985a) reported an inverse linear relationship between dietary concentrations of up to 0.7 mg/kg DON and egg weight, eggshell weight and eggshell thickness. The feeding of up to 4.9 mg/kg DON in subsequent studies, however, did not result in such a linear relationship. The researchers speculated that the response observed earlier may have been due to differences in nutritional content of the different wheat sources (Hamilton et al., Reference HAMILTON, THOMPSON, TRENHOLM, FISER. P.S. and GREENHALGH1985a).

Dänicke et al. (Reference DÄNICKE, UEBERSCHÄR, HALLE, MATTHES, VALENTA and FLACHOWSKY2002) suggested that the adverse effect of contaminated corn-based diets containing 12.3 mg/kg DON and 3.8 mg/kg 15-acetyl-DON, in addition to lesser amounts of other Fusarium toxins, on laying hens was related to the reduced feed intake at the beginning of the experiment. After this point, birds adjusted to the mycotoxin-contaminated feed. Similar findings were reported by Chowdhury and Smith (Reference CHOWDHURY and SMITH2004) who observed a decrease in egg production, egg weigh and eggshell weight only in the first 4 weeks of feeding diets containing 12.1 mg/kg DON in combination with 0.5 mg/kg 15-acetyl-DON and 0.6 mg/kg ZEN. It would seem that, after the initial reduction in feed intake and egg production, layers increase feed intake in an attempt to maintain egg production. This may result, however, in deterioration in feed efficiency (feed consumed/egg mass). This effect may be caused, in part, by increased hepatic amino acid oxidation due to trichothecene-induced reduction in hepatic protein synthesis (Chowdhury and Smith, Reference CHOWDHURY and SMITH2004). Increased hepatic amino acid oxidation may be responsible for the observed increase in serum uric acid in layers, a finding similar to the observations in broilers. Increased relative kidney weight due to increased excretion of uric acid was also observed in layers (Chowdhury and Smith, Reference CHOWDHURY and SMITH2004). Effects of Fusarium mycotoxins in naturally contaminated diets on layers are summarised in Table 2.

There are discrepancies in the effects of Fusarium mycotoxins on blood chemistry in poultry. Serum uric acid decreased while γ-glutamyl transferase and alkaline phosphatase activities increased in laying Leghorns fed diets containing 18 mg/kg DON from hatching (Kubena et al., Reference KUBENA, HARVEY, CORRIER, HUFF and PHILLIPS1987a). Swamy et al. (Reference SWAMY, SMITH, COTTER, BOERMANS and SEFTON A.E.2002), on the other hand, reported an increase in serum γ-glutamyl transferase activities in broilers fed diets containing a lower DON concentration (4.2 mg/kg) but not at higher concentrations. A decrease in plasma γ-glutamyl transferase activity in layers fed contaminated diets was observed by Chowdhury and Smith (Reference CHOWDHURY and SMITH2004) and can be explained by the inhibitory effect of Fusarium mycotoxins on protein synthesis. Naturally contaminated feedstuffs contain multiple mycotoxins as well as unidentified metabolites which complicate measuring the effects of feed-borne mycotoxins on plasma chemistry. Interpretation of the effect of contaminated diets on some blood parameters such as enzyme activities is also difficult because of the lack of respective reference values (Dänicke et al., Reference DÄNICKE, VALENTA, UEBERSCHÄR and MATTHES2007b).

Like broilers, layers exposed to Fusarium mycotoxins undergo immune-modulations. Layers fed diets naturally contaminated with DON alone or DON combined with other Fusarium mycotoxins had low titres to NDV vaccines administered in the first few weeks post hatching or during laying (Harvey et al., Reference HARVEY, KUBENA, HUFF, ELISSALDE, HOLT, NAQI and PHILLIPS1988; Dänicke et al., Reference DÄNICKE, UEBERSCHÄR, HALLE, MATTHES, VALENTA and FLACHOWSKY2002). Chowdhury et al. (Reference CHOWDHURY, SMITH, BOERMANS and WOODWARD2005c) observed decreased numbers of B lymphocytes and CD4⁺ T lymphocytes as well as reduced biliary IgA concentration in layers fed diets containing 12.1 mg/kg DON.

