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
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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 The fungal pathogens causing Dutch elm disease are some of the best examples of the dramatic effect that the introduction of exotic fungal pathogens can have. It was international trade of timber and other products that made their intercontinental spread possible. After its introduction from an unknown origin, O. novo-ulmi met several widely distributed, highly susceptible host species in Europe, western Asia and North America and subsequently has killed uncounted millions of elm trees on the three continents (Brasier, 2000a). This probably makes it the most important pathogen of woody plants in the world. Its close association with bark beetles has made its spread over large areas and its integration into a fully functioning host-vector-pathogen system possible. The wide distribution, cultivation and management of the host population has greatly influenced the way the DED epidemics have developed. If man had not planted elm trees so extensively, there would not have been the large areas of genetically identical host material when O. novo-ulmi attacked the elm in the urban environment. The close spacing in the plantations has also made spread of the disease via root grafts so effective (Gibbs, 1978). Man has helped to quicken the spread by transporting infested timber and firewood over large distances and/or obstacles like mountain ranges. Its high virulence and, probably even more, its ability to colonize elm phloem (bark) very effectively, have helped O. novo-ulmi to very quickly replace any other fungal species that had been a colonizer of elm bark, including its close relative O. ulmi. Considering the recent development of the pandemics, no decrease in disease incidence can be expected. O. novo-ulmi has today become fully established in most parts of Europe, North America and western Asia and its eradication is no longer an option in these areas. The introduction of the Dutch elm disease fungi had occurred when the possible impact of such a disease had not been anticipated. The recent introduction of the pathogen to New Zealand and its successful eradication there (Gadgil et al., 2000) have shown how effective these measures can be, if implemented before the pathogen can become established.
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 Ophiostoma novo-ulmi is the causal organism of the current Dutch elm disease (DED) pandemics. Two other Dutch elm disease fungi are known: Ophiostoma ulmi and the Asian Ophiostoma himal-ulmi. Before O. novo-ulmi was recognized at species rank (Brasier, 1991) it was called the aggressive strain or subgroup of O. ulmi, or the aggressive form of Ceratocystis ulmi before re-classification of the genus (de Hoog and Scheffer, 1984). Two taxonomic entities have been identified within O. novo-ulmi by Brasier (1979): the EAN (Eurasian) and NAN (North American) races of O. novo-ulmi (or the EAN and NAN races of the aggressive subgroup of O. ulmi before the description of O. novo-ulmi) (Brasier, 1986a). These races have recently been designated as subspecies (Brasier and Kirk, 2001). The EAN race has been renamed subsp. novo-ulmi and the NAN race should now be referred to as subsp. americana. The two subspecies show different geographic distributions and many morphological, ecological and genetic differences (Brasier and Kirk, 2001).
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 Colonies of O. novo-ulmi are greyish- to cream-white when grown on Oxoid malt extract agar (MEA) at 20°C for 7 days in darkness followed by 10 days in diffuse daylight. The colony form ranges from regular striate petaloid to irregular lobed. The colonies commonly show moderate aerial mycelium, aggregated into ropes to give a fibrous, striate appearance. Occasionally, colonies are observed with less aerial mycelium and frosty to smooth mycelium ('uniform powdery' form, only in subsp. novo-ulmi; Brasier and Kirk, 2001). Diurnal zonation of the colonies is moderate to strong. Growth on MEA at 20°C in the dark ranges from 3.1 to 4.8 mm per day, the growth optimum is around 20-22°C, and the maximum temperature is 32-33°C. This feature is important for distinguishing O. novo-ulmi from O. ulmi.
