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Dutch Elm Disease (Ophiostoma ulmi)

Family: Ophiostomataceae Order: Ophiostomatales Class: Sordariomycetes Genus: Ophiostoma

This species has been nominated as among 100 of the "World's Worst" invaders

Evidence from pollen analysis in peat sediments suggests that there were major fluctuations in elm populations in prehistoric times, related primarily to climate change but also perhaps to disease caused by the fungus Ophiostoma ulmi, the cause of Dutch elm disease.

Dutch elm disease was first noticed in Europe in 1910, and spread slowly, reaching Britain in 1927. This first strain was a relatively mild one, which only killed a small proportion of elms, more often just killing scattered branches, and had largely died-out by 1940.

Ophiostoma ulmi was first discovered and was isolated in Holland in 1921 by Marie Beatrice Schwarz, a pioneering Dutch phytopathologist with six other women researchers, hence the name Dutch elm disease. It is a highly virulent fungal wilt disease caused by a pathogenic fungus disseminated by specialized bark beetles. Responsible for Dutch elm disease (DED), this fungus is also present in North America, and parts of Asia. Trees infected by beetles first show wilting, curling and yellowing of leaves on one or more branches in the upper portion of the tree and subsequent mortality to all three elm species (Ulmus spp.) native to Europe. Large trees may survive and show progressively more symptoms for one or more years. Frequently, by the time first symptoms are noted, the fungus has already reached scaffold branches or the main trunk of the tree. Once the fungus is established within a tree, it spreads rapidly via the water-conducting vessels. The tree reacts to the presence of the fungus by plugging its own cambial tissue in an attempt to block the fungus from spreading further. As the area around cambium (the vascular tissue) is crucial for delivering nutrients and water to the rest of the

Elm die back 0176077

: UK Forestry Commission Archives, www.forestryimages.org

plant, these plugs or tyloses prevent them from travelling up the trunk of the tree, eventually killing it. The first symptom of infection is usually an upper branch of the tree with leaves starting to wither and yellow in summer, months before the normal autumnal leaf shedding. This progressively spreads to the rest of the tree, with further dieback of branches. Eventually, the roots die, starved of nutrients from the leaves. Trees infected through root grafts wilt and die rapidly; this frequently occurs in the spring soon after the trees have leafed out and progresses from the base of the tree upward. Often, not all the roots die: the roots may put up small suckers. These may grow up for some years into small elm trees, but after a decade or so the new trunks become large enough to support the bark beetles, and with their inevitable arrival the fungus returns, and the new tree dies.

There have been two destructive pandemics of the disease in Europe during the last century, caused by the successive introduction of two fungal pathogens: Ophiostoma ulmi and Ophiostoma novo-ulmi, the latter much more aggressive.

Two subspecies have been described (Brasier & Kirk, 2001), the ssp. novo-ulmi and the ssp. americana, which are partially reproductively isolated, behaviourally distinct and exhibit morphological differences (Brasier & Kirk, 2001). They can be distinguished by a number of genetic markers (RAPD’s) (Hoegger et al., 1996).

 Elm tree range of foliar symptoms DED 0454016

: UK Forestry Commission Archives, www.forestryimages.org

O. ulmi is a rather complex fungus. It has four spore types: conidia produced on mycelium, conidia borne on a mycelial stalk (synnema), yeast like spores that are variable in size, and ascospores, which are produced in a black fruiting body (perithecium) which ooze through the long neck of the perithecium, and accumulate at the tip in sticky mass.

Three strains are now recognized, Ophiostoma ulmi, which afflicted Europe in 1910, reaching North America on imported timber in 1928, Ophiostoma himal-ulmi, a strain endemic to the western Himalaya, and Ophiostoma novo-ulmi, the extremely virulent strain that has devastated Europe's elms since the late 1960s. O. novo-ulmi is now considered to be a hybrid between O. ulmi and O. himal-ulmi. The new strain was widely believed to have originated in China, but a comprehensive survey there in 1986 found no trace of it, although elm bark beetles were very common.

The cellulolytic activity (exoglucanase, endoglucanase and β-glucosidase) of Ophiostoma ulmi (four isolates), O. novo-ulmi (19 isolates) and `fast-waxy' (five isolates) was determined in growth media containing carboxymethylcellulose (CMC) and cellulose powder. Differences in enzyme activities were observed among isolates, irrespective of the species and substrate used. Inoculation experiments on Ulmus minor with randomly selected isolates of O. ulmi (two isolates), O. novo-ulmi (five isolates) and `fast-waxy' (two isolates) were also performed. Disease was assessed as the percentage of leaves showing yellowing and browning. Ophiostoma novo-ulmi and `fast-waxy' isolates exhibited a great variability in their capacities to cause the disease. In the presence of CMC, a significant correlation between the activity of exoglucanase and β-glucosidase in vitro and virulence was found.

