R O Clements
Institute of Grassland and Environmental Research, North Wyke Research Station, Okehampton, Devon, EX20 2SB, UK.
Abstract
Introduction
Pest damage
Disease damage
Control measures
Conclusions
Acknowledgements
References
Despite its well recognised attributes for agriculture, white clover does not always thrive. It has become apparent that a major contributory reason for this is the ravages of various pests and diseases. Sitona weevils, slugs (e.g. Deroceras), various nematodes, especially stem nematode (Ditylenchus dipsaci) and cyst nematodes (Heterodera trifolii), and the fungal disease, clover rot (Sclerotinia trifoliorum), are all implicated. The significance of other foliar fungal diseases has not been fully evaluated although leaf spots are common as are several viruses and although all these can reduce yield, vigour and competitiveness, effects are largely unquantified. Losses of clover seedlings caused by slugs, Sitona and other organisms are also significant.
Determining the magnitude of damage caused to clover by pests and diseases is complicated because the direct effects on clover growth and development are compounded by indirect adverse effects on it's ability to fix N that otherwise would contribute to growth of the sward. Further complicating any assessment is the fact that, ultimately, losses are manifested by reduced animal production. Some clover pathogens may also affect animal health.
Insect and mollusc pests and possibly some fungal diseases could probably be controlled with agrochemicals, although the desirability of this seems dubious for economical and environmental reasons. One possible exception could be the use of seed dressings to control seedling pests and diseases. There is no prospect of directly controlling virus diseases with agrochemicals although insect vectors of some viruses are potential targets. There are several indications that slugs, nematodes, clover rot and Sitona weevils could be controlled by breeding resistant plants. It may also be possible to develop other biological control strategies or cultural methods for these pests.
Considerable effort is being focused on exploiting the potential of white clover in animal production systems. Despite the many advantages of clover the proportion in established grassland is often small, (Hopkins et al., 1985). Possibly less than 5% of pastures in the UK contain optimal amounts of clover. There are many reasons why clover fails to thrive, including inadequate phosphate fertilizer input, high N fertilizer use, inadequate pH, overgrazing, wrong choice of variety and misuse of herbicide. However, injury by pests and diseases is also frequently obvious, and is probably at least partly responsible for the demise or poor growth of clover in many instances.
Much of the published literature relating to pests and diseases of white clover in Europe stems from work done in the UK, France and Poland. For example Raynal et al., (1989) detail the biology of the major pests and diseases of several forage legume crops, including clover and give much further useful information. Tables indicate which pests occur on which legume crops (in France) and also which viruses occur. They also point out the difficulty of quantifying damage in white clover. There are few reports from other European countries, although work done in New Zealand and parts of the USA is relevant.
In Europe the foliage of white clover is attacked by several pests (Mowat and Shakeel, 1988). In a survey in England and Wales (Lewis and Thomas, 1991) the mean number of leaves damaged by slugs ranged from 23% to 67%, while that by weevils (Sitona spp.) ranged from 3% to 62%. In a related survey on commercial farms total damage i.e. % of leaf area removed or colonised by various organisms, over 10 sites and 24 dates averaged some 11.9%. Damage by Sitona, molluscs, pigeons, seed weevils (Apion) and leaf diseases averaged, over all sites and dates, 7.5, 1.8, 0.4, 0.1, and 0.3% respectively (Clements and Murray, 1993). In an earlier survey where poorly growing clover was sampled, stem nematode occurred at 41% of sites (Cook et al., 1992). Clearly these results indicate a generally high incidence of pest damage, particularly by slugs and Sitona spp.
Patches of poor growth in once uniform swards may also be a good indication of damage by stem nematode (Ditylenchus dipsaci). In England and Wales, 40% of swards were infested (Cook et al., 1992), and D. dipsaci is most probably present wherever white clover has become naturalised. There is other evidence, from New Zealand, that stem nematodes contributed to poor vigour of at least some white clover varieties (West and Steele, 1986). In the Netherlands Ennik et al., (1970) found that white clover responded positively to agrochemical application and attributed the response to the control of nematodes.
Cook and Yeates (1993) recently summarised work done on clover cyst nematode (H. trifolii). which is widely distributed throughout at least the temperate world.
There is a considerable volume of literature relating to damage by slugs on arable crops, but very little relating to clover. However, in a white clover variety trial incidence of feeding damage by molluscs was high on all varieties, but large differences between them were apparent (Ferguson et al., 1989).
As well as damaging leaves, molluscs also graze and damage growing points and transmit at least one important clover disease, namely white clover mosaic virus (WCMV), and at least one nematode pest (Cook et al., 1989). Sitona and Apion larvae damage root and stolons.
Hopkins and Gilbey (1987) applied pesticides to grass/clover swards and obtained significant yield increases. Pesticide application increased the DM production of nine white clover varieties studied by Clements and Henderson (1983) by, on average, 9% in 1978 and 13% in 1979. In related work in Northern Ireland (Mowat and Shakeel, 1989), pesticide treatment produced large increases in clover content and yield over a 3-year period.
James et al., (1980) and Chamblee et al., (1983) reported that a pathological-entomological complex is a major factor involved with lack of persistence of clover in north-eastern USA. In work in New Zealand, pesticides applied to ryegrass/clover pasture significantly increased clover production, N fixation and the number of nodules per root (Steel et al., 1985).