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 O. novo-ulmi is currently causing the pandemics of Dutch elm disease in Europe, North America and western Asia. It has also recently reached the southern hemisphere by spreading to New Zealand (Gadgil et al., 2000). At present, O. novo-ulmi has replaced O. ulmi in most parts of its range, and only in some areas do they still co-exist (Brasier, 1991, 2001). Often no distinction has been made between O. ulmi and O. novo-ulmi, or between non-aggressive and aggressive subgroups, especially in North America, where there has been no decrease of disease incidence since the 1930s. For this reason, the current distribution of O. novo-ulmi in North America is not fully known, but this species is considered to be the causal agent of the current epidemics throughout the USA and Canada (Brasier, 1991; Haugen, 1998).
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.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Armenia||Present||Introduced||Invasive||Brasier, 1991; Brasier and Kirk, 2001|
|Georgia (Republic of)||Present||Introduced||Invasive||Brasier, 1991; Brasier and Kirk, 2001|
|Iran||Present||Introduced||1974||Invasive||Brasier and Afsharpour, 1979|
|Kazakhstan||Present||Introduced||Invasive||Brasier and Kirk, 2001|
|Canada||Present||Present based on regional distribution.|
|-Alberta||Present, few occurrences||Introduced||1998||Invasive||Anon., 1999|
|-Manitoba||Restricted distribution||Introduced||Invasive||Hintz et al., 1993|
|-New Brunswick||Widespread||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-Nova Scotia||Restricted distribution||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-Ontario||Widespread||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-Prince Edward Island||Restricted distribution||Introduced||Invasive||Brasier and Kirk, 2001|
|-Quebec||Widespread||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|USA||Present||Present based on regional distribution.|
|-California||Restricted distribution||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-Connecticut||Widespread||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-Illinois||Widespread||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-Iowa||Widespread||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-Kansas||Widespread||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-Maine||Widespread||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-Maryland||Widespread||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-Minnesota||Widespread||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-New Hampshire||Widespread||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-New York||Widespread||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-Ohio||Widespread||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-Oregon||Restricted distribution||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-Vermont||Widespread||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-Virginia||Widespread||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|-Wisconsin||Widespread||Introduced||Invasive||Brasier, 1996a; Brasier and Kirk, 2001|
|Albania||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Austria||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Belgium||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Bosnia-Hercegovina||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Bulgaria||Widespread||Introduced||Invasive||Brasier and Kirk, 2001; Stoyanov, 2004|
|Bulgaria||Present||Brasier and Kirk, 2001; Stoyanov, 2004|
|Croatia||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Czech Republic||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Czechoslovakia (former)||Present||Introduced||Invasive||Brasier and Kirk, 2001|
|Denmark||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Greece||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Hungary||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Ireland||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Macedonia||Widespread||1973||Invasive||Brasier and Kirk, 2001|
|Moldova||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Norway||Restricted distribution||Introduced||Invasive||Brasier and Kirk, 2001|
|Poland||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Portugal||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Romania||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Russian Federation||Present||Present based on regional distribution.|
|-Siberia||Present||Kondakov SYu, 2002|
|-Southern Russia||Widespread||Introduced||1968||Invasive||Gibbs, 1978|
|San Marino||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Serbia||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Slovakia||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Slovenia||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Spain||Widespread||Introduced||1980||Invasive||Munoz and Ruperez, 1980|
|-Balearic Islands||Present||Introduced||Invasive||Rotger and Casado, 1996|
|Sweden||Restricted distribution||Introduced||Invasive||Brasier and Kirk, 2001|
|-England and Wales||Present||Parker, 2003|
|Ukraine||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|Yugoslavia (former)||Widespread||Introduced||Invasive||Brasier and Kirk, 2001|
|New Zealand||Restricted distribution||Introduced||1989||Invasive||Gadgil et al., 2000|