O. ulmi undergoes sexual and asexual reproduction and has three asexual phases: a yeast phase, a Sporothrix -like stage, and a Graphium stage.

scolytus Elm bark beetle 0176087

: UK Forestry Commission Archives, www.forestryimages.org

 Large Elm beetle feeding grooves in crotch of twig 0176086

: UK Forestry Commission Archives, www.forestryimages.org

 Feeding galleries 0176085

: UK Forestry Commission Archives, www.forestryimages.org

large elm beetle Hexapoda (including Insecta) > Coleoptera > Curculionidae Scolytus scolytus (Fabricius)

The disease is spread by two species of Scolytus beetles which act as vectors for infection, the efficiency of which is dependant on their body dimension. In Europe the main vector is the large European bark beetle Scolytus scolytus, and S. multistiatus, S. pygmaeus and S. kirschii are also active. These beetles breed under the bark of dying elm trees. The young adults fly from the infected pupal chambers to feed on twig crotches of healthy elm trees. As a consequence spores of the fungus carried on the bodies of these beetles are deposited in healthy plant tissue. O. ulmis can also spread via root grafts. When elms are growing near each other, the fungus may spread when their roots come in contact in the soil and graft together. If infected wood is to be used as firewood, it should first be debarked.

The first fungicide used for preventive treatment of Dutch elm disease was Lignasan BLP (carbendazim phosphate), which was introduced in the 1970s. This had to be injected into the base of the tree using specialized equipment, and was never especially effective. It is still sold under the name "Elm Fungicide". Arbotect (thiabendazole hypophosphite) became available some years later, and it has been proven effective. Arbotect must be injected every 2 to 3 years to provide ongoing control; the disease generally cannot be eradicated once a tree is infected.

 showing characteristic dark patches 0454017

: UK Forestry Commission Archives, www.forestryimages.org

Alamo (propiconazole) has become available more recently and shows some promise, though several university studies show it to be less effective than Arbotect treatments. Alamo is primarily recommended for treatment of Oak Wilt.

Treatment of diseased trees is costly and at best will prolong the life of the tree, perhaps by as many as five or ten years. It is usually only justified when a tree has unusual symbolic value or occupies a particularly important place in the landscape.

Dutch elm disease cannot be eliminated once it begins. A year-round community cleansing program is the key to slowing the spread of the disease. The most available control is removing infected trees and promptly destroying the wood. If infected wood is to be used as firewood, it should first be debarked. Trenching to disrupt root grafts is also recommended to protect healthy elm trees near diseased ones. In urban situations, insecticide spraying of high value trees has been effective in keeping bark beetles from attacking susceptible trees. In ornamental plantings, suggested control measures include planting trees further apart to prevent root grafts or choosing mixed tree species. The use of resistant selections for new plantations is strongly recommended.

Research to select resistant cultivars and varieties began in the Netherlands in 1928, and in the USA since the disease became endemic there. Initial efforts in the Netherlands involved crossing varieties of U .minor and U. glabra, but later included the Himalayan or Kashmir Elm U. wallichiana as a source of anti-fungal genes. Early efforts in the USA involved the hybridization of the Chinese Elm with the American Elm, and produced a resistant tree that lacked the beauty, traditional shape, and landscape value of the American Elm. Few were planted.

Three major groups of resistant cultivars are commercially available now; The Princeton Elm, a cultivar selected in 1922 by Princeton Nurseries for its landscape value. By happy coincidence, this cultivar was revealed to be highly resistant in inoculation studies carried out by USDA in the early 1990s, to Dutch elm disease. Because mature trees planted in the 1920s still remain, the properties of the mature plant are well known. The Liberty Elm, a set of five cultivars produced through selection over several generations starting in the 1970s. Marketed as a single variety, nurseries selling the "Liberty Elm" actually distribute the five cultivars at random. Two of the cultivars are covered by patents. The Valley Forge elm, and some related cultivars, have demonstrated resistance to Dutch elm disease approximately equal to that of the Princeton elm cultivar, in controlled USDA tests.

Even resistant cultivars can become infected, particularly if the tree is under stress from drought and other environmental conditions, and if the disease pressure is high. With the exception of the Princeton Elm, no trees have yet been grown to maturity. The oldest liberty elm was planted in about 1980, and the trees cannot be said to be mature until they have reached an age of sixty years.