During establishment, weevils and other pests cause damage and major loss of seedlings (Barratt and Johnstone, 1984), (Clements et al., 1982).
Pests and diseases affect clover seed production. For example, Foulkes and Clifford (1990) found that controlling all pests and diseases increased clover seed yield from 521 to 917 kg ha-1. Wiech and Wnuk (1987) studied the biology and occurrence of Apion virens on white clover seed production in Poland and found differences between varieties of the numbers of eggs laid and of leaf damage.
Lenné (1989) described some problems associated with the evaluation of diseases of pasture plants in general. Commonly, visual estimates of disease incidence and severity are based on assessment keys and scales, which Thomas (1985) criticised because of the lack of standardized sampling methodology.
However, Gibbs et al., (1966) collected and tested 683 plants from old pastures in Britain and 23% were infected with viruses. Scott and Hughes (1979) examined white clover plants from 49 upland sites in Great Britain and France and only four plants contained no viruses.
Mycoplasma-like organisms (MLO) also occur. White clover phyllody has been observed since the 17th century and is now known to be caused by the same persistent leaf-hopper transmitted MLO as that responsible for strawberry green petal.
O'Rourke (1970) reported on disease surveys in Ireland. About twelve diseases were found to occur commonly; all have been recorded elsewhere and some are thought to affect yield and quality seriously.
In a survey of the distribution and prevalence of pathogens in a naturally infected field of white clover grown for seed in Poland white clover was infected by a number of pathogens (Nadolnik, 1981). The most prevalent attacking leaves were: Peronosproa trifoliorum, Pseudopeziza trifolii and Ascochyta trifolii. The stem, peduncles and occasionally also leaves were infected by Kabatiella caulivora and Botrytis cinerea. Flower greening caused by mycoplasmas was also present.
Oestrogenic coumestans accumulate in diseased white clover leaves (Newton and Betts, 1973; Saba et al., 1972) which leads to the possibility that the reproductive performance of sheep may be adversely affected. Bowen (1978) commented that pests and diseases may affect clover nodulation and the ability of the plant to fix N.
In Great Britain, clover rot (Sclerotinia trifoliorum) is usually considered an important disease of red clover (T. pratense) but not of white clover, substitution of white for red clover being recommended as a control measure (Dillon-Weston et al., 1946). However, in recent years the disease has become prevalent and damaging on white clover (Scott, 1981). Scott and Evans (1980) found that herbage DM yields of sown plots of white clover were greatly reduced by a natural infection of clover rot, the extent of the reduction being related to the level of infection. There is also some evidence from other countries that clover rot is a problem. For example, Hughes et al., (1962) in the U.S.A. and Willis (1966) in Canada have all reported damage to white clover under field conditions.
Murray and Clements (1992) and Clements and Murray, (1993) indicated clearly that there is considerable scope for breeding Sitona resistant varieties, but more needs to be known about the biology of the weevils and the impact of their larvae on N cycling. In New Zealand Sitona weevils in lucerne have been controlled by the introduction of a parasitic wasp (Barlow and Goldson, 1993). P.J.Murray (pers. comm.) has shown recently that the parasites are prevalent in Europe under some conditions.
Despite the impact of cyanogens in clover decreasing attack by slugs, there can be animal husbandry problems associated with increasing the cycanogenic potential of clover so clovers with a high content of cyanogens are not on the Swiss Recommended List (Lehmann et al., 1991).
Slugs can be controlled effectively in some crops by the use of a nematode parasitoid (Wilson et al., 1993) and there seems no reason why this could not be developed for use in grass/clover crops.
Pests and diseases frequently imperil the growth and persistence of white clover although there appear to be no reliable estimates in cash terms of the losses caused. The major pests and diseases have been identified with some degree of certainty, at least for countries in western Europe. Considerable damage is caused by Sitona weevils and by slugs. There is also evidence to indicate the widespread occurrence and importance of clover rot (Sclerotinia) and some nematodes (Ditylenchus and Heterodera). Viruses may also be important. Foliar leaf-spotting fungi are common, but they do not appear to greatly reduce clover's persistence in the field. Apion and Sitona weevils reduce yields of clover seed crops.
There is a substantial need to devise appropriate control measures for these damaging organisms. The desirability of developing agrochemicals for this purpose seems dubious for economical and environmental reasons. Possible exceptions could be the use of seed dressings to control seedling pests and diseases and chemicals to control pests of clover seed crops. There is no current prospect of directly controlling virus diseases with agrochemicals although insect vectors of some viruses are potential targets. There are several indications that slugs and Sitona weevils could be controlled by breeding resistant plants - possible via increasing clover's cyanogenic potential. It may be possible to use biological control strategies or cultural methods to control slugs and Sitona, but more research would be needed. There is strong evidence that nematodes and clover rot (Sclerotinia) would best be controlled using plant resistance and considerable progress towards this end is being made. Virus diseases would also best be controlled by plant breeding.
The Institute of Grassland and Environmental Research is a BBSRC sponsored Institute and the above article was abstracted from a review written while the author was in receipt of MAFF commission research funds.
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