The significance of Fusarium mycotoxin transmission into eggs appears to be very low in view of the negligible levels reported. The relatively low consumption of eggs compared with other sources of exposure to mycotoxins such as cereal-based products must also be considered. The feeding of diets containing 82.8 mg/kg DON to laying hens resulted in no detectable residues in eggs, muscles, or viscera, with the exception of the gizzard musculature (Lun et al., Reference LUN, YOUNG, MORAN, HUNTER and RODRIGUEZ1986). No DON could be detected in the eggs laid by chickens fed up to 18 mg/kg DON from hatching (Kubena et al., Reference KUBENA, HARVEY, CORRIER, HUFF and PHILLIPS1987a) or 5 mg/kg DON from 21 weeks of age through laying (El-Banna et al., Reference EL-BANNA, HAMILTON, SCOTT and TRENHOLM1983). No DON, de-epoxy-DON or their glucuronide conjugates were detected in eggs produced by layers fed diets containing up to 11.9 mg/kg DON and lesser amounts of multiple Fusarium mycotoxins for 16 weeks (Valenta and Dänicke, Reference VALENTA and DÄNICKE2005). Dietary concentration of 1.1 mg/kg ZEN did not result in a detectable residue of ZEN or its metabolites in eggs, ovaries or muscles (Dänicke et al., Reference DÄNICKE, UEBERSCHÄR, HALLE, MATTHES, VALENTA and FLACHOWSKY2002). Mycotoxin transmission from naturally contaminated wheat-based diets containing up to 10 mg/kg DON and 0.27 mg/kg ZEN into eggs was reported at a level corresponding to 0.002% - 0.004% for DON and non-detectable level for ZEN or its metabolites (Sypecka et al., Reference SYPECKA, KELLY and BRERETON2004). The latter authors, however, reported methods with relatively high limits of detection. The low transfer of Fusarium mycotoxins and metabolites into eggs may be explained by complete degradation of the toxins, low transmission into eggs, or transmission into eggs in the form of unidentifiable metabolites (Valenta and Dänicke, Reference VALENTA and DÄNICKE2005).

Fusarium mycotoxicoses in breeders

The feeding of naturally contaminated diets containing up to 18 mg/kg DON to breeders was found to have no effect on fertility, hatchability, or weight of chicks at hatch (Bergsjø et al., Reference BERGSJØ, HERSTAD and NAFSTAD1993; Kubena et al., Reference KUBENA, HARVEY, CORRIER, HUFF and PHILLIPS1987a, Reference KUBENA, HARVEY, PHILLIPS, HOLMAN and CREGER1987b). The feeding of 38 mg/kg DON in F. graminearum-infected corn increased the percentage of non-viable germs and late embryonic deaths (Moran et al., 1987). It is noteworthy that eggs in the latter study had relatively less yolk and more albumen. Yegani et al. (Reference YEGANI, SMITH, LEESON and BOERMANS H.J.2006b) reported increased early embryonic mortality associated with reduced eggshell thickness in eggs produced by broiler breeder hens fed naturally contaminated diets containing 12.6 mg/kg DON, and lesser amounts of 15-acety-DON and ZEN. Lower concentrations of those mycotoxins (Table 3) in diets fed to roosters did not affect semen quality. DON at a concentration of 4.9 mg/kg combined with other Fusarium toxins in naturally contaminated oats increased embryonic developmental anomalies and delayed ossification (Bergsjø et al., Reference BERGSJØ, HERSTAD and NAFSTAD1993). It is interesting that body weight, feed efficiency and egg production were not affected in breeders fed diets contaminated with Fusarium mycotoxins in spite of the various adverse effects in the above-mentioned experiments. Feed restriction may play a role in reducing exposure of breeders to mycotoxins. The high reserve of energy may also help protect these birds from mycotoxicoses (Yegani et al., Reference YEGANI, SMITH, LEESON and BOERMANS H.J.2006b).

Kubena et al. (Reference KUBENA, SWANSON, HARVEY, FLETCHER, ROWE and PHILLIPS1985) reported transitory anaemia characterised by lowered haemoglobin and haematocrit values that were more pronounced at 28 days in male Leghorn chicks fed contaminated diets containing up to 18 mg/kg DON for 35 days. A transitory decrease in blood haemoglobin concentration occurred at 4 weeks of age in male Leghorns fed naturally contaminated wheat-based diets containing 18 mg/kg DON from hatching to 12 weeks of age (Kubena and Harvey, Reference KUBENA and HARVEY1988). Alterations in haematological parameters might have a more profound impact under field conditions (Kubena and Harvey, Reference KUBENA and HARVEY1988).