In about 1967, a new, far more virulent strain arrived in Britain on a shipment of Rock Elm logs from North America, and this strain proved both highly contagious and lethal to all of the European native elms; more than 25 million trees died in the UK alone. By 1990-2000, very few mature elms were left in Britain or much of northern Europe. One of the most distinctive English countryside trees, the English Elm U. procera, is particularly susceptible. Thirty years after the epidemic, these magnificent trees, which often grew to over 45 m high, are long gone. The species still survives in hedgerows, as the roots are not killed and send up root sprouts ("suckers"). These suckers rarely reach more than 5 m tall before succumbing to a new attack of the fungus. However, established hedges kept low by clipping have remained apparently healthy throughout the nearly 40 years since the onset of the disease in the UK.

The largest concentration of mature elm trees remaining in Britain is found in Brighton, where 15,000 elms still stand (2005 figures). Their survival is due to a concerted effort by local authorities to identify and remove infected sections of trees as soon as they show signs of the disease to save the tree and prevent it spreading.

The Dutch research programme ended in 1992, after raising two complex hybrids, later released as Columella and (Lutèce ™), found to be actually immune to the disease when inoculated with unnaturally high doses of the fungus. In Italy, research is continuing at the Istituto per la Protezione delle Piante, Florence, to produce a wide range of disease-resistant trees using a variety of Asiatic species crossed with the early Dutch hybrid Plantyn as a safeguard against any future mutation of the disease. Two trees with very high levels of resistance, San Zanobi and Plinio, were released in 2003. Both feature the Siberian Elm U. pumila as the male parent.

The Red Elm U. rubra is less susceptible to Dutch elm disease than many elms, but this quality seems to have somehow largely evaded the attention of the resistance programme.

In 2001, English Elm was genetically engineered to resist disease in experiments at Abertay University, Dundee, by transferring anti-fungal genes into the elm genome using minute DNA-coated ball bearings. However, there are no plans to release the trees into the countryside.

Summary

Dutch elm disease is one of the most serious tree diseases in the world. It is caused by two related species of fungi in the genus Ophiostoma which are disseminated by various elm bark beetles.

This page provides information on the impact of the disease during the last five years.

Recent information on research on disease control can be found in Clive Brasier’s paper New Horizons in Dutch Elm Disease Control (PDF-3893K) published in ‘Report on Forest Research 1996’.

History of the disease

Dutch elm disease (DED) first appeared in north-west Europe around 1910, and much of the seminal work on its cause was carried out between 1919 and 1934 by several outstanding Dutch women scientists. UK Forestry Commission research on the disease began in the late 1920s when Dr Tom Peace began monitoring its rapid spread into Britain from its first recorded sites on the continent.

By the 1940s this first epidemic had died down after causing losses of 10—40% of elms in different European countries. Indeed Peace, in a thorough review, was able to write in 1960 "unless it completely changes its present trend of behaviour it will never bring about the disaster once considered imminent". Such a change did come, however, in the late 1960s with the beginning of a second and far more destructive outbreak of the disease.

Forestry Commission (FC) research showed that the new outbreak of DED was caused by an entirely different, far more aggressive DED fungus than that responsible for the epidemic of the 1920s—40s, and that the new fungus had been imported into Britain on infested elm logs. What followed was the catastrophic epidemic once feared by Peace:

Within a decade about 20 million elms out of an estimated UK elm population of 30 million were dead. By the 1990s the number was probably well over 25 million. Studies on the new DED fungus showed that it differed from the original fungus in almost all its important biological properties. The two pathogens were later described as separate species:

Ophiostoma ulmi being the original O. novo-ulmi the new highly aggressive pathogen. Central and southern Britain Our main native elms, English elm (U. procera), smooth-leaved elm (U. carpinifolia or U. minor) and wych elm (U. glabra) are all susceptible to O. novo-ulmi.

In lowland central and southern Britain, with predominantly English elm, the new epidemic took rapid hold during the early to mid-1970s, leading to the death of most mature English elm by the early 1980s. There were scattered escapes. Even pockets of mature elm survived occasionally, as in Brighton and Hove where the geographic situation has facilitated an effective and continuing sanitation control programme. However, once most suitable breeding material (inner elm bark) had been used by the beetles the disease virtually disappeared from many southern and south-western areas in the 1980s.

During this period suckers growing from surviving roots of English elm and some smooth-leaved elm types appeared in enormous numbers, together with occasional young seedlings of wych elm. Many small hedgerow elms that escaped the disease have been allowed to mature, in some cases through careful husbandry but often through absence of hedgerow maintenance. Consequently there developed a numerically massive and increasing elm resource, mainly of small to semi-mature U. procera, across much of southern Britain. From Essex to the Welsh borders they probably numbered many tens of millions.

In 1982 FC studies on the biology of O. novo-ulmi, on disease transmission and on the recent spread of the disease across eastern Europe (Romania to Poland) were combined to produce a prognosis for the future of the disease and of the elm. This suggested that the disease would not die down as had the first epidemic caused by O. ulmi, but instead, that the new DED pathogen O. novo-ulmi would return, in a continuing cycle, to attack the following generation of small elms once they were large enough to support beetle breeding. This is what is now happening in southern Britain.

