Ophiostoma novo-ulmi (Dutch elm disease)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- History of Introduction and Spread
- Risk of Introduction
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Notes on Natural Enemies
- Means of Movement and Dispersal
- Pathway Vectors
- Plant Trade
- Wood Packaging
- Vectors and Intermediate Hosts
- Impact Summary
- Environmental Impact
- Impact: Biodiversity
- Social Impact
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Distribution Maps
Don't need the entire report?
Generate a print friendly version containing only the sections you need.Generate report
PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Ophiostoma novo-ulmi Brasier 1991
Preferred Common Name
- Dutch elm disease
Other Scientific Names
- Ceratocystis ulmi sensu auct.
- Ceratostomella ulmi sensu auct.
- Graphium ulmi sensu auct.
- Ophiostoma ulmi sensu auct.
- Pesotum ulmi sensu auct.
International Common Names
- Spanish: grafiosis
- French: maladie hollandaise de l'orme
Local Common Names
- Austria: Holländische Ulmenkrankheit; Ulmensterben
- Germany: Holländische Ulmenkrankheit; Ulmensterben
- Switzerland: Holländische Ulmenkrankheit; Ulmensterben
- OPHSNU (Ophiostoma novo-ulmi)
Summary of InvasivenessTop of page
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Fungi
- Phylum: Ascomycota
- Subphylum: Pezizomycotina
- Class: Sordariomycetes
- Subclass: Sordariomycetidae
- Order: Ophiostomatales
- Family: Ophiostomataceae
- Genus: Ophiostoma
- Species: Ophiostoma novo-ulmi
Notes on Taxonomy and NomenclatureTop of page
O. novo-ulmi is most closely related to a group of Ophiostoma species called the O. piceae-complex (Harrington et al., 2001). In molecular studies O. novo-ulmi shows high affinity to its sister taxon O. ulmi, but also to O. himal-ulmi and O. quercus. With the exception of the three DED fungi, species in the O. piceae complex are weak parasites or saprobes on both conifers and hardwoods (Smalley et al., 1993b).
DescriptionTop of page
Hyphae are septate, and ca 1-6 µm diameter; the aerial hyphae are often aggregated into strands. Mycelial conidia are usually produced abundantly. The sporothrix conidiophores are mostly lateral, ca 10-30 µm long; their conidia are borne on short denticles of 0.5-1 µm. Sporothrix-like conidia are non-septate, hyaline, variably ellipsoid to elongate, often tapering and slightly curved, with a small attachment collar. Conidia are 4.5-14 x 2-3 µm. The mycelial conidia are often aggregated into mucilaginous droplets and bud in a yeast-like fashion. The synnemetal anamorph (Pesotum) is usually absent on malt agar and is only produced on elm wood or on media containing elm wood. Synnemata are single or multiple, brown-black, slender and up to 1-2 mm tall. They are attached to the substratum by brown, rhizoid-like hyphae and are composed of parallel bundles of brown, septate hyphae, flaring at the top to branched hyaline hyphae producing non-septate, hyaline, ovoid to ellipsoid conidia (2-6 x 1-3 µm), which aggregate into a cream-white mucilaginous spore drop. The budding, yeast-like anamorph is produced in liquid cultures, and on the surface of solid media. Ascoma (perithecia) are only formed when isolates of different mating types (termed A and B) are present and only on media containing elm wood. The ascoma are globose at the base, black, 75-140 µm wide, sparsely to moderately bristly; their necks are black, 230-640 µm long, and carry numerous ostiolar hyphae. Asci are thin-walled, globose to oval, evanescent. Ascospores are hyaline, non-septate, orange-segment shaped, 4.5-6 x 1-1.5 µm and accumulate as a cream-white mucilaginous spore drop (Brasier, 1991).
O. novo-ulmi subsp. novo-ulmi differs from O. novo-ulmi subsp. americana as follows: the radial growth rate on Oxoid MEA at 20°C is ca 3.1-4.4 mm/day (3.2-4.8 mm/day in subsp. americana). Colonies on MEA at 20°C are commonly irregularly fibrous striate (regularly fibrous striate in subsp. americana). 'Uniform powdery' ('up-mut') mycelial-mycelial dimorphism is present (not present in subsp. americana). Ascoma have neck lengths of approximately 230-640 µm (only ca 160-420 µm in subsp. americana); the base width is ca 75-160 µm (85-150 µm in subsp. americana); neck length/base width ratio lies between 1.9 and 7.4 (1.6-4.5 in subsp. americana) (Brasier, 1981; Brasier and Kirk, 2001).
Colonies of O. novo-ulmi are prone to degeneration in culture and should be stored at low temperatures, preferentially in liquid nitrogen (Brasier, 1991).
DistributionTop of page
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.Last updated: 25 Feb 2021
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Bosnia and Herzegovina||Present, Widespread||Introduced||Invasive|
|Federal Republic of Yugoslavia||Present, Widespread||Introduced||Invasive|
|North Macedonia||Present, Widespread||1973||Invasive|
|-Southern Russia||Present, Widespread||Introduced||1968||Invasive|
|San Marino||Present, Widespread||Introduced||Invasive|
|United Kingdom||Present, Widespread||Introduced||1971||Invasive|
|Canada||Present||Present based on regional distribution.|
|-Alberta||Present, Few occurrences||Introduced||1998||Invasive||Original citation: Anon. (1999)|
|-New Brunswick||Present, Widespread||Introduced||Invasive|
|-Nova Scotia||Present, Localized||Introduced||Invasive|
|-Prince Edward Island||Present, Localized||Introduced||Invasive|
|United States||Present||Present based on regional distribution.|
|-New Hampshire||Present, Widespread||Introduced||Invasive|
|-New York||Present, Widespread||Introduced||Invasive|
|New Zealand||Present, Localized||Introduced||1989||Invasive|
History of Introduction and SpreadTop of page
Although the spread of DED has been studied for more than 80 years it is still unclear where O. ulmi and O. novo-ulmi have their origin. The most plausible theory is that the fungi were accidentally introduced from an east Asian origin, because some Asian elm species show high resistance to the disease (Smalley and Guries, 2000). During a survey of China in 1986, which included areas of central and eastern China and Xinjiang, no Dutch elm disease pathogens were found on elms, not even an Ophiostoma species (Brasier, 1990). In 1993 a further survey was carried out in the western Himalayas, which led to the discovery of a third DED fungus, Ophiostoma himal-ulmi (Brasier and Mehrotra, 1995). This species proved to be a very aggressive pathogen to European and American elm species, but caused no wilt symptoms on Ulmus wallichiana, its native host. The discovery of this closely related species has led to the suggestion that the eastern Himalaya/Burma region, which is still unsurveyed, could be the origin of O. ulmi and/or O. novo-ulmi, or other DED pathogens (Brasier and Mehrotra, 1995).
Risk of IntroductionTop of page
O. novo-ulmi is already listed as a quarantine pest in several countries. Countries which list only O. ulmi as quarantine pest are also considered here because not all countries have changed to the new nomenclature. Despite the fact that the pathogen is well established in Europe, it is listed as a quarantine pest in several European countries (Switzerland, Hungary, Poland, Norway, Iceland) (OEPP/EPPO, 1999). Other countries which list it as quarantine pest are Algeria, Morocco (OEPP/EPPO, 1999), Canada (Anon., 2003b), China (Anon., 1991), Australia (Anon., 2003a) and New Zealand (Anon., 2002a). However, O. ulmi and O. novo-ulmi are not listed as quarantine pests in any country of the European Union (OEPP/EPPO, 1999) and are not mentioned on the APHIS list of regulated pests for the USA (Anon., 2000). This may pose a significant risk, because the fact that a particular fungal species has been recorded in a given region does not mean that there is nothing to fear from further introductions of what is believed to be the same species elsewhere (Gibbs, 2001). This is emphasised by the example of O. novo-ulmi, which was introduced into the UK when O. ulmi was already established there. The discovery of the endemic O. himal-ulmi in the Himalayas shows that a number of highly aggressive Dutch elm disease fungi or other pathogens of elm may still be undiscovered in some parts of Asia, awaiting their introduction.
