Dutch elm disease

Dutch elm disease (DED) is the most devastating disease for elms all over the world (Brasier 1991; Brasier and Webber 2019). Elms have experienced two pandemics – the first at the beginning of the 20th century when 10-40% of elms were killed (Peace 1960; Gibbs 1978; Brasier 1996a; Brasier 2000) and the second since the second half of the 20th century (Brasier and Buck 2001) when also billions of elms were killed (Phillips and Burdekin 1992; Herald 2019). By the beginning of the 21st century (Brasier and Buck 2001; Kirisits 2013) approximately 80-90% (28 million) of mature elms had died in the UK, as well as hundreds of millions in North America (Brasier 2001; Brasier and Buck 2001).

DED agent is known to kill trees rapidly, even during one or two seasons (Phillips and Burdekin 1992, Schmidt 2006). Mortality by DED varies according to the host (Ulmus) species and depends on the susceptibility and genetic variety (Martín et al. 2019), the stand density and possible rootgrafts (Santini and Faccoli 2013), as well as on the seasonality of the infection and stress factors like drought (Kirisits 2013); also, mortality is influenced by the pathogen´s spore concentration inside the tree (Flower et al. 2017).

Phylum - Ascomycota

Class - Sordariomycetes

Family - Ophiostomataceae

 Genus - Ophiostoma

Three species are now recognized:

• The first agent of DED Ophiostoma ulmi (Buisman) Melin & Nannf. (previous synonyms Graphium ulmi M.B. Schwartz, Ceratostomella ulmi Buisman, Ceratocystis ulmi (Buisman) C. Moreau, Pesotum ulmi (M.B. Schwartz) J.L. Crane and Schokn) (Lepik 1940a; Brasier and Buck 2001).
• Ophiostoma himal-ulmi, a species endemic to the western Himalaya (Mehrotra 1995).
• Ophiostoma novo-ulmi, a virulent species the causal agent of second pandemic. It has two different subspecies – O. novo-ulmi subsp. novo-ulmi and O. novo-ulmi subsp. americana (Brasier and Kirk 2001, Brasier et al. 2004). Also, their hybrids were discovered and introduced thereafter (Konrad et al. 2002, Brasier and Kirk 2010). Because subspecies of O. novo-ulmi overlap in Europe (Martín, Fuentes-Utrilla et al. 2010) and gene flow between them lacks strong barriers (Brasier and Buck 2001), they are hybridizing freely (Santini et al. 2005, Tziros et al. 2017).

The disease affects species in the genera Ulmus and Zelkova.

European elms: Ulmus glabra Huds., U. minor Mill. U. laevis Pallas

Among European species, there is the unique example of the European white elm U. laevis, which has little innate resistance to DED, but is eschewed by the vector bark beetles and only rarely becomes infected. Recent research has indicated it is the presence of certain organic compounds, such as triterpenes and sterols, which serves to make the tree bark unattractive to the beetle species that spread the disease (Newhouse 2007). Another reason maybe the narrower vessels, that makes the species less vulnerable (Venturas et al. (2013). Recent research in Sweden has established that early-flushing clones are less susceptible to DED owing to an asynchrony between DED susceptibility and infection (Ghelardini 2007).

There is a wide range of elm hybrid varieties, usually crossed with Asian elms (Martín et al. 2014), some of them are generally resistant to DED (Eisele 2018) and are recommended to be planted in green areas.

It is important to know that that in Northern Europe elms grow in the northern limit of their natural range (Laasimer 1965, Ignatieva et al. 2011) resulting in an increase in their sensitivity to climate change and in their susceptibility to pathogens (Hanso and Drenkhan 2007, 2013).

DED is a lethal vascular wilt, being tracheomycosis-type disease (Brasier 2001), that reproduces by budding, similar to yeast-like fungi and the spores spread rapidly in xylem with sap flow (Webber and Brasier 1984). In response to the fungal infection tyloses and resins are accumulated in xylem vessels that eventually block water transportation to the crown causing the tree to wilt and finally death (Sherif et al. 2014).

The first symptoms of which are yellowing and browning (flagging) of leaves, a cross-section of an elm twig showing brown spots or streaks in the recent wood rings (Clinton and McCormick 1936; Stipes and Campana 1981). 