The effect of Fusarium mycotoxins on avian immunity has recently received considerable attention. Robust immunity is particularly important in breeders to protect these birds during their relatively long life and to ensure success of vaccination programs. It is also required for the transfer of maternal immunity to the progeny at a level sufficient to provide protection during the first few days post hatching. Fusarium mycotoxins, even at concentrations that do not cause obvious adverse effects on performance, can be subtle modulators of immunity (Girgis et al., Reference GIRGIS, SHARIF, BARTA, BOERMANS and SMITH2008). Serum antibody titres to infectious bronchitis virus decreased in broiler breeders fed naturally contaminated diets (Yegani et al., Reference YEGANI, SMITH, LEESON and BOERMANS H.J.2006b). Broiler breeder pullets fed naturally contaminated grains did not restore the pre-challenge percentage of circulating CD8⁺ T cells upon recovery from coccidial infection (Girgis et al., Reference GIRGIS, SHARIF, BARTA, BOERMANS and SMITH2008). Decreased immune response to vaccines has been observed in layers, broilers and other poultry species. Antibodies to Newcastle disease virus (NDV) decreased in layers exposed to DON (Harvey et al., Reference HARVEY, KUBENA, HUFF, ELISSALDE and PHILLIPS1991) or to multiple Fusarium mycotoxins (Dänicke et al., Reference DÄNICKE, UEBERSCHÄR, HALLE, MATTHES, VALENTA and FLACHOWSKY2002). Linear decreases in serum antibody titres to NDV were observed in broilers fed diets containing naturally contaminated wheat with DON concentrations of up to 14 mg/kg (Dänicke et al., Reference DÄNICKE, MATTHES, HALLE, UEBERSCHÄR, DÖLL and VALENTA2003). Adversely affected immune parameters have also been reported in broilers (Swamy et al., Reference SWAMY, SMITH, COTTER, BOERMANS and SEFTON A.E.2002, Reference SWAMY, SMITH, KARROW and BOERMANS2004a), layers (Chowdhury et al., Reference CHOWDHURY, SMITH, BOERMANS and WOODWARD2005c), turkeys (Chowdhury et al., Reference CHOWDHURY, SMITH, BOERMANS and WOODWARD2005b; Girish et al., Reference GIRISH, SMITH, BOERMANS and KARROW2008b) and ducks (Chowdhury et al., Reference CHOWDHURY, SMITH, BOERMANS, SEFTON, DOWNEY and WOODWARD2005a).

Fusarium mycotoxicoses in turkeys

Turkeys are more sensitive to Fusarium mycotoxins than other avian species. Earlier reports suggested that turkey poults would tolerate 5 mg/kg DON in naturally contaminated wheat-based diets without any significant changes in feed intake or body weight gain (Hamilton et al., Reference HAMILTON, TRENHOLM, THOMPSON and GREENHALGH1985b). Increasing proportions of artificially contaminated wheat in turkey diets up to 5.4 mg/kg DON and 0.4 mg/kg ZEN, however, resulted in a dose dependent decrease in body weight gain and an increase in serum glutamate dehydrogenase activity (Dänicke et al., Reference DÄNICKE, VALENTA, UEBERSCHÄR and MATTHES2007b). Even lower levels of DON, combined with 15-acetyl-DON and ZEN, in naturally contaminated diets caused decreased body weight gain, increased plasma uric acid, and increased relative weight of the gizzard and bursa of Fabricius (Girish et al., Reference GIRISH, SMITH, BOERMANS and KARROW2008b). Feeding highly contaminated grains to turkeys for 12 weeks reduced growth rates in all growth phases. Body weight gain decreased as early as the third week of feeding (Chowdhury and Smith, Reference CHOWDHURY and SMITH2007).

It was observed that cellular and humoral immune responses decreased in turkey poults fed for 12 weeks diets containing corn and wheat naturally contaminated with up to 3.3 mg/kg DON and lesser concentrations of 15-acetyl-DON and ZEN (Girish et al., Reference GIRISH, SMITH, BOERMANS and KARROW2008b). These birds also had decreased blood total lymphocytes and CD4⁺ T lymphocyte subsets. Chowdhury et al. (Reference CHOWDHURY, SMITH, BOERMANS and WOODWARD2005b) reported transient immune changes in turkey poults comparable to those observed in layers (Chowdhury et al., Reference CHOWDHURY, SMITH, BOERMANS and WOODWARD2005c) suggesting that Fusarium mycotoxins affect cell-mediated immunity more than humoral immunity.