History of Introduction and SpreadTop of page Because O. novo-ulmi appeared when O. ulmi was still very active in some areas, especially in North America, the introduction event(s) were not immediately recognized. Today it is believed that the second pandemic of Dutch elm disease, caused by O. novo-ulmi, probably began, more or less simultaneously, in the 1940s at two different locations: the Moldova-Ukraine area of Eastern Europe (subsp. novo-ulmi) and the southern Great Lakes area of North America (subsp. americana) (Brasier, 1990). Subsp. novo-ulmi steadily moved westwards across Europe, reaching the Netherlands by the mid-1970s. It also spread eastwards into south-west and central Asia, the latter almost certainly through a separate introduction during the 1970s and 1980s. At the same time subsp. americana spread across the North American continent, reaching both the east and west coasts by the 1970s and 1980s (Brasier, 1990; Brasier and Mehrotra, 1995). In the early 1970s subsp. americana had been accidentally introduced from the Windsor area (Canada) into the UK with a shipment of Ulmus thomasii logs and started the second pandemic there (Gibbs and Brasier, 1973; Brasier, 1979, 1990). Subsequently subsp. americana spread into the Netherlands, France, Spain and most other western and central European countries. As a result of this development in central and other parts of Europe, the ranges of the two subspecies overlap and hybrids between them have been identified (Jeng et al., 1988; Konrad et al., 2002). O. novo-ulmi is currently extending its range into western Canada and the eastern states of the USA as well as into Central Asia (Brasier and Kirk, 2001). The most recent event in the spread of O. novo-ulmi was the introduction of O. novo-ulmi to New Zealand in 1989 (Gadgil et al., 2000).
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 Most of the distribution range of elms today is affected by Dutch elm disease in Europe, western and central Asia and North America. O. novo-ulmi is not yet established in Alberta, Canada, and not present in some states of the USA and some counties of California. These areas have quarantine regulations to prevent introduction of the pathogen (Anon., 1995, 2002b). All countries with native or introduced elm populations not already affected by the disease are in danger of becoming infested with O. novo-ulmi in the future. This is emphasised by the recent introduction of the pathogen to New Zealand (Gadgil et al., 2000). The introduction of O. novo-ulmi into eastern Asia is a serious threat, because at least some of the elm species there have been reported to be susceptible and none is immune (Gibbs, 1978; Brasier, 1990).
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 While O. ulmi affects mostly ornamental elms in urban areas, O. novo-ulmi also affects elm trees growing in the forest. In one well-studied example from Austria, all mature elm trees growing in the virgin forest reserve of Dobra in lower Austria survived a pandemic caused by O. ulmi unharmed, but were killed within a few years by O. novo-ulmi (Mayer and Reimoser, 1978). This demonstrates the far more devastating effect of O. novo-ulmi on wild elm populations and on the ecosystem as a whole. As more mature elms have been killed, smaller trees and saplings are increasingly affected by the disease in both Europe and North America (Brasier, 1996b; Houston, 1991).
Hosts/Species AffectedTop of page Natural infections by O. novo-ulmi have only been found in elms (Ulmus spp.) and in Zelkova carpinifolia. Both hosts belong to the Ulmaceae (Sinclair and Campana, 1978). All three European elm species are severely affected by O. novo-ulmi and show very limited or no resistance. Ulmus laevis is affected to a lesser extent in Europe, which has been attributed to its avoidance by the vectors of O. novo-ulmi rather than its resistance against the fungus (Zanta and Battisti, 1989). Of the six American elm species, Ulmus americana, U. thomasii, U. alata, U. serotina and U. rubra have been reported to be highly susceptible, whereas U. crassifolia shows some resistance. No data are available for Ulmus mexicana (Sinclair and Campana, 1978). The two Asian elm species Ulmus parvifolia and U. pumila show high levels of resistance and have been used in breeding programmes. The latter species also has been planted extensively to replace endemic elm species in North America and Europe. However, some provenances of U. pumila from eastern Asia (east-central China) have shown to be extremely susceptible to the disease (Smalley and Guries, 2000). Asian elm species that show high levels of resistance include Ulmus davidiana, U. szechuanica, U. gaussenii, U. bergmanniana and U. castaneifolia; these are promising candidates for breeding (Smalley and Guries, 2000). Although Zelkova carpinifolia has been reported to be highly susceptible, Z. serrata is resistant (Sinclair and Campana, 1978). Inoculation studies have been carried out with other members of the Ulmaceae and Celtidaceae. Species of Celtis always proved to be resistant, whereas Planera aquatica was susceptible. Trema spp., Holoptelea integrifolia and Hemiptelea davidii were resistant (Sinclair and Campana, 1978; Smalley and Guries, 2000).
