Occurrence and Significance of Mycotoxins in Forage Crops And
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J Sci Food Agric 1998, 77,1È17 Occurrence and Signiücance of Mycotoxins in Forage Crops and Silage: a Review Keith A Scudamore1* and Christopher T Livesey2 1 Central Science Laboratory, London Road, Slough, Berks, SL3 7HJ, UK 2 Veterinary Laboratories Agency, New Haw, Woodham Lane, Addlestone, Surrey, KT15 3NB, UK (Received 5 December 1996; revised version received 29 May 1997; accepted 4 September 1997) Abstract: Study of mycotoxins in animal feeding stu†s has concentrated on the occurrence of aÑatoxins and, to a lesser extent, other mycotoxins in cereals, raw materials and concentrate feeds. However, ruminant diets contain a high propor- tion of forage crops such as grass or maize silage, hay and straw. Under adverse growing, production or storage conditions, fungal spoilage is likely to occur with some degree of mycotoxin contamination. The mould Ñora of forage crops is likely to di†er signiÐcantly from that of cereals and mycotoxin contamination, should it occur, could di†er qualitatively and quantitatively. Information relating to forage crops as a potential source of mycotoxins is reviewed. Some Ðeld inci- dents and animal disease which may be mycotoxin related are discussed and analytical methods are reviewed. Information on dose and e†ect of candidate mycotoxins is given where available. The review suggests areas which the authors consider merit further study. Crown Copyright 1998. J Sci Food Agric 77,1È17 (1998) Key words: mycotoxins; fungi; moulds; silage; forage crops; hay; straw; occurrence; analysis; risk assessment; animal disease INTRODUCTION access, silage will be at risk from storage moulds such as Penicillium and Aspergillus. However, moulds may be During growth, forage crops are at risk in the Ðeld from aerobic or anaerobic and this means that, even if infection by a number of di†erent fungi, some of which oxygen is excluded, some moulds may be able to may produce mycotoxins. These fungi include species of develop and metabolism proceed. Fusarium, Alternaria, Cladosporium, Claviceps and Stored hay and straw, if not dried e†ectively, could endophytic infections of grass. Consequently, forage give rise to similar or additional moulds and toxins. crops at harvest or when directly grazed could contain a Surveillance for mycotoxins in cereals and animal feeds number of potential toxins. Good quality silage is pre- for instance (Scudamore et al 1986a, 1997) has shown pared from grass, maize or other crops and by-products that, where mycotoxins are identiÐed, mixtures of these under anaerobic conditions and, if oxygen is suc- toxins can also occur. Since the use of silage and similar cessfully excluded, further mould growth and mycotoxin feeding stu†s is increasing, it is important to assess development is unlikely. These conditions also tend to whether mycotoxin contamination is occurring and, if reduce levels of some mycotoxins should they already so, whether it is a potential threat to human or animal be present at ensilement. If air subsequently gains safety. Silage making in the UK, for example, has developed * To whom correspondence should be addressed at: KAS Mycotoxins, 6 Fern Drive, Taplow, Maidenhead, Berkshire, into the biggest preservation operation carried out on SL6 0JS, UK. farms. Approximately 40 million tonnes of crops are Contract/grant sponsor: MAFF. harvested, transported and stored for later use each 1 Crown Copyright 1998. J Sci Food Agric 0022È5142/98/$17.50. Printed in Great Britain 2 K A Scudamore, C T L ivesey year and in 1990, about 90% of the total silage was pre- are susceptible to infection in the Ðeld by a range of pared from grass, with maize, legumes, whole-crop fungi and some may also produce toxic metabolites cereals and by-products such as brewers grains playing should appropriate conditions arise. This can occur in only a minor role (Wilkinson 1990). Maize is also used conditions ranging from cool, damp weather, to widely in Europe. Silos may be stacks, bunkers or pits drought when crops become stressed. A number of Ðtted with roofs to prevent rain damage. Big bale silage moulds are also plant pathogens and cause disease in is increasing in popularity. There is a huge choice of the crop. additives available including 45% sulphuric acid, formic Grass is grazed directly by ruminants and several and propionic acids, enzymes and cultures of lactic acid mycotoxicoses are known, or suspected to arise, as a bacteria. result of moulds or fungal endophytes present in the When crops are harvested and stored, most of the grass (eg Lewis and Clements 1986). Any such moulds toxic compounds present will remain stable under or toxic metabolites will be present by the beginning of aerobic conditions. However, the Ðeld-derived fungi the silage or hay making processes. will, in time, be replaced by storage fungi, particularly Cereals such as wheat, barley and maize may be simi- with inadequate drying or if the moisture content is not larly infected with Fusarium, Alternarium, Cladosporium