Most danger of introduction of DED fungi comes from logs and branches with the bark attached (including firewood), loose bark used for mulching and especially elm wood (with the bark attached) used for crates. The latter goes mostly unrecognized and has been the source of introduction in many cases (Sinclair and Campana, 1978). The fungus may also be present in all parts of an infected elm (except for the seeds), but the highest risk for spread of the disease comes from the bark, as it also harbours the vectors of O. novo-ulmi. To date, there have been no reported cases of deliberate introduction of O. novo-ulmi, but this is theoretically possible. International mail may be used for such an intention.
HabitatTop of page
Hosts/Species AffectedTop of page
Host Plants and Other Plants AffectedTop of page
|Ulmus alata (Winged elm)||Ulmaceae||Main|
|Ulmus americana (American elm)||Ulmaceae||Main|
|Ulmus glabra (mountain elm)||Ulmaceae||Main|
|Ulmus laevis (Russian white elm)||Ulmaceae||Main|
|Ulmus minor (European field elm)||Ulmaceae||Main|
|Ulmus procera (english elm)||Ulmaceae||Main|
|Ulmus pumila (dwarf elm)||Ulmaceae||Main|
|Ulmus rubra (slippery elm)||Ulmaceae||Main|
|Ulmus serotina (red elm)||Ulmaceae||Main|
|Ulmus thomasii (rock elm)||Ulmaceae||Main|
|Zelkova carpinifolia (caucasian elm)||Ulmaceae||Main|
Growth StagesTop of page
SymptomsTop of page
Symptoms usually start to appear between July and autumn leaf fall. When the infection is mediated by bark beetles, symptoms start at single branches, which die back starting from the top. If the disease reaches the stem the whole tree may die in the same year (especially smaller trees) or the year after the infection. O. novo-ulmi is a far more virulent pathogen than O. ulmi and can move from the branches towards the stem in only a few weeks (Scala et al., 1997). Infections via root grafts usually kill a tree faster than infections caused by vectors as the propagules are rapidly distributed throughout the tree with the sapstream (Stipes and Campana, 1981). Recovery of infected elms is rarely seen with O. novo-ulmi infection (Brasier, 1991). If the infection occurs during late summer and autumn, leaves will often only change colour prematurely and have normal budset; however, the branch will be dead in the next spring and the disease will have spread further into the tree.
List of Symptoms/SignsTop of page
|Growing point / dieback|
|Growing point / wilt|
|Leaves / abnormal leaf fall|
|Leaves / wilting|
|Leaves / yellowed or dead|
|Roots / necrotic streaks or lesions|
|Stems / dieback|
|Stems / internal discoloration|
|Stems / mycelium present|
|Stems / necrosis|
|Whole plant / plant dead; dieback|
|Whole plant / wilt|
Biology and EcologyTop of page
There are usually five chromosomes in the haploid genome of O. novo-ulmi. However, Dewar and Bernier (1993) identified an isolate with seven chromosomes. This polymorphism proved stable in pairings with other isolates and did not have any effect on growth and pathogenicity (Dewar and Bernier, 1995; Dewar et al., 1997). Polymorphism in chromosome size and number is a characteristic found in other fungal species (e.g. Kistler and Miao, 1992). The mitochondrial DNA of O. novo-ulmi is 48-71 kb, compared to 74-88 kb in O. ulmi (Brasier, 1991).
Considerable research has been devoted to the molecular characterization of O. novo-ulmi and its differentiation from O. ulmi. Differences between the two species have been found in protein and isoenzyme patterns (Bernier et al., 1983; Jeng and Hubbes, 1983; Jeng et al., 1988), and in RFLPs of mitochondrial (Bates et al., 1993b), nuclear (Bates et al., 1993a) and ribosomal DNA (Hintz et al., 1993). RAPDs have also been used to differentiate the two species (Pipe et al., 1995; Hoegger et al., 1996). Differences have also been found in the cerato-ulmin gene (Jeng et al., 1996; Pipe et al., 1997). The two species are separated most effectively by PCR-RFLP of ribosomal DNA (Harrington et al., 2001).
The two subspecies (subsp. novo-ulmi and subsp. americana) of O. novo-ulmi can be separated using a wide range of markers. The mitochondrial DNA is 65-71 kb in subsp. novo-ulmi compared to 48-60 kb in subsp. americana (Brasier and Kirk, 2001). Differences were found in isoenzyme patterns (Jeng et al., 1988), RFLPs of mitochondrial (Bates et al., 1993b) and nuclear DNA (Bates et al., 1993a), RAPDs, and in the DNA sequence of the cerato-ulmin gene (Pipe et al., 1997). The two subspecies can be further differentiated by PCR-RFLP of their cerato-ulmin and colony type genes (Konrad et al., 2002). Evidence for natural hybridization between the two subspecies in Europe was provided by Jeng et al. (1988) and Konrad et al. (2002).
Both subspecies of O. novo-ulmi and O. ulmi show different degrees of sexual incompatibility to each other. Both species are heterothallic with the two mating types A and B (Shafer and Liming, 1950; Brasier, 1991). While O. novo-ulmi strongly rejects O. ulmi as the male in pairings, O. ulmi unrestrictedly accepts O. novo-ulmi as the male mating partner (Brasier, 1981). In pairings between isolates of the two subspecies, subsp. novo-ulmi partially rejects subsp. americana as the male (ca 90% less fertile perithecia than in novo-ulmi x novo-ulmi matings), whereas in pairings with subsp. americana as the female and subsp. novo-ulmi as the male mating partner, full mating can be observed (Brasier, 1979). These mating barriers strongly support both the species status of O. novo-ulmi and O. ulmi as well as the designation of the two subspecies of O. novo-ulmi. Hybrids between O. novo-ulmi and O. ulmi also show a marked loss in fitness and are transient in natural populations (Brasier et al., 1998), but may act as a 'genetic bridge' in the transfer of genes between the two species.
Mycoviruses, termed d-factors (Brasier, 1983) occur naturally in the cytoplasm of the Dutch elm disease fungi. They spread by hyphal fusion between compatible mycelia and cause detrimental effects on affected isolates, resulting in reduced spore production and loss of virulence (Brasier, 1984). The spread of d-factors within a population is hindered by the production of ascospores, which are free of virus particles, and by vegetative incompatibility (vic) between fungal strains. Hence, diversity in both mating type (allows sexual sporulation) and vic genes (creates incompatibility between mycelia) is an important fitness trait in populations of O. novo-ulmi. Recent evidence suggests that interspecific hybridization events have played a major role in the evolution of Dutch elm disease fungi. O. ulmi introgressants into O. novo-ulmi have been identified in different parts of the O. novo-ulmi population (Brasier, 2001). There is evidence that a pathogenicity gene from O. ulmi introgressed into a hypovirulent isolate of O. novo-ulmi (Et-Touil et al., 1999). The acquisition of a mating type gene of O. ulmi by O. novo-ulmi has been shown and vegetative incompatibility (vic) genes of O. ulmi have also been found in isolates of O. novo-ulmi (Brasier, 2001). These hybridization events and their effect on the vic system of O. novo-ulmi may be, at least partially, responsible for the persistent high fitness of the pathogen population (Brasier, 2000a). The hybridization occuring between the two subspecies of O. novo-ulmi in central and other parts of Europe contributes to the ongoing evolution of the Dutch elm disease fungi (Brasier, 2001; Konrad et al., 2002).
Physiology and Phenology
O. novo-ulmi is the causal agent of the current Dutch elm disease pandemics in North America, Europe and western and central Asia. It exhibits a much higher degree of virulence than O. ulmi (Brasier, 1991). Phytotoxic compounds have been assumed to be responsible for the high level of virulence in O. novo-ulmi. In particular, the role of the hydrophobin cerato-ulmin (CU) in the pathogenesis of DED has been the subject of extensive investigation because it was reported as a wilt toxin (Takai, 1974). CU production is one of the distinguishing features between O. ulmi and novo-ulmi, as O. novo-ulmi (in contrast to O. ulmi) produces moderate to high amounts of CU in liquid culture (Scheffer et al., 1987). Takai (1980) showed a correlation between high CU production and high virulence. The injection of purified CU into elms caused wilting, a reduction in transpiration, an increase in leaf respiration and electrolyte loss (Takai, 1974). Symptoms were the same as those observed in elms infected with the fungus (Takai and Hiratsuka, 1984). The higher aggressiveness of O. novo-ulmi compared to O. ulmi was thus attributed to a higher expression of the protein in the aggressive species caused by differences in the promoter sequence of the CU gene and the derived amino-acid sequence (Jeng et al., 1996). Further evidence suggested that the role of CU should be re-evaluated because a non-CU-producing natural mutant of O. novo-ulmi (Brasier et al., 1995) and mutants induced in the laboratory (Bowden et al., 1996) retained high virulence. CU was therefore proposed to be a parasitic fitness factor, with its main function to protect against desiccation, thereby helping spores to survive during unfavourable conditions such as dispersal (Temple et al., 1997; Temple and Horgen, 2000). However, when non-pathogenic O. quercus was transformed with the CU gene from O. novo-ulmi it was able to cause symptoms of DED on elm (Del Sorbo et al., 2000). This emphasises the need for further investigation of the aetiology of Dutch elm disease.
