Hymenoscyphus fraxineus
(ash dieback)

Pictures

Picture	Title	Caption	Copyright
Title Symptoms Caption Hymenoscyphus fraxineus (ash dieback); ash die-back symptoms, caused by the fungal disease, Chalara fraxinea. Akershus, Norway. 03 June 2008. Copyright ©Prof. Halvor Solheim/NIBIO - All Rights Reserved	Symptoms	Hymenoscyphus fraxineus (ash dieback); ash die-back symptoms, caused by the fungal disease, Chalara fraxinea. Akershus, Norway. 03 June 2008.	©Prof. Halvor Solheim/NIBIO - All Rights Reserved
Title Symptoms Caption Hymenoscyphus fraxineus (ash dieback); ash die-back symptoms, caused by the fungal disease, Chalara fraxinea; canker on Ash sapling. Vestby, Akershus, Norway. 29 May 2008. Copyright ©Prof. Halvor Solheim/NIBIO - All Rights Reserved	Symptoms	Hymenoscyphus fraxineus (ash dieback); ash die-back symptoms, caused by the fungal disease, Chalara fraxinea; canker on Ash sapling. Vestby, Akershus, Norway. 29 May 2