maintained below about 15%. and other fungi (Niles 1980). The formation of mycotox- The range of materials likely to be sources of myco- ins in cereal grains has been studied extensively and is toxins include pasture grass grazed directly, dried grass, not considered further. The production of maize silage husks or cha† used as components of compound feeds, entails incorporation of the whole plant, seed and green by-products such as sugar pulp, brewers grains and dis- matter. Therefore, the extent and type of infection tillers grains, hay and straw (both barley and wheat), a†ecting all parts of the maize plant, rather than solely grass (which may also contain leguminous plants such in the grain, must be considered. Whole barley and as clovers) and maize silage subject to spoiling following wheat plants are sometimes used in the same way. access of oxygen (Anon 1995). Mycotoxins would not be Straws arising from harvested barley or wheat contain expected in properly prepared and maintained silage few seeds although hay will contain grass seeds them- although some “ÐeldÏ mycotoxins such as zearalenone selves subject to fungal infection. have been reported to survive ensilage. Considerable research has been carried out on the acute and chronic toxicity of some single pure mycotox- Fungal growth during ensilation ins to a range of laboratory and domestic animal species, but sub-clinical toxicological e†ects (such as Silage making is based on the principle of preservation immunosuppression) and possible synergistic inÑuence under anaerobic conditions together with the growth of of mycotoxin mixtures has received little attention. lactic acid bacteria which promote a natural fermenta- There have been few cases in which a mycotoxicosis tion, lowering the pH to a level at which clostridial has been proven as the cause of disease in livestock. growth is prohibited. The conditions associated with However, this does not preclude the existence of well preserved silage, ie low pH and anaerobiosis, are mycotoxin-associated animal disease problems. In addi- also unfavourable for the growth of most moulds. tion, mycotoxins at sub-clinical levels in animal feeds Exclusion of air should ensure that few fungi are able to might be translocated to human food through meat and grow or survive under these conditions. Indeed, their animal products (eg Allcroft 1969; Hult et al 1980). presence in silage is unwelcome since they not only Forage crops and silage have received little attention. In break down sugars and lactic acid, but also metabolise a major review commissioned by the EC (Smith et al cellulose and other cell wall components and may also 1994), less than two pages included mention of forage produce mycotoxins. The acidic anaerobic fermentation crops or silage. of good silage may also metabolise some of the myco- This paper reviews existing information on mould toxins already present at harvest. Damaglou et al (1984) spoilage of forage crops and possible mycotoxin prob- inoculated rye grass with Fusarium roseum and F tri- lems. cinctum prior to ensiling in laboratory experiments. Although F tricinctum survived longer than F roseum, there was only 1% remaining after 15 days. Pre-formed FORAGE CROPS AND SILAGE AS SOURCES zearalenone only remained stable for a very short time OF FUNGI AND POTENTIAL MYCOTOXIN in grass or after ensiling (Hacking 1979). However, CONTAMINATION silage made from corn cob maize infected with F culmo- rum and containing naturally produced zearalenone was Infection in the Ðeld studied over a 12 week period. By 11 days, no F culmo- rum could be isolated but zearalenone levels remained Animal fodder and silage are prepared from harvested unchanged for the whole 12 week period (Lepom et al growing crops such as grass and cereals. These crops 1988). Mycotoxins in forage crops and silage 3 Fungal development during storage of hay and straw Sclerotia (ergot bodies) are commonly produced by several species of Claviceps and may be found in pasture Fungi present at harvest in hay and straw are likely to grasses and cereals. Langdon (1954) listed at least 30 persist during storage even if further fungal growth is di†erent species of Claviceps. Fortunately, ergotism in prevented by drying. If the crops become damp and man is no longer prevalent but remains a potential risk fungal growth occurs, Ðeld species of fungi are likely to for animals. Ergots do occur but the dose of the toxic be gradually replaced by storage fungi such as species of compounds associated with them is usually at a sub- Penicillium and Aspergillus. The rate at which this clinical level (Osborne et al 1988). happens depends on the conditions of storage. Poor storage conditions, caused by insufficient drying, con- densation, leakage of rain water or insect infestation, Silage can lead to further mould growth and heating. Live- stock may then be faced with the dual hazard of myco- During a survey of moulds infecting stored maize silage toxins and high levels of fungal spores in the in France and Italy, Pelhate (1977) achieved a non- atmosphere.