By analysing European populations of O. novo-ulmi, Brasier (1988) showed that populations can rapidly change their genetic structure after establishment at a new disease location. The initially clonal population commonly consists only of isolates of mating type B with one, or a few, vegetative incompatibility (vic) types predominating. The predominance of mating type B in all populations of O. novo-ulmi has been ascribed to the slightly higher virulence of B type isolates (Brasier, 1991). However, the population soon becomes highly diverse in terms of vic and mating types. High selection pressure for sexual reproduction, which creates vic diversity in the population within a short period of time through the spread of mycoviruses in the clonal population, is believed to be the cause of this phenomenon (Brasier, 1996a). However, differences in the structure of European and North American populations of O. novo-ulmi have been reported. Although European populations generally show a high diversification of vic types at post-epidemic sites, only three vic types made up 88% of the isolates in a study in the USA (Brasier, 1996a). A low incidence of mycovirus infection in North America is believed to be the cause of this difference (Brasier and Kirk, 2000).
The life cycle of O. novo-ulmi is one of the best studied in plant pathology and often is used as a textbook example of insect-pathogen interactions. Two stages are distinct in the life cycle: the parasitic phase involving host colonization, overcoming host resistance, and growth inside the host tissue; and the saprophytic phase inside the bark involving sporulation of the fungus in the breeding galleries of its bark beetle (Scolytus and Hylurgopinus) vectors. As O. novo-ulmi is fully reliant on dissemination by bark beetles, its lifestyle is perfectly adapted to its vectors.
When the young bark beetles emerge in spring from their pupation chambers in the bark of an elm tree they already carry the fungus. The fungus has spread and sporulated inside the breeding gallery of the beetles during the winter and spring. The young beetle is often surrounded in its pupal chamber by synnemata of the fungus and has ample opportunity to catch a high number of spores (Webber, 1990). After pupation, the young beetles fly to the twigs of healthy elms for maturation feeding. They feed on the phloem and also the xylem tissue on branches, in twig crotches or leaf axils. The fungus is inoculated into the elm tree by the beetle during this essential phase. After the establishment of infection, the fungus spreads throughout the xylem vessels of the elm tree in its yeast-like stage and causes a vascular wilt (Sinclair and Campana, 1978). To complete the disease cycle, the pathogen must again come into contact with its vectors. The scolytid beetles must breed in the bark of the dying elms in order for this to occur. As the galleries of the bark beetles superficially penetrate the xylem, the fungus is 'released' from the vascular system of the elm and starts growing into the phloem (bark) of the elm. Other O. novo-ulmi genotypes are introduced into the bark with the beetles (Webber, 2000). The combined process of beetle and pathogen colonization of elm bark is known as the saprophytic phase (Webber et al., 1987). During this phase a marked sequence in sporulation can be seen in the breeding galleries of the bark beetles. The production of fruiting structures appears to follow a predetermined, ontogenetic sequence which starts with the mycelial sporothrix stage, is followed by the formation of synnemata (Pesotum), and ends with the production of perithecia (Webber et al., 1987). Sexual sporulation is important for the fungus to maintain the fitness of the population by the creation of new genotypes. The saprophytic phase is therefore one of the most crucial periods in the life cycle of O. novo-ulmi (Brasier, 1984). In the case of an overwintering brood, the formation of perithecia coincides with the fall in temperature; perithecia might thus act as an overwintering stage (Lea and Brasier, 1983). When the young beetles, which by now carry the fungus, emerge from the breeding systems they fly to the branches of healthy elm trees for feeding. After successful inoculation of the fungus into the elm the disease cycle is complete.
O. novo-ulmi inhabits the xylem and bark of elm trees, particularly in and around the breeding galleries of scolytid beetles. Climatic conditions in the breeding galleries of the bark beetles are important for the growth of O. novo-ulmi inside the bark and its subsequent sporulation (saprophytic phase). Microclimatic conditions are best for the fungus in relatively thick parts of the bark, where the moisture content is highest and relatively constant. Prolonged exposure to high summer temperatures and the combined action of a lower initial moisture content and lack of nutrients in the outer bark usually inhibits sporulation of O. novo-ulmi in stems and branches of smaller diameter (Webber, 1990). The preferred breeding site of a bark beetle therefore largely determines its success as a vector of Dutch elm disease (Webber, 2000).
As the optimum growth temperature for O. novo-ulmi is around 22°C (Brasier, 1981), the pathogen is able to move further to the north than O. ulmi, which has an optimum growth temperature of ca 28°C. This is exemplified by the situation in northern Scotland, UK, where Dutch elm disease became evident only after the arrival of O. novo-ulmi (Brasier, 1996b).
O. novo-ulmi is closely associated with its bark beetle vectors from the genera Scolytus (North America, Europe and western Asia) and Hylurgopinus (in North America only). The bark beetles act not only as vectors, but also provide sites for sporulation of the fungus in their breeding galleries. Scolytus scolytus is the most effective vector carrying up to 350,000 spores (Webber, 1990). About 1000 spores are generally required for effective infection by O. novo-ulmi on an intermediate susceptible host such as Ulmus procera (Webber, 2000). Two smaller species Scolytus multistriatus and S. pygmaeus, are less effective vectors in Europe (Faccoli and Battisti, 1997). Spore load was found to vary between spring-emerging beetles (e.g. 58% beetles infested with spores) and summer-emerging beetles (e.g. only 8% beetles infested with spores) (Faccoli and Battisti, 1997). This probably relates to climatic conditions in the bark, which may be too dry in summer for extensive sporulation to occur. The relationship between O. novo-ulmi and its vectors can be considered as mutualistic because both profit from their combined attack on the elms. However, the vectors do not rely solely on the fungus for creating breeding sites and, in fact, the high aggressiveness of O. novo-ulmi is decimating the number of available hosts for the beetles, especially Scolytus scolytus in Europe, which needs relatively mature trees for successful breeding. Webber and Gibbs (1989) also found that S. scolytus has to feed on phloem tissue that is free of fungal growth for successful development from first- to third-instar larvae, otherwise the larvae are killed.
The role of mites in the breeding galleries of bark beetles must not be disregarded. Although they eat a significant part of the fungal biomass, they also play an important role in the dissemination of fungal spores inside the breeding galleries (Brasier, 1978). Fransen (1939) reported that mites drag the spores of the pathogen through the frass in the larval galleries to the pupal chambers, thus forming a carpet of synnemata inside the chamber, which greatly enhances the opportunities for distribution of the spores by the young beetles. Brasier (1984) showed experimentally that the activity of the mites can enhance sexual sporulation of the fungus.
Notes on Natural EnemiesTop of page
Fungi that compete effectively with O. novo-ulmi in the colonization of diseased bark are Phomopsis oblonga [Diaporthe eres], Botryosphaeria stevensii and Nectria coccinea. D. eres is a very effective antagonist of O. novo-ulmi in vivo because it is already present in healthy elms and can invade the diseased phloem before the bark beetles start to breed (Webber, 1980; Brasier, 1996b).