Flagging leaves of dying elm

The elm (Ulmus spp.) has been under attack, mostly on the Northern Hemisphere (Brasier and Buck 2001) for more than a century (Santini and Faccoli 2013; Smith and Hulcr 2015; Wingfield et al. 2016; Martín et al. 2019) due to Dutch elm disease (DED).

Dutch elm disease was first noticed in continental Europe in 1910 and spread slowly and eventually extended to all other countries except Greece and Finland (Clouston and Stansfield 1979). Barendina Gerarda Spierenburg (1921) compiled records of trees displaying symptoms from 1900 - 1905 onwards in the Netherlands and her publication of this information in 1921 was one part of the start of extensive research and practical measures to try to halt the disease. In addition the fungus that caused the disease was isolated in 1921 in The Netherlands by Bea Schwarz, a pioneering Dutch phytopathologist, and this discovery would lend the disease its name (Holmes and Heybroek 1990). Following this, in the 1920s and 30s Christine Buisman, working in the Netherlands and USA, identified the sexual stage of the fungal pathogen and also developed methods for experimental infections of elm seedlings that led to selection of resistant trees (Clinton and McCormick 1936, Heybroek and Nijboer 2013).

The geographical origin of first agent of DED Ophiostoma ulmi is unclear.

Elms have experienced two pandemics of DED – the first at the beginning of the 20th century when 10-40% of elms were killed (Peace 1960, Gibbs 1978, Brasier 1996, Brasier 2000) and the second since the second half of the 20th century (Brasier and Buck 2001) when also billions of elms were killed (Phillips and Burdekin 1992, Herald 2019).

By the beginning of the 21st century (Brasier and Buck 2001, Kirisits 2013) approximately 80-90% (28 million) of mature elms had died in the UK (Brasier 2001, Brasier and Buck 2001).

First, Ophiostoma ulmi killed elms in most of the European countries (Peace 1960). The northernmost findings of O. ulmi are known in Norway (Solheim et al. 2011), in Sweden (Menkis et al. 2016b; ‘EPPO Global Database’ 2019), Finland (Hintikka 1974), Estonia (Lepik 1940). But then the pathogen spread declined, apparently due to fungal viruses (Mitchell and Brasier 1994).

Thereafter, step by step, O. ulmi was replaced by a more aggressive new pathogen Ophiostoma novo-ulmi (Brasier and Buck 2001) causing the second pandemic.

The second pandemic of DED, the current one, had begun already in the 1940s at two different locations: the Moldova–Ukraine region in Eastern Europe and the Southern Great Lakes area in North America (Brasier 1990, 1996b). In Estonia the spread and some outbreaks of DED had been observed for the first time in the last decades of the last century. At that time the disease was considered insignificant. The outbreaks of DED have been increasing since the second decade of the new century.

There is no evidence that DED is still present in Finland (Hantula 2021).

The geographical ranges of the two O. novo-ulmi subspecies are overlapped in several parts of Europe (Brasier and Buck 2001) which also has induced their hybridisation (Konrad et al. 2002; Santini et al. 2005b; Martín et al. 2010), because the gene flow between them lacks strong barriers (Brasier and Buck 2001).

Reports on hybrid fungi were quite rare until the 1990s (Brasier 1995; Brasier and Buck 2001). In the eastern part of Europe, hybrids between the two subspecies of pathogen had already been detected in Hungary (Brasier et al. 2004), Poland (Brasier and Kirk 2010), the Czech Republic (Dvořák et al. 2007), Lithuania (Motiejūnaitė et al. 2016) and Latvia (Matisone et al. 2020), Estonia (Jürisoo 2021a) and Sankt Petersburg (Jürisoo 2021b).

DED was first reported in the United States in 1928, with the beetles believed to have arrived in a shipment of logs from the Netherlands. By the beginning of the 21st century hundreds of millions in North America (Brasier 2001, Brasier and Buck 2001).

Dutch elm disease has reached New Zealand. It was found in Napier where it was eradicated and was also found in the Auckland Region in 1989 (Ganley 2016).