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 Vegetative growing stage
SymptomsTop of page The symptoms of infection by O. novo-ulmi are that of a typical vascular wilt disease. The first external symptoms on an elm tree are discoloration or drooping of the leaves at the tip of a branch. Subsequently, the leaves yellow, curl, turn brown, and finally fall off the tree soon after they have died. Alternatively, leaves can dry out rapidly, turn a dull green before dying, and remain attached to the twigs for several weeks. The shoot tip may wither and droop. A branch carrying only a few wilted leaves at the tip is called a 'flag'. Small flags develop when Scolytus bark beetles feed on the twig crotches of elms. Hylurgopinus rufipes causes the formation of large elm flags, because it feeds on the branches. This is important in control programmes as the small flags caused by the Scolytus feeding are easily missed during surveys (Sinclair and Campana, 1978). Characteristic diagnostic symptoms for DED are commonly seen in the xylem of affected twigs and branches. Browning of the water-conducting vessels of the whole outer growth ring can be seen on cross-section, also brown streaking in the direction of the grain on the twig, after removal of the bark. However, symptoms may vary and trees with extensive wilting may not show any discoloration and vice versa (Sutherland et al., 1997). The discoloration is caused by tylosis formation by the elm as a reaction to the fungal infection (Duchesne, 1993).
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 Genetics
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 Mites that live in the galleries of bark beetles can be considered as natural enemies of O. novo-ulmi as they eat a large amount of its mycelium and spores. However, these mites also play an important role in the dissemination of different O. novo-ulmi genotypes within the breeding galleries of the bark beetles and thus faciliate the sexual sporulation of O. novo-ulmi. Their effect on O. novo-ulmi therefore appears to be more beneficial than detrimental (Brasier, 1978).
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 Natural Dispersal
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 The introduction of O. novo-ulmi to North America, Europe and parts of Asia has resulted in a catastrophic pandemic in which most mature elms have died. Numbers are difficult to obtain, but in some areas of Europe 60-70% of the elm trees were killed (Tainter and Baker, 1996), with some 30 million elms killed in the UK (Brasier, 1996b). In North America the destructive impact of O. novo-ulmi has been even greater, with 46 million trees of urban Ulmus americana killed alone (Wallner, 1996). Losses caused by the two Dutch elm disease pandemics have been estimated to be over hundreds of millions of elms (Brasier, 2001). Although the disease does not reduce the value of the timber, a significant economic damage is caused. Leaving aside the aesthetic value of the trees in urban environments, the removal of diseased trees, replanting and disease management costs have been enormous. For example, the city of Winnipeg, Canada, spent Can $2,000,000 for Dutch elm disease management of its 200,000 elm trees in 2000 (Allen, 2000). The total economic loss caused by O. novo-ulmi is difficult to quantify because of the unequalled devastating impact of the pathogen on elm populations on three continents, but may go into hundreds of billions of US dollars (Heybroek, 1993b).
Environmental ImpactTop of page The environmental impact of O. novo-ulmi is even greater than that of its predecessor O. ulmi and can only be compared to that of Chestnut blight (Cryphonectria parasitica) in North America (Tainter and Baker, 1996). O. novo-ulmi has strongly affected elms in the forest and has changed the species composition of several forest communities, for example, floodplain forests in Europe. Although elm coppice is still relatively common in these forests, because elms are prolific seed producers, they have largely vanished from the canopy and other species have taken over their niche in the ecosystem (Hall et al., 1996). Before the introduction of DED fungi, wild elm populations had already suffered from human influences such as lowering of the groundwater table, intensification of harvesting operations, and habitat destruction, but the two pandemics of DED have resulted in a dangerous loss in genetic diversity within the genus. A European project, in which nine countries are working together, was initiated to save this diversity (Collin et al., 2000).