However, the most important natural antagonists for O. novo-ulmi are fungal viruses and virus-like RNAs, which are of common occurrence in fungi. An extranuclear virus-like factor (the d-factor) which causes degenerative disease in O. novo-ulmi was first identified by Brasier (1983). Several different d-factors have since been identified within the population of O. novo-ulmi (Sutherland and Brasier, 1997). Most are associated with multiple virus-like RNA segments (Rogers et al., 1986). Infection by O. novo-ulmi results in a severe reduction in growth rate and reproductive fitness, depending on the particular d-factor involved. Infected isolates show unstable amoeboid colony morphology in vitro (Brasier, 1983, 1986b). D-factors are spread within the fungal population by hyphal anastomosis and transmission is most effective in isolates of the same vegetative incompatibility type (Brasier, 1983). Selection pressure for high diversity of vegetative compatibility types and sexual reproduction of O. novo-ulmi in Europe has been attributed to the negative effects of d-factors on clonal pathogen populations, where virus spread is not restricted (Brasier, 2000b).
Means of Movement and DispersalTop of page
In addition to dispersal by its vectors, O. novo-ulmi is only known to be spread to new hosts via root grafts, which frequently occur between neighbouring trees, especially in rows of planted trees. This way of dispersal is very effective, because the inoculum goes directly into the stem and is carried upwards with the sapstream, affecting the whole tree simultaneously. Usually no countermeasures can be taken and the elm tree will be killed soon after infection (Stipes and Campana, 1981; Stipes, 2000).
Vector transmission is the most important means of dispersal for O. novo-ulmi. It is associated with bark beetles of the genus Scolytus and Hylurgopinus. The main vectors in Europe and western Asia are Scolytus scolytus, S. multistriatus, S. pygmaeus and S. triarmatus. Other, less important or potential vectors of O. novo-ulmi in Europe and western Asia include Scolytus laevis, S. mali, S. kirschi, S. orientalis, S. ensifer, S. sulcifrons, S. zaitzevi, S. schevyrewi semenor, S. jacobsoni, S. japonicus, Pteleobius vittatus and P. kraatzi (Stipes and Campana, 1981). In North America only two species of bark beetles are known to be vectors of O. novo-ulmi: S. multistriatus (introduced from Europe) and the American elm bark beetle Hylurgopinus rufipes. Three North American species of ambrosia beetles have also been named as probable occasional vectors of the disease: Xylosandrus germanus, Xyloterinus politus and Monarthrum mali (Stipes and Campana, 1981).
The bark beetles breed in the inner bark of cut, diseased, or otherwise weakened elm stems. The dispersing adult beetles fly to healthy elms where they feed (maturation feeding) or directly to declining elms for breeding. During feeding on healthy elms the spores of O. novo-ulmi are introduced into a new host. Scolytus beetles usually feed on twig crotches and prefer vigorously growing young twigs at the crown periphery. Scolytus spp. produce two or more generations each year. The overwintering brood will emerge in May to June and the second brood follows in August. In H. rufipes, one or one-and-a-half generations are produced each year depending on the climate. H. rufipes overwinters either as adult or as larva. For hibernation the adults enter the bark at the base of healthy elm trees, where they are well protected against the cold (Tainter and Baker, 1996). Transmission of the pathogen by H. rufipes occurs either in autumn, when feeding on the lower boles, or more commonly during spring, when feeding in the branches (Stipes and Campana, 1981). Although the endemic H. rufipes is the main vector of DED in northern areas of North America (with winter temperatures below -21°C), the introduced S. multistriatus is the main vector of O. novo-ulmi and O. ulmi in other regions (Haugen, 1998).
Pathway VectorsTop of page
|Land vehicles||Truck, ship, aeroplane, train||Yes|
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Bark||fruiting bodies; hyphae; spores||Yes||Yes||Pest or symptoms usually invisible|
|Growing medium accompanying plants||spores||Yes||Pest or symptoms usually invisible|
|Leaves||spores||Yes||Pest or symptoms usually invisible|
|Roots||hyphae; spores||Yes||Pest or symptoms usually invisible|
|Seedlings/Micropropagated plants||hyphae; spores||Yes||Pest or symptoms usually invisible|
|Stems (above ground)/Shoots/Trunks/Branches||fruiting bodies; hyphae; spores||Yes||Pest or symptoms usually invisible|
|Wood||fruiting bodies; hyphae; spores||Yes||Yes||Pest or symptoms usually invisible|
|Plant parts not known to carry the pest in trade/transport|
|Fruits (inc. pods)|
|True seeds (inc. grain)|
Wood PackagingTop of page
|Wood Packaging liable to carry the pest in trade/transport||Timber type||Used as packing|
|Solid wood packing material with bark||Elm (Ulmus sp.)||No|
|Wood Packaging not known to carry the pest in trade/transport|
|Loose wood packing material|
|Processed or treated wood|
|Solid wood packing material without bark|
Vectors and Intermediate HostsTop of page
Impact SummaryTop of page
|Fisheries / aquaculture||None|
ImpactTop of page
Environmental ImpactTop of page
Impact: BiodiversityTop of page
Social ImpactTop of page
The association of elm and man goes back to prehistoric times and elms have always played an important role in cultural history (Heybroek, 1993b). For example, elms were used for fodder and in agricultural systems, and the wood was important for tools and wheels as well as archery (Richens, 1983). It is especially tragic that a tree that has had so many uses for man is so severely affected by a disease brought about by man.
DiagnosisTop of page
Identification of subspecies of O. novo-ulmi is more complicated and involves a laboratory fertility test, based on the partial reproductive barrier between ssp. americana and ssp. novo-ulmi. Known reference isolates of both subspecies and mating types are required for this test (Brasier, 1981).
Detection and InspectionTop of page
When logs or firewood of elm or Zelkova are inspected, the bark should be searched for any signs of bark beetle breeding. If galleries of bark beetles are found, they should be carefully inspected for the presence of mycelium or fruiting structures of O. novo-ulmi. In conditions that are adverse to the fungus, no sporulation will be seen despite the presence of the fungus in the bark. In such cases, samples should be put into a moist chamber and inspected after a few days for fungal growth. For assurance, isolations from the bark may be needed.
Similarities to Other Species/ConditionsTop of page
Verticillium wilt causes symptoms similar to Dutch elm disease. It is caused by two species, Verticillium dahliae and V. albo-atrum. These soilborne pathogens have been reported from Europe, Asia and North America (Stipes and Campana, 1981). Elm infection with Verticillium usually starts with wilting of the leaves on one or several twigs on a branch. External symptoms of Verticillium wilt resemble those of Dutch elm disease, but crown involvement is less prominent. Systemically infected elms show foliage discoloration, sharply reduced twig growth, and partial leaf abscission on severely infected branches. Before abscission, leaf blades may develop necrotic patches on their surface. Branches often die during the dormant season. A characteristic symptom of Verticillium wilt is sapwood discoloration in the roots, stems and branches. Extensive invasion of the xylem with the fungus may finally result in the death of younger trees and decline in older ones. Positive diagnosis of Verticillium wilt relies on the isolation of the pathogen on suitable media in the laboratory (Stipes and Campana, 1981). Verticillium wilt is more a disease of nurseries and ornamental trees than of forest trees (Butin, 1995).
Dothiorella wilt is another wilt disease that affects elm trees. The causal organism is Dothiorella ulmi, which occurs only in North America but is not believed to be native there (Stipes and Campana, 1981). Symptoms include wilting, yellowing of leaves and dieback of the affected branches. Flat cankers develop on newly killed parts of the bark and pycnidia develop on the bark. A brownish discoloration can be observed in the outer annual rings of the xylem. The disease progresses slowly and may take several years to kill a mature elm tree (Stipes and Campana, 1981). This disease is distinguished from Dutch elm disease by the slower progression of dieback and the presence of cankers and fruiting bodies on the affected branches. In some cases, laboratory isolation of the fungus may be necessary to distinguish it from DED fungi (Boyce, 1938; Stipes and Campana, 1981).