Long range

It is regional or global trade that increases the risk of invasion of new pests (Brasier 2008; Hemery et al. 2010) and pathogens (Rytkönen et al. 2008, 2011; Santini et al. 2013; Müller et al. 2016; Ghelardini et al. 2017; Liebhold et al. 2017). It is possible that the threat to Ulmus spp. has risen due to the transportation of infected elm seedlings, plants or timber, similarly to what has happened in Sweden, Norway, the UK and the USA (La Porta et al. 2008; Brasier and Kirk 2010; Solheim et al. 2011; Menkis et al. 2016b).

Climate change, also unusual fluctuation of temperatures and heavy rains (Roloff et al. 2009) have an impact on trees making them more susceptible to pests and diseases (Hanso and Drenkhan 2013; Bentz and Jönsson 2015; Ramsfield et al. 2016) in forest ecosystems, as well as in urban areas (Sturrock 2012).

Short range

Bark beetles are essential agents in spreading of DED pathogens (Coleoptera: Curculionidae, Scolytinae); however, if they are not in association with fungal pathogens (Wingfield et al. 2016), they are minor pests. Scolytid species are distributed worldwide (Heliövaara and Peltonen 1999), the number of the species is increasing from north to south (Nikulina et al. 2015) depending on suitable tree species (Heliövaara and Peltonen 1999).

DED is spread in North America by three species of bark beetles:

·  The native elm bark beetle, Hylurgopinus rufipes (Jacobi et. al 2013, Webber 2000).

·  The smaller European elm bark beetle, Scolytus multistriatus (Jacobi et. al 2013).

·  The banded elm bark beetle, Scolytus schevyrewi (Jacobi et. al 2013).

In Europe:

·  The smaller European elm bark beetle, S. multistriatus (Webber 2000)

·   Large elm bark beetle, S. scolytus. (Webber 1990, Waller 2013)

·   Other reported DED vectors include Scolytus sulcifrons, S. pygmaeus, S. laevis, Pteleobius vittatus and Р. kraatzi, S. triarmatus, Xyleborinus saxesenii and Xyleborus dispar ((Anderbrant and Schlyter 1987a, Ижевский 2005, Santini and Faccoli 2013, Webber 1990, 2004, Menkis et al. 2016a, Jürisoo et al. 2021b, Jürisoo et al.  2021c).  

It has been argued that Northern Europe is protected from DED because bark beetles do not occur there (Caulton et al. 1998, La Porta et al. 2008, Santini and Faccoli 2013, Martín et al. 2019); however, warmer climate has probably extended the northern range of Scolytus spp., as recorded in Northwest Russia (Selikhovkin et al. 2020).

The life cycle of bark beetles passes mostly in the wood or secondary phloem where female beetles create a tunnel into the bark of dying or dead elm wood and lay their eggs (Kirisits 2007; Sherif et al. 2014). After hatching into larvae, the larvae feed on sapwood and inner bark and after maturing adult elm bark beetles fly to feed on twig crotches and the inner bark of healthy elm trees transferring DED pathogen spores on the surface of their body and in their gut (Webber 1990, 2004; Moser et al. 2010; Bernier et al. 2014) to xylem tissues (Sherif et al. 2017).

Although elm bark beetles are the primary vector of DED pathogen, the fungus can also spread from infected trees to healthy elms through grafted roots (Gibbs 1978), more frequently in the areas where elms are closely spaced (Sherif et al. 2014).

Ecological Impacts

Elms are ecologically important trees as many different organisms are associated with them (Thor et al. 2010) incl. red-listed lichens (Jüriado et al. 2009) and endangered fungi (Rhodotus palmatus, Hymenochaete ulmicola) (Corfixen and Parmasto 2005; Kalamees 2011).

Economic Impacts

The annual cost of removing dead and severely diseased elms in the United States alone has reached $ 100 million (Campbell and Schlarbaum 1994) and keeping the disease under control has cost the same amount (Pimentel, Zuniga et al. 2005)

Social Impacts

Traditionally elms have also been multi-purpose trees (Martín et al. 2019) and valued for their timber, suitability for coppicing, landscaping and as roadside trees (Richens 1983; Heybroek 2015; Caudullo and De Rigo 2016).

Elms are one of the main amenity tree species because they tolerate city conditions e.g. polluted air, anti-slip salts, grow on different soil types (incl. compacted) (Whiteley 2004), resist winds, recover well from mechanical damage and survive in droughts and temporary floods (Townsend and Douglass 2004; Scheffer et al. 2008; Zalapa et al. 2008; Buiteveld et al. 2015).

