Fungi

In addition to O. ulmi s.l., over fifty fungal species have been found on beetle-infested elm bark {[426],[548]}. A limited number of these fungi are able to compete with the DED fungus for space and nutrients in uncolonized bark (primary antagonists), or to replace O. ulmi s.l. within the host tissue (secondary antagonists) {[426]}. Besides these two types of antagonist, there are fungi such as Verticillium dahliae, which are able to induce the resistance of the elm tree to subsequent infection with O. ulmi s.l. (see DED control) {[621],[625]}.

In the terminology of Gibbs et al. {[426]}, primary antagonists are fungi with some pathogenic abilities that are able to colonize living or dying phloem. Secondary antagonists become abundant weeks or months after bark invasion by primary colonizers. In general, the abilities of the latter group to invade and establish living elm phloem are poor {[426],[548]}. Replacement of the DED fungus may occur through mycoparasitism and/or the production of antibiotics {[548]}. The deuteromycetous fungus Phaeotheca dimorphospora has been shown to synthesize toxic compounds able to lyse O. ulmi conidia and mycelia in vitro {[213]}. Therefore, this fungus can be considered a secondary antagonist of O. ulmi. However, Bernier et al. {[119]} showed that inoculation of elm seedlings with P. dimorphospora prior to infection with the DED fungus results in high resistance to DED. In these experiments, P. dimorphospora appears to induce resistance of the host tree.

The influence of antagonists on the development of the different species within the O. ulmi s.l. complex has been found to vary; e.g., compared to O. ulmi, O. novo-ulmi has a higher tolerance for P. dimorphospora {[119]}.

In Table 7, a number of fungi shown to exhibit antagonistic activities towards O. ulmi s.l. in vitro and/or in vivo are listed. The fungi Phomopsis oblonga, Botryoshaeria stevensii,Nectria coccinea, and Fusarium solani are elm bark inhabitants with a significantly stronger bark colonizing capacity than O. ulmi. In addition, the first three of these fungal species appear to be more effective as bark colonizers than O. novo-ulmi {[548]}. P. oblonga – a major colonizer of diseased elm bark – is also abundantly present in the dead outer bark layers of healthy elms {[539]}. From its base in the outer bark, P. oblonga is able to rapidly invade large areas of dying inner bark tissue before the bark beetles start breeding, thereby preventing establishment of vector-introduced O. ulmi s.l. {[548]}.In contrast to P. oblonga, B. stevensii and N. coccinea rarely colonize large areas of inner bark before initiation of beetle breeding activities. Several fungi exhibit a dual detrimental effect on both the growth of O. ulmi s.l. and the development of elm bark beetles, e.g., P. oblonga and entomogenous fungi Metarhizium and B. bassiana {[347],[483],[602],[619]}. However, the two last-mentioned fungal species act as antagonists only against O. ulmiin vitro {[619]}. As with a number of other fungi which exhibit growth inhibition of the DED fungus in vitro, their activity in planta remains to be determined {[618]}.

Table 7:  Primary and secondary fungal antagonists of O. ulmi s.l. {[119],[213],[371],[426],[483],[548],[577],[597],[ 618],[619]}