Elm yellows (also known as elm phloem necrosis) is a debilitating or lethal disease caused by elm yellows phytoplasma. Although the disease was first noticed in the USA (Stipes and Campana, 1981), it is now believed to be widespread in Italy and some parts of France (Mittempergher, 2000). The disease has been largely overlooked because it causes only minor disease effects on European elms and the number of symptomatic plants is low. Symptoms on European elms include the formation of witches' brooms and stunted growth. The situation is, however, much more dramatic in North American elm species. Elm yellows is widespread in the eastern USA, where sporadic epidemics have killed endemic elms but not those of Eurasian origin. Elm yellows symptoms on American elm species usually involve rootlet necrosis, degeneration of conductive phloem and cambium in the roots and lower trunk, foliar epinasty, yellowing and leaf casting. Foliage changes colour in a few weeks from green to yellowish-green and reddish-gold before the leaves are cast or suddenly wilt, shrivel, turn brown and remain attached to the twigs. At first only individual branches may be affected but eventually the whole tree will be affected and die. The degenerating phloem is a uniform yellow colour and may in also have small necrotic lesions (i.e. elongated, brown spots on the inner bark surface). Fresh diseased phloem in most North American elm species has a characteristic wintergreen odour (Sinclair, 2000). Elm yellows can be distinguished from Dutch elm disease by the different combination of symptoms (in Elm yellows all branches are affected at once) and the discoloration of the phloem, which is not usually seen in a fresh infection of O. novo-ulmi or O. ulmi. The causal organism of Elm yellows cannot be isolated onto artificial media (Tainter and Baker, 1996).
Low levels of nutrients, summer drought, re-plantation of elm trees, and insect and mite injury can result in leaf discoloration, wilting and leaf fall (Stipes and Campana, 1981). These conditions can be confused with those of Dutch elm disease, but usually the whole tree is affected, not only single branches, and recovery within the next year is common. For assurance, isolations from twigs are needed to distinguish these causes from infection by O. novo-ulmi.
Prevention and ControlTop of page
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.Phytosanitary Measures
The import of elm wood with the bark attached is not allowed into countries with a quarantine for O. novo-ulmi or O. ulmi (e.g. Anon., 2003a). Debarked elm timber has to be properly treated for import. Treatments can consist of kiln drying, ethyl bromide fumigation or other methods able to disinfect the logs (e.g. Anon., 2003b). All shipments of elm wood have to carry a phytosanitary certificate (FAO, 1997) and are subject to inspection. The shipment of live plants of Ulmus is prohibited to some countries such as China (Anon., 1991). The same quarantine regulations apply to Zelkova spp. in some countries (OEPP/EPPO, 1999), and also to Planera sp. (Anon., 2002b). Although seeds have not been shown to carry the disease, the import of elm seeds is prohibited into India with reference to DED fungi (Anon., 1989).
Cultural Control and Sanitary Methods
Sanitation is the most effective way of controlling the Dutch elm disease fungi and may account for 80% of the total effort in urban control programmes (Stipes, 2000). This method is directed against both the pathogen and its vectors. Sanitation can reduce the probability of infection significantly, but cannot eradicate the pathogen or vector. It involves the destruction (burning) of all elm wood attractive to beetle infestation, such as any elm stems and branches weakened, dying, or dead from the disease or any other cause (Stipes and Campana, 1981).
Removal of the entire vascular lesion by pruning can be sufficient for an infected elm to recover from DED. For this approach to be effective, two prerequisites should be taken into account: the elm may not wilt before mid-summer, and early disease detection is necessary, i.e. the elm may not have more than 5% crown damage (Himelick and Ceplecha, 1976). Wilt symptoms observed early in the season are indicative of a DED infection that occurred in a previous year. In this case, the disease will be far more established than is apparent from foliar symptoms, and therapeutic pruning will probably fail. All branches showing characteristic streaking in the outer sapwood are removed. However, if the streaking has reached the stem, the infection will persist in the tree. Cutting tools should be sterilized between different trees. The success of eradicative pruning is limited when bark beetle populations are large, and is most effective in areas where multiple or successive infections are rare (Sinclair and Campana, 1978). Eradicative pruning is mostly used in urban areas, often together with the application of other (chemical) disease treatments, but is not practical in the forest (Haugen, 1998; Stennes, 2000).
Root grafts have been shown to spread O. novo-ulmi infection between trees, especially in hedgerows (Haugen, 1998). Root severance between infected and healthy trees is therefore a common control measure. A spade or trench-digging machine may be used for the purpose, depending on the size of the tree (Burdekin and Gibbs, 1974).
Extensive work has been done in Europe and North America to exploit resistance in the host. Most clones developed for resistance to O. ulmi later proved susceptible to O. novo-ulmi. Today a broad range of elm cultivars is available which show at least some resistance to O. novo-ulmi (Heybroek, 1993a; Smalley et al., 1993a; Townsend and Santamour, 1993). However, resistance, especially in American elm (Ulmus americana) is not yet satisfactory. In addition to the slow progress connected to generation period in elms, the main problem of elm breeding is the fact that the basic mechanisms for disease resistance are still not known (Guries and Smalley, 2000). Genetic transformation has been successfully established in several elm species and may lead to the allocation of resistance genes against O. novo-ulmi as well as to the production of resistant elm cultivars (Gartland et al., 2000).
Several attempts have been made for biological control of O. novo-ulmi. Organisms that have been or could be utilised include bacteria, fungi and mycoviruses.
The bacterium Pseudomonas syringae (not pathogenic to elm) has been reported to suppress the growth of O. novo-ulmi within living American elm (Ulmus americana) (Myers and Strobel, 1983). Inoculation of elm trees with P. syringae prior to infection with O. novo-ulmi induced resistance of the host to Dutch elm disease (Scheffer, 1983) and a similar result was obtained using Pseudomonas fluorescens (Murdoch et al., 1984). Nevertheless, this method is not considered effective today (Stipes, 2000).
The injection of conidial spores of a hypovirulent strain of Verticillium dahliae into the xylem of a healthy elm tree has proved to be effective in inducing resistance to O. novo-ulmi (Scheffer, 1990; Elgersma et al., 1993). This biological control system has been extensively tested in the Netherlands and the USA and is now commercially available in both countries (Voeten, 2003). Sutherland et al. (1995) screened a range of fungi for their ability to induce resistance against O. novo-ulmi infection in European and hybrid elms under field conditions in the UK and Italy. These experiments were carried out with Verticillium dahliae, Ophiostoma piceae and also O. ulmi. Significant symptom suppression was only observed in a few elm clones pretreated with either O. ulmi or V. dahliae. Using a similar approach, a glycoprotein isolated from O. ulmi was used to pretreat American elm clones before inoculation with O. novo-ulmi. Results indicated that the success of induced resistance depends on the genetic constitution of the tree, its health and environmental conditions (Hubbes and Jeng, 1981; Hubbes, 1993, 2003).
Mycoviruses (d-factors) have a debilitating effect on the growth of O. novo-ulmi and can drastically reduce its effectiveness as an elm pathogen. It has been shown that virus infection acts as a selection force within natural populations of O. novo-ulmi (Brasier, 1986b, 1988). One possible approach for utilising the d-factors for biological control would be their artificial release into populations of O. novo-ulmi, which consist largely of isolates of the same vegetative incompatibility type, i.e. they are clonal. Such locations include the Washington DC area and Oregon in the USA (Brasier, 2000b). If successfully introduced into the population, this could lead to a more balanced host-pathogen relationship.
Chemical control against DED fungi has been under investigation since the mid-1930s and over 600 compounds have been tested for DED management ability (Stipes, 2000). Chemicals can either be applied as a soil application or by injection into the vascular system of the tree. The former method has certain environmental drawbacks and therefore the latter is currently preferred.
Six chemicals are currently available in the USA for injection: three benimidazole compounds (carbendazim phosphate, thiabendazole hypophosphite, benzimidizole carbamate), two triazole compounds (propiconazole and tebuconazole) and a patented formulation of copper sulphate pentahydrate (Haugen and Stennes, 1999). Thiabendazole hypophosphite and propiconazole are the compounds most widely used as they show good systemic qualities and work selectively against certain ascomycetes and fungi imperfecti (Klopping, 1960). The injection or infusion (without applying pressure) of systemic fungicides into the xylem is applied either as a prophylactic or therapeutic measure.
The chemicals are applied by exposed root flare injection at the highest dosage allowed. Only elm trees in good condition (despite O. novo-ulmi infection) and with minor symptoms (5-15% symptoms in the crown) should be treated with fungicides (Scheffer et al., 1988; Stipes, 2000). Systemic fungicides move with the transpiration stream through infected sapwood that is still functional, stop the pathogenic action of the fungus, and allow the tree to wall off the infection with a layer of new sapwood. It is most important that the fungicide is completely distributed throughout the crown of the affected tree during the injection procedure. Symptomatic branches should be removed after successful application. Success rates of between 55 and 79% were obtained for thiabendazole and propiconazole (Stennes, 2000). If the infection has spread to the roots, no chemical treatment will be effective.