Detection

Molecular analysis is the most reliable way of detection of pathogens even if it is time-consuming and costly (Stenlid et al. 2011).

There is an urgent need for developing more effective molecular tools for the identification of DED agent hybrids (Konrad et al. 2002) with the help of high-throughput or hopefully portable molecular detection (Luchi et al. 2020) at an early stage of the disease development to protect the plants in the stage of prevention.

Preventive measures and suppression measures

• Elms resistant to Dutch elm disease

Breeding for resistance began in the Netherlands in 1928 and continued until about 1992 (Heybroek 1993, 2000, Scheffer et al. 2008). Early emphasis was placed primarily on selecting for resistance within native species, especially Ulmus glabra and U. carpinifolia and their various hybrids. During the second disease pandemic in Europe that peaked during the 1970s (Brasier 2000) decimated many surviving native populations and some of the early “resistant” cultivars (e.g., ‘Commelin’) (Scheffer et al. 2008). This led to more extensive use of Asian elm germplasm, particularly the Himalayan elm, U. wallichiana, as a source of resistance genes. More recent elm breeding efforts in Spain and Italy emphasize the native European species Ulmus glabra and U. carpinifolia (=U. minor) but rely on the Siberian elm (U. pumila) as the source of disease resistance genes (Santini et al. 2003, Solla et al. 2000, Scheffer et al. 2008). Siberian elm seems better adapted to the warmer, drier parts of the Mediterranean region than to the cooler, moister climates of Great Britain and the Netherlands where other diseases take their toll on U. pumila. Similar breeding experiences took place in the United States beginning in the 1930s with early efforts focused on identifying resistant individuals in North American species, especially U. americana (Smalley and Guries 1993, Scheffer et al. 2008). Subsequent programs shifted to exploiting either selections within a resistant species, such as various cultivars of U. parvifolia developed by the U.S. Department of Agriculture (Townsend 2000) or released by private nurseries, or interspecific hybrids.

In 2005, the National Elm Trial (USA) began a 10-year evaluation of 19 cultivars in plantings across the United States. The trees in the trial were exclusively American developments; no European cultivars were included. Based on the trial's final ratings, the preferred cultivars of the American elm (Ulmus americana) are ‘New Harmony’ and ‘Princeton’. The preferred cultivars of Asian elms are the Morton Arboretum introductions and ‘New Horizon’ (National… 2018, Griffin et al. 2017).

New trials in different European countries have been started for now.

Respond & Control

• Biological control

The University of Amsterdam developed a biological vaccine by the late 1980s. DutchTrig (Scheffer et al. 2008) is nontoxic, consisting of a suspension in distilled water of spores of a strain of the fungus Verticillium albo-atrum that has lost much of its pathogenic capabilities, injected in the elm in spring. injections with Verticillium WCS850 restricted new infections by the Dutch elm disease pathogen to less than 1% annually. However, infections through root grafts are not controlled and the treatment must be repeated annually (Scheffer et al. 2008). Preventive treatment is usually justified only when a tree has unusual symbolic value or occupies a particularly important place in the landscape. Pheromone traps can catch millions of beetles, but they have never proven effective in controlling Dutch elm disease (Peacock 1981).

• Sanitation and beetle population control

Eradication of Dutch elm disease has often been attempted, but without success. All dying and dead elm wood should be promptly destroyed; at a minimum, the bark has to be pared from the wood. Otherwise, new beetles will emerge to sustain the epidemic. Eradication program is more effective while initiated immediately upon discovery of the disease (Scheffer et al. 2008).

More success stories exist, such as the Integrated Elm Program of the City of Hamburg, Germany, which reports losses due to Dutch elm disease of less than 1%, and similar programs in a number of cities in North America (Scheffer et al. 2008).

• Fungicide treatment

Control of the pathogen by fungicide treatment has focused mainly on benzimidazoles (benomyl, carbendazim, and thiabendazole) and sterol biosynthesis inhibitors, like Arbotect 20-S® and Alamo®. Both products are often effective as a single treatment when properly applied by exposed root flare injection at the highest dosage rates allowed (Stennes 2000). Arbotect 20-S appears effective in protecting elm trees for up to 3 years (Scheffer et al. 2008).

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