Girish et al. (Reference GIRISH, MACDONALD, SCHEININ and SMITH2008a) reported significant decreases in the concentrations of 5-hydroxyindoleacetic acid (5-HIAA) and 5-HIAA: 5-hydroxytryptamine (5-HT) ratios in the pons region of brains of turkeys fed Fusarium mycotoxin-contaminated diets for 6 weeks. These changes in brain neurochemistry may be related to altered behaviour and emotional stress in turkeys. Comparable findings in brain neurochemistry have been described in layers fed naturally contaminated diets (Yegani et al., Reference YEGANI, CHOWDHURY, OINAS, MACDONALD and SMITH2006a). Feeding naturally contaminated diets containing 3.3 mg/kg DON, and lesser amounts of 15-acetyl-DON and ZEN, reduced villus heights (VH) in the duodenum of turkey poults in the starter phase, and reduced VH and apparent surface area (AVSA) in the jejunum in the starter and grower phases (Girish and Smith, Reference GIRISH and SMITH2008). These birds had reduced growth rate (Girish et al., Reference GIRISH, SMITH, BOERMANS and KARROW2008b). Reduced duodenal VH and AVSA have been observed in broiler breeder pullets fed naturally contaminated diets containing 3.8 mg/kg DON and lesser amount of 15-acetyl-DON and ZEN. Unlike turkeys, broiler breeder pullets suffered no changes in growth rate, and appeared to have a compensatory increase in the VH and AVSA of the jejunum and ileum (Girgis et al., Reference GIRGIS, BARTA, BRASH and SMITH2010).

In turkey poults fed diets containing up to 5.4 mg/kg DON, concentrations of 13-23 ng/ml DON and 4 ng/ml de-epoxy-DON were detected in bile but none was detected in plasma, liver or muscle (Dänicke et al., Reference DÄNICKE, VALENTA, UEBERSCHÄR and MATTHES2007b). Those authors suggested that turkeys have a higher capacity to metabolize ZEN than laying hens and ducks. In the experiments conducted by this group, the mean proportions of ZEN, α-zearalenol (α-ZEL) and β-ZEL in turkey poults were 19%, 77% and 4%, respectively, whereas the respective figures in laying hens were 75%, 15% and 10%, and in ducks 80%, 16% and 4%. (Dänicke et al., Reference DÄNICKE, UEBERSCHÄR, HALLE, MATTHES, VALENTA and FLACHOWSKY2002; Dänicke et al., Reference DÄNICKE, UEBERSCHÄR, VALENTA, MATTHES, MATTHÄUS and HALLE2004; Dänicke et al., Reference DÄNICKE, VALENTA, UEBERSCHÄR and MATTHES2007b). Effects of feed-borne Fusarium mycotoxins on turkeys are summarised in Table 4.

Fusarium mycotoxicoses in ducks

Ducks appear to be the most resistant poultry species to feed-borne Fusarium mycotoxins. Mallard ducks did not exhibit reduced feed intake when fed wheat containing 5.8 mg/kg DON for 14 days. There were no apparent adverse effects on body weight, serum chemistry or organ weights (Boston et al., Reference BOSTON, WOBESER and GILLESPIE1996). Dänicke et al. (Reference DÄNICKE, UEBERSCHÄR, VALENTA, MATTHES, MATTHÄUS and HALLE2004) reported no effect of up to 7 mg/kg DON and 0.06 mg/kg ZEN, in combination with other Fusarium mycotoxins, on the performance and health of Pekin ducks. Feed intake and body weight gain were not affected although during the 1st week of the experiment a slight depression in weight gain was observed, which was compensated for during subsequent weeks. Higher contamination levels (18.6 mg/kg DON) did not affect production parameters in ducks but only induced minor or transient changes in haematological and immunological parameters (Chowdhury et al., Reference CHOWDHURY, SMITH, BOERMANS, SEFTON, DOWNEY and WOODWARD2005a). A dose dependent decrease in the relative weight of the bursa of Fabricius was observed in ducks fed contaminated wheat but DON, ZEN and their metabolites were not detected in plasma or liver (Dänicke et al., Reference DÄNICKE, UEBERSCHÄR, VALENTA, MATTHES, MATTHÄUS and HALLE2004). Khajarern et al. (Reference KHAJARERN, KHAJARERN, MOON and J.H.2003) observed a decrease in the relative weight of bursa and testis, and an increase in the relative weight of the oviduct in ducks fed diets containing 0.15 mg/kg ZEN from naturally contaminated soybean meal. The presence of further Fusarium toxins was not reported, but contamination with DON is very likely if ZEN is present in naturally contaminated feedstuffs. Activities of glutamate dehydrogenase, γ-glutamyl transferase, aspartate aminotransferase and creatine kinase in serum were either not affected or were inconsistently affected by exposure to DON (Boston et al., Reference BOSTON, WOBESER and GILLESPIE1996; Chowdhury et al., Reference CHOWDHURY, SMITH, BOERMANS, SEFTON, DOWNEY and WOODWARD2005a). Effects of feed-borne Fusarium mycotoxins on ducks are summarised in Table 5.