The application of fungicides has certain disadvantages. In low concentrations the chemicals will not kill the fungus but only inhibit it, thus the remission of symptoms may be expected. In addition, severe wounding at the injection site and phytotoxic effects on the leaves are commonly observed. The treatment must also be repeated at maximum intervals of 3 years. For economic reasons, chemical control is usually only applied to single trees of high value (Haugen, 1998).
Many cities in North America such as Minneapolis, USA (Stennes, 2000) and Winnipeg, Canada (Allen, 2000) have made DED control a priority and have invested in effective disease management programmes. A 15-year study by the United States Department of Agriculture concluded that control programmes cost 37-76% less than applying no control measures and having to remove killed trees and replant with new trees (Anon., 1977). An annual loss of 1-2% of the trees in a community is seen as successful management (Cannon et al., 1977). Communities that implement no control programme may lose 90% of their elms within only a decade. A successful example of disease management is the city of Fredericton, New Brunswick, Canada, which was able to save 70% of its elms after 30 years of Dutch elm disease in the area. In 1990 the annual loss in the city was only 0.5% (Magasi et al., 1993). In New Zealand O. novo-ulmi was successfully eradicated by the application of an integrated management approach (Gadgil et al., 2000).
Sanitation combined with the use of insecticides and root graft severance is reported to be the most effective approach to control (Anon., 1977). Sanitation is the most important component, as it is aimed at both the pathogen and the vector. For timely detection of disease symptoms, a primary inventory of the elm stands present should be conducted and subsequent systematic surveys should be carried out at least twice each year during the growing season (Stipes and Campana, 1981). Elm wood infested with bark beetles or trees which could provide sites for breeding should be removed promptly, within 2-3 weeks during the growing season or before April in the dormant season (Haugen, 1998). All firewood of elm has to be destroyed by early spring. Harvested elm wood has to be debarked and dried. Wood can be immersed in water for long-term storage (Stipes and Campana, 1981). Declined branches that may attract beetles must be pruned off. If the disease is localized in a single branch, eradicative pruning may be sufficient to halt disease development.
Pheromone trapping of the vectors can help to estimate population size and identify high-risk locations (Haugen, 1998; Gadgil et al., 2000). The use of trap logs has been successful in reducing the number of bark beetle vectors. Trap logs should be treated with an insecticide, or debarked and burned (or buried) before the beetles are ready to emerge (Stipes and Campana, 1981). The application of insecticides to the crown of the tree to kill the vectors is often not effective and not environmentally justifiable (Haugen, 1998). The treatment of the lower bole with an insecticide in late summer or early autumn is effective against overwintering adults of Hylurgopinus rufipes (Haugen, 1998). The severance of root grafts is another measure to contain the disease in urban plantations. Single trees of high value can also be treated with fungicides.
The replacement of susceptible elms with resistant cultivars is necessary to reduce the impact of the disease. Plantation of other species is also a common practice and should be carried out as it was elm monocultures that made the immense impact of Dutch elm disease in the urban environment possible in the first place. Elms are remarkably protected when growing in a diverse or heterogeneous community of other tree species (Stipes and Campana, 1981). The eradication of all elms from an area has sometimes been suggested, and should be considered under certain conditions (Haugen, 1998).
ReferencesTop of page
Allen MS, 2000. The control of Dutch elm disease in Winnipeg. Winnipeg, Canada: Forestry Branch.
Anon., 1977. Dutch elm disease: status of the disease, research and control. Washington DC, USA: USDA Forest service.
Anon., 1989. The Plants Fruits & Seeds (Regulation of Import into India) Order. Appendix 12.3, Schedule II. New Delhi, India: Ministry of Agriculture.
Anon., 1991. Law of the People's Republic of China on the Entry and Exit Animal and Plant Quarantine. Beijing, China: Order No. 53 of the President of the People's Republic of China.
Anon., 1995. Plant protection regulations. P-14.8/SOR-95-212. Ottawa, Canada: Ministry of Agriculture.
Anon., 1999. Summary of Plant Quarantine Pest and Disease Situations in Canada 1999. Ottawa, Canada: Canadian Food Inspection Agency.
Anon., 2000. Regulated plant pest list. Washington, DC, USA: United States Department of Agriculture Animal and Plant Health Inspection Service.
Anon., 2002. Biosecurity (Notifiable Organisms) Order 2002. SR 2002/92. Wellington, New Zealand: Ministry of Agriculture and Forestry.
Anon., 2002. Exterior quarantine against Dutch elm disease. Quarantine of Agricultural Commodities Chapter 554. Carson City, NV, USA: Nevada Administrative Code.
Anon., 2003. Dutch elm disease. Fact sheet 27. Canberra, Australia: Department of Agriculture Fisheries and Forestry.
Anon., 2003. Import requirements of non-manufactured wood and other non-propagative wood products, except solid wood packaging material, from areas other than the continental United States. D-02-12. Nepean, Ontario, Canada: Canadian Food Inspection Agency.
Bates MR; Buck KW; Brasier CM, 1993. Molecular relationships between Ophiostoma ulmi and the NAN and EAN races of O. novo-ulmi determined by restriction fragment length polymorphisms of nuclear DNA. Mycological Research, 97(4):449-455
Bates MR; Buck KW; Brasier CM, 1993. Molecular relationships of the mitochondrial DNA of Ophiostoma ulmi and the NAN and EAN races of O. novo-ulmi determined by restriction fragment length polymorphisms. Mycological Research, 97(9):1093-1100
Bowden CG; Smalley E; Guries RP; Hubbes M; Temple B; Horgen PA, 1996. Lack of association between cerato-ulmin production and virulence in Ophiostoma novo-ulmi. Molecular Plant-Microbe Interactions, 9(7):556-564; 43 ref.
Boyce JS, 1938. Forest Pathology. New York, USA: McGraw-Hill.
Brasier CM, 1981. Laboratory investigation of Ceratocystis ulmi. In: Stipes RJ, Campana, RJ eds. Compendium of elm diseases. St. Paul, MN, USA: The American Phytopathological Society, 76-79.
Brasier CM, 1984. Inter-mycelial recognition systems in Ceratocystis ulmi: their physiological properties and ecological importance. In: Jennings, DH, ed. The ecology and physiology of the fungal mycelium. Cambridge: Cambridge University Press, 451-497.
Brasier CM, 1986. The d-factor in Ceratocystis ulmi - its biological characteristics and implications for Dutch elm disease. In: Buck KW, ed. Fungal virology. Boca Raton, USA: CRC Press, 177-208.
Brasier CM, 1996. New Horizons in Dutch Elm Disease Control. Report on Forest Research 1996. London, U. K.: HMSO, Forestry Commission, 20-28.
Brasier CM, 2000. Intercontinental spread and continuing evolution of the Dutch elm research pathogens. Boston, USA: Kluwer Academic Publishers, 61-72.
Brasier CM, 2000. Viruses as biological control agents of the Dutch elm disease fungus Ophiostoma novo-ulmi. In: Dunn CP, ed. The elms - Breeding, Conservation and Disease management. Boston, USA: Kluwer Academic Publishers, 201-212.
Brasier CM; Kirk SA; Pipe ND; Buck KW, 1998. Rare interspecific hybrids in natural populations of the Dutch elm disease pathogens Ophiostoma ulmi and O. novo-ulmi. Mycological Research, 102(1):45-57; 57 ref.
Butin H, 1995. Tree diseases and disorders. Oxford, UK: Oxford University Press.
Collin E; Bilger I; Eriksson G; Turok J, 2000. The conservation of elm genetic resources in Europe. In: Dunn CP, ed. The elms - Breeding, Conservation and Disease management. Boston, USA: Kluwer Academic Publishers, 281-294.
Dewar K; Bousquet J; Dufour J; Bernier L, 1997. A meiotically reproducible chromosome length polymorphism in the ascomycete fungus Ophiostoma ulmi (sensu lato). Molecular and General Genetics, 255(1):38-44; 33 ref.