In 20 elm plots established by the FC across the south of England, only about 1% of regenerating elms were killed annually between 1980 and 1990, but disease reappeared on a significant scale after 1991. Around the Research Station in the Farnham—Guildford area, no trace of the disease was found during 1981—1987, two separate infections were seen near Godalming in 1988, and by 1990 new infections were scattered across the whole area. By 1994—95 substantial tracts of hedgerow elms 3—12 m in height were dead or dying.

The above pattern has now occurred across most of the old 1970s U. procera disease-outbreak areas. In many areas c.50—90% of elms are dead or dying. Indeed the current disease situation is often remarkably reminiscent of the mid-1970s, except that the affected elms are much smaller. About 20 years separates this second wave of disease from the initial outbreak.

Three points should be noted:

The regenerating sucker elms are just as susceptible to O. novo-ulmi as were the parent trees from which they have developed.

The sudden resurgence of disease in the 1990s probably coincides with the return of the larger elm bark beetle, Scolytus scolytus, to the affected areas following its disappearance in the intervening period when little suitable breeding material was available. S. scolytus probably migrated back from neighbouring parts of Britain where it has survived. The smaller beetle, S. multistriatus, may actually be the first to return to an area, since it can use smaller diameter branches as its breeding material. However FC research shows that S. multistriatus is a very ineffective vector of the disease, in contrast to S. scolytus.

The best way to conserve hedgerow elms at present may be to keep them trimmed, since prominent elms are more likely to attract the bark beetles for feeding.

With these losses, DED remains by far our most destructive tree disease. However, although further cycles of disease can be expected, the elm will survive to provide a potential contribution to future landscapes.

Cornwall and East Anglia

In the early 1970s the rate of disease progress was markedly slower in the smooth-leaved elm populations of East Anglia and the Cornish elm (U. carpinifolia var. cornubiensis) populations of the south-west peninsula. The majority of mature Cornish elm and East Anglian smooth-leaved elms have now been killed by the disease.

However smooth-leaved elm is highly variable, and even now certain local East Anglian smooth-leaved elm clones have suffered only limited losses, with some isolated trees or significant groups of mature trees surviving. Many examples are in woodlands or on woodland edges. Some of these clones are being propagated by local authorities as possible sources of resistant material for replanting. They do not necessarily possess a higher level of resistance to the Dutch elm disease fungus: many factors can lead to reasonable 'field performance'.

All smooth-leaved elm varieties are believed to be introduced into Britain from central and southern Europe and some, being beyond their natural climatic range or site conditions, may be growing rather slowly and producing smaller springwood vessels restrictive to the fungus. Good field performance may also involve resistance to beetle feeding or breeding, or involve a natural biological control of the fungus or beetle. Some smooth-leaved elm types have very pendulous twigs when mature, a feature which could make them unattractive to the beetles for feeding.

Scotland and north-west England

Epidemic progress has also been much slower on the large predominantly wych elm (U. glabra) populations of Scotland and north-west England. The result is that the first wave of the 1970s epidemic is still active and continuing in these areas today.

At least three likely causes of this slower progression of disease are apparent:

U. glabra does not sucker like U. procera or U. carpinifolia, hence it suffers less from disease transmission via root grafts.

Although U. glabra is considered even more susceptible to O. novo-ulmi than is U. procera, it is much less favoured by the bark beetles for feeding.

A competitor of the elm bark beetles, the fungus Phomopsis, is a common, rapid invader of the bark of newly dying Wych elm, thereby acting as a competitor of the elm bark beetles which normally breed in the bark. Phomopsis appears to exert a strong natural biological control of the beetle populations of the north and west.

In addition climatic constraints probably reduce the disease activity of the pathogen by producing fewer opportunities for beetle originated infections in the summer. The climate may also restrict the size and number of annual bark beetle generations as compared with southem Britain or continental Europe. Such factors have aided a disease management campaign within the Edinburgh city limits.

Nonetheless, the disease is still active in Scotland. It has moved into U. glabra populations that were not affected by the first DED epidemic, such as those in the Glasgow area. It is continuing to push northwards, particularly on the east coast north of Aberdeen. This northwards expansion probably reflects the fact that O. novo-ulmi has a lower optimum temperature for growth than did O. ulmi, and the much greater epidemic momentum that O. novo-ulmi has generated, allowing Scolytus scolytus to expand beyond its previous northern territorial limits.

The disease is now well-established in an area around Nairn to the east of Inverness, with several hundred trees are known to be affected. It should be pointed out that this area has an appreciably higher average temperature than is common in this part of Scotland and that significant disease losses there do not mean that the whole region is equally vulnerable.

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