Impact: BiodiversityTop of page The disappearance of mature and old elm trees caused by Dutch elm disease has certainly had a negative effect on biodiversity; however, few data are available in this respect. Möller (1993) names 79 species of insects specialised on elm. In the Netherlands some rare epiphytes such as liverworts and mosses are only found on the bark of large elm trees. In the UK alone 161 species of lichens associated with elm have been described (Richens, 1983). In consequence it can be assumed that at least some of these species are in danger of extinction after more than 80 years of Dutch elm disease.
Social ImpactTop of page There is no other disease of trees that has become so well known to the public as Dutch elm disease. Elms were once a premier kind of tree planted in urban landscapes in Europe but were, and are, even more common in cities throughout the north-east and mid-western USA. In particular, the American elm (Ulmus americana) had been extensively planted there and, with its vase-shape, gave the streets and boulevards a distinct appearance. Dutch elm disease has had an enormous social impact and huge efforts are being made in many cities to save their elms, fully supported by the public. Large urban elm populations have been preserved in this way in many American cities (e.g. Minneapolis; Stennes, 2000). Elms are very prominent in the capital, Washington DC, and form an important part of the parklands at the Monumental Core and along the National Mall, where they provide a unique American cultural statement (Sherald, 1993). The US national park service is implementing an elaborate management plan to protect this important plantation.
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 The best medium for the isolation of O. novo-ulmi from field samples is malt extract agar (MEA) supplemented with streptomycin sulphate and cycloheximide (Brasier, 1981). Chips of infected wood, which have been surface sterilized, are placed on the selective medium and the fungus will start to grow on it within a few days. Alternatively, bark beetle frass of spore masses can be taken from bark beetle galleries and placed onto the agar. The formation of synnemata (Pesotum) may be observed after 1 week. Synnemata are usually only formed on elm wood or media containing elm wood such as elm sapwood agar (Brasier, 1981). Differentiation of O. novo-ulmi from the similar O. ulmi relies on a growth test and the evaluation of colony morphology. Petri dishes containing Oxoid MEA are inoculated with the isolate and incubated in the dark at 20°C for 48 hours. The diameters of two colonies are measured at right angles from the reverse of each plate. The plates are then incubated for a further 5 days before being measured again. The mean growth per day is then calculated. O. novo-ulmi will grow at a rate of 3.1-4.8 mm/day, whereas O. ulmi only grows at 2.0-3.1 mm/day. The plates are kept for further 10 days in diffuse light at room temperature before evaluation of the culture morphology. Oxoid MEA must be used for the examination of the morphology as it brings out very clearly the distinct characteristics of both species. A further growth test at 33°C must be conducted. Although O. ulmi will grow at 33°C with a growth rate of 1.1-2.8 mm/day, O. novo-ulmi will only grow at 0-0.5 mm/day (Brasier, 1981, 1991).
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 The detection of Dutch elm disease symptoms on an elm tree is usually not difficult because the wilting of the branches is very conspicuous. However, early symptoms are often difficult to detect in large trees. Examination of the xylem of an affected branch often reveals a brown discoloration of the outer year ring on a transversal cut. When a twig or stem is stripped of its bark, brown streaking can be seen in the outer xylem. Laboratory isolation of the pathogen is required to rule out infection by other pathogens.
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 The symptoms produced by O. novo-ulmi can be confused with those caused by other diseases and with damage caused by abiotic stresses. O. novo-ulmi infection can most easily be mistaken for O. ulmi infection, but disease caused by O. novo-ulmi usually progresses much faster than that caused by O. ulmi. For certainty, it is essential to isolate the fungus from its host and carry out laboratory investigations to distinguish between the two species (Brasier, 1981).
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 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.
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