Duchesne LC, 1993. Mechanisms of Resistance: Can they help save susceptible elms? In: Sticklen MB, Sherald JL, eds. Dutch elm disease research - Cellular and Molecular Approaches. New York, USA: Springer, 239-254.
Elgersma DM; Roosien T; Scheffer, 1993. Biological control of Dutch elm disease by exploiting resistance in the host. Proceedings of the 2nd international symposium on Dutch elm disease, East Lansing, august 1992, pp. 188-192.
Et-Touil A; Brasier CM; Bernier L, 1999. Localization of a pathogenicity gene in Ophiostoma novo-ulmi and evidence that it may be introgressed from O. ulmi. Molecular Plant-Microbe Interactions, 12(1):6-15; 35 ref.
Faccoli M; Battisti A, 1997. Observations on the transmission of Ophiostoma ulmi by the Smaller Elm Bark Beetles (Scolytus spp.). Meeting IUFRO: Integrating Cultural Tactics Into The Management of Bark Beetles and Reforestation Pest. Vallombrosa (FI), 1-3 September 1996: 172-176.
FAO, 1997. International Plant Protection Convention. FAO Conference at its 29th Session. Rome, Italy: FAO.
Fransen JJ, 1939. Lepenziekte, iepenspintkevers en beider bestrijding. Wageningen, Netherlands: Veenman & Zonen, 1-118.
Gadgil PD; Bulman LS; Dick MA; Bain J, 2000. Dutch elm disease in New Zealand. In: Dunn CP, ed. The elms - Breeding, Conservation and Disease management. Boston, USA: Kluwer Academic Publishers, 189-200.
Gartland KMA; Gartland JS; Fenning TM; Mchugh AT; Irvine RJ; Main GD; Brasier CM, 2000. Genetic manipulations with elms. In: Dunn CP, ed. The elms - Breeding, Conservation and Disease Management. Boston, USA: Kluwer Academic Publishers, 259-270.
Gibbs JN, 1978. Intercontinental epidemiology of Dutch elm disease. Annual Review of Phytopathology 16: 287-307.
Gibbs JN, 2001. Management of the disease burden. In: Evans J, The Forests Handbook - Volume 2: Applying forest science for sustainable management. London, UK: Blackwell Science, 202-217.
Guries RP; Smalley EB, 2000. Once and future elms - classical and molecular approaches to Dutch elm disease resistance. In: Dunn CP, ed. The elms - Breeding, Conservation and Disease management. Boston, USA: Kluwer Academic Publishers, 231-248.
Hafstad GE, 1958. Possible long distance spread of Dutch elm disease by transported beetles. Plant Disease Reporter 42, 893-894.
Harwood TD; Tomlinson I; Potter CA; Knight JD, 2011. Dutch elm disease revisited: past, present and future management in Great Britain. Plant Pathology, 60(3):545-555. http://onlinelibrary.wiley.com/doi/10.1111/j.1365-3059.2010.02391.x/full
Haugen L, 1998. How to identify and manage Dutch elm disease. Publication NA-PR-07-98. St. Paul, MN, USA: USDA Forest Service.
Haugen L; Stennes M, 1999. Fungicide injection to control Dutch elm disease: understanding the options. Plant Diagnostics Quarterly 20: 29-38.
Heybroek H, 1993. The Dutch elm breeding program. In: Sticklen MB, Sherald JL, eds. Dutch elm disease research - Cellular and Molecular Approaches. New York, USA: Springer, 16-25.
Heybroek H, 1993. Why bother about the elm? In: Sticklen MB, Sherald JL, eds. Dutch elm disease research - Cellular and Molecular Approaches. New York, USA: Springer, 1-8.
Himelick EB; Ceplecha DW, 1976. Dutch elms disease eradication by pruning. Journal of Arboriculture 2: 81-84.
Hoegger PJ; Binz T; Heiniger U, 1996. Detection of genetic variation between Ophiostoma ulmi and the NAN and EAN races of O. novo-ulmi in Switzerland using RAPD markers. European Journal of Forest Pathology, 26(2):57-68; 32 ref.
Hubbes M, 1993. Mansonones, elicitors and virulence. In: Sticklen MB, Sherald JL, eds. Dutch elm disease research - Cellular and Molecular Approaches. New York, USA: Springer, 208-215.
Hubbes M, 2003. Induced resistance on elms. In: Second International Elm Conference Valsain, Segovia (Spain) May 20-23, 2003. Posters and Abstracts. Madrid, Spain: Ministerio de medio ambiente, 69.
Jeng RS; Bernier L; Brasier CM, 1988. A comparative study of cultural and electrophoretic characteristics of the Eurasian and North American races of Ophiostoma ulmi. Canadian Journal of Botany, 66(7):1325-1333
Jeng RS; Hintz WE; Bowden C, 1996. A comparison of the nucleotide sequence of the cerato-ulmin gene and the rDNA ITS between aggressive and non-aggressive isolates of Ophiostoma ulmi sensu lato, the causal agent of Dutch elm disease. Current Genetics 29: 168-173.
Klopping HL, 1960. Patent 2,933,502. Benzimidazole derivatives. United states patent office official gazette 753: 725.
Konrad H; Kirisits T; Riegler M; Halmschlager E; Stauffer C, 2002. Genetic evidence for natural hybridization between the Dutch elm disease pathogens Ophiostoma novo-ulmi ssp. novo-ulmi and O. novo-ulmi ssp. americana. Plant Pathology, 51(1):78-84; 39 ref.
Lea J; Brasier CM, 1983. A fruiting succession in Ceratocystis ulmi. Transactions of the British Mycological Society 80:381-387.
Magasi LP; Harrison KJ; Urquhart DA; Murray DM, 1993. Three decades of Dutch elm disease in Fredericton, NB. Information Report - Maritimes Region, Canadian Forest Service, No. M-X-185E:vi + 39 pp.; 18 ref.
Mayer H; Reimoser F, 1978. Die Auswirkungen des Ulmensterbens im Buchen-Naturwaldreservat Dobra (Niederösterreichisches Waldviertel). Forstwissenschaftliches Centralblatt 97, 314-321.
Mittempergher L, 2000. Elm yellows in Europe. In: Dunn CP, ed. The elms - Breeding, Conservation and Disease management. Boston, USA: Kluwer Academic Publishers, 103-120.
Munoz C; Ruperez A, 1980. La desaparacion de los olmos. Boletin de Servicio del Plagas, 6: 105-106.
Murdoch CW; Campana RJ; Hoch J, 1984. On the biological control of Ceratocystis ulmi with Pseudomonas fluorescens. Phytopathology 74:805-0.
Myers DF; Strobel GA, 1983. Pseudomonas syringae as a microbial antagonist of Ceratocystis ulmi in the apoplast of American elm. Transactions of the British Mycological Society 80:389-394.
Möller G, 1993. Ulmenerhaltung aus der Sicht des Naturschutzes - Probleme und Möglichkeiten. In: Kleinschmit J, Weisgerber, H, eds. "Ist die Ulme noch zu retten?". Berichtsband des 1. Ulmensymposiums in Hann. Münden am 21. und 22. Mai 1992, veranstaltet von den Abteilungen Forstpflanzenzüchtung der Niedersächsischen und der Hessischen Forstlichen Versuchsanstalt. Forschungsberichte der Hessischen Forstlichen Versuchsanstalt 16: 68-86.
OEPP/EPPO, 1999. EPPO summary of phytosanitary regulations. Paris, France: OEPP/ EPPO.
Pipe ND; Buck KW; Brasier CM, 1997. Comparison of the cerato-ulmin (cu) gene sequences of the Himalayan Dutch elm disease fungus Ophiostoma himal-ulmi with those of O. ulmi and O. novo-ulmi suggests that the cu gene of O. novo-ulmi is unlikely to have been acquired recently from O. himal-ulmi. Mycological Research, 101(4):415-421; 39 ref.
Richens RH, 1983. Elm. London, UK: Cambridge University Press.
Rogers HJ; Buck KW; Brasier CM, 1986. The molecular nature of the d-factor in Ceratocystis ulmi. In: Buck KW, ed. Fungal virology. Boca Raton, USA: CRC Press, 209-220.
Scala A; Pattuelli M; Coppola L; Guastini M; Tegli S; Sorbo Gdel; Mittempergher L; Scala F, 1997. Dutch elm disease progression and quantitative determination of cerato-ulmin in leaves, stems and branches of elms inoculated with Ophiostoma novo-ulmi and O. ulmi. Physiological and Molecular Plant Pathology, 50(5):349-360; 43 ref.
Scheffer RJ; Brakenhoff AC; Kerkenaar A; Elgersma DM, 1988. Control of Dutch elm disease by the sterol biosynthesis inhibitors fenpropimorph and fenpropidin. Netherlands Journal of Plant Pathology, 94(3):161-173
Scheffer RJ; Liem JI; Elgersma DM, 1987. Production in vitro of phytotoxic compounds by non-aggressive and aggressive isolates of Ophiostoma ulmi, the Dutch elm disease pathogen. Physiological and Molecular Plant Pathology, 30(3):321-335
Sherald JL, 1993. Demands and opportunities for selecting disease-resistant elms. In: Sticklen MB, Sherald JL, eds. Dutch elm disease research - Cellular and Molecular Approaches. New York, USA: Springer, 60-68.
Sinclair WA, 2000. Elm Yellows in North America. In: Dunn CP, ed. The elms - Breeding, Conservation and Disease management. Boston, USA: Kluwer Academic Publishers, 121-136.
Smalley EB; Guries RP, 2000. Asian elms: sources of disease and insect resistance. In: Dunn CP, ed. The elms - Breeding, Conservation and Disease management. Boston, USA: Kluwer Academic Publishers, 215-230.
Smalley EB; Guries RP; Lester DT, 1993. American Liberty elms and beyond: Going from the impossible to the difficult. In: Sticklen MB, Sherald J, eds. Dutch Elm Disease: Cellular and Molecular Approaches. New York, USA: Springer-Verlag, 26-45.
Smalley EB; Raffa KF; Proctor RH; Klepzig KD, 1993. Tree responses to infection by species of Ophiostoma and Ceratocystis In: Wingfield MJ, ed. Ophiostoma and Ceratocystis. St. Paul, MN, USA: The American Phytopathological Society, 207-218.
Sorbo Gdel; Scala F; Parrella G; Lorito M; Comparini C; Ruocco M; Scala A, 2000. Functional expression of the gene cu, encoding the phytotoxic hydrophobin cerato-ulmin, enables Ophiostoma quercus, a nonpathogen on elm, to cause symptoms of dutch elm disease. Molecular Plant-Microbe Interactions, 13(1):43-53; 42 ref.
Stennes MA, 2000. Dutch elm disease chemotherapy with Arbotect 20-S and Alamo In: Dunn CP, ed. The elms - Breeding, Conservation and Disease Management. Boston, USA: Kluwer Academic Publishers, 173-188.
Stipes RJ, 2000. The Management of Dutch elm disease. In: Dunn CP, ed. The elms - Breeding, Conservation and Disease Management. Boston, USA: Kluwer Academic Publishers, 157-172.
Stoyanov N, 2004. Elm forests in North Bulgaria and conservation strategies. Investigación Agraria, Sistemas y Recursos Forestales [New approaches to elm conservation. Second International Elm Conference, Valsaín, Spain, 20-23 May 2003.], 13(1):255-259.
Takai S, 1974. Pathogenicity and cerato-ulmin production in Ceratocystis ulmi. Nature 252: 124-126.
Takai S, 1980. Relationship of the production of the toxin, cerato-ulmin, to synnemata formation, pathogenicity, mycelial habit, and growth of Ceratocystis ulmi isolates. Canadian Journal of Botany, 58(6):658-662
Takai S; Hiratsuka Y, 1984. Scanning electron microscope observations of internal symptoms of white elm following Ceratocystis ulmi infection and cerato-ulmin treatment. Canadian Journal of Botany, 62(7):1365-1371
Temple B; Horgen PA; Bernier L; Hintz WE, 1997. Cerato-ulmin, a hydrophobin secreted by the causal agents of Dutch elm disease, is a parasitic fitness factor. Fungal Genetics and Biology, 22(1):39-53; 50 ref.
Townsend AD; Santamour FS Jr, 1993. Progress in the development of disease-resistant elms. In: Sticklen MB, Sherald JL, eds. Dutch elm disease research - Cellular and Molecular Approaches. New York, USA: Springer, 46-50.
Voeten J, 2003. Dutch Trig - A decade of successful biological control of Dutch elm disease in Europe and the USA. In: Second International Elm Conference Valsain, Segovia (Spain) May 20-23, 2003. Posters and Abstracts. Madrid, Spain: Ministerio de medio ambiente, 44.
Webber JF, 1981. A natural biological control of Dutch elm disease. Nature, 292:449-451.
Webber JF, 1990. Relative effectiveness of Scolytus scolytus, S. multistiatus and S. kirschi as vectors of Dutch elm disease. European Journal of Forest Pathology, 20:184-192.
Webber JF, 2000. Insect vector behaviour and the evolution of Dutch elm disease. In: Dunn CP, ed. The elms - Breeding, Conservation and Disease management. Boston, USA: Kluwer Academic Publishers, 47-60.
Webber JF; Brasier CM; Mitchell AG, 1987. The role of the saprophytic phase in Dutch elm disease. In: Pegg GF, Ayres PG, eds. Fungal infection of plants: symposium of the British Mycological Society. Cambridge, UK: Cambridge University Press, 298-313.
Webber JF; Gibbs JN, 1989. Insect dissemination of fungal pathogens of trees. Insect-fungus interactions. 14th Symposium of the Royal Entomological Society of London in collaboration with the British Mycological Society [edited by Wilding, N.; Collins, N.M.; Hammond, P.M.; Webber, J.F.] London, UK; Academic Press, 161-193
Zanta F; Battisti A, 1989. Notes on the distribution and biology of the elm bark beetles in north-eastern Italy (Coleoptera Scolytidae). Gortania - Atti del Museo Friulano di Storia Naturale, Udine, 11:189-205.
CABI, Undated. Compendium record. Wallingford, UK: CABI
CABI, Undated a. CABI Compendium: Status inferred from regional distribution. Wallingford, UK: CABI
CABI, Undated b. CABI Compendium: Status as determined by CABI editor. Wallingford, UK: CABI
Gadgil PD, Bulman LS, Dick MA, Bain J, 2000. Dutch elm disease in New Zealand. In: The elms - Breeding, Conservation and Disease management, [ed. by Dunn CP]. Boston, USA: Kluwer Academic Publishers. 189-200.
Hintz W E, Jeng R S, Yang D Q, Hubbes M M, Horgen P A, 1993. A genetic survey of the pathogenic fungus Ophiostoma ulmi across a Dutch elm disease front in western Canada. Genome. 36 (3), 418-426. DOI:10.1139/g93-057
Jacobi W R, Koski R D, Harrington T C, Witcosky J J, 2007. Association of Ophiostoma novo-ulmi with Scolytus schevyrewi (Scolytidae) in Colorado. Plant Disease. 91 (3), 245-247. DOI:10.1094/PDIS-91-3-0245
Masuya H, Brasier C, Ichihara Y, Kubono T, Kanzaki N, 2010. First report of the Dutch elm disease pathogens Ophiostoma ulmi and O. novo-ulmi in Japan. Plant Pathology. 59 (4), 805. DOI:10.1111/j.1365-3059.2009.02239.x
Matisone I, Kenigsvalde K, Zaluma A, Burnevica N, Šnepste I, Matisons R, Gaitnieks T, 2020. First report on the Dutch elm disease pathogen Ophiostoma novo-ulmi from Latvia. Forest Pathology. 50 (4), DOI:10.1111/efp.12601
Munoz C, Ruperez A, 1980. (La desaparacion de los olmos). In: Boletin de Servicio del Plagas, 6 105-106.
Rotger M G, Casado J R, 1996. Presence of the "Dutch elm disease" on Ibiza (the Balearic islands). (Detección de la grafiosis agresiva en la isla de Ibiza (Baleares).). Boletín de Sanidad Vegetal, Plagas. 22 (4), 789-801.
Distribution MapsTop of page
Select a dataset
CABI Summary Records
Unsupported Web Browser:
One or more of the features that are needed to show you the maps functionality are not available in the web browser that you are using.
Please consider upgrading your browser to the latest version or installing a new browser.
More information about modern web browsers can be found at http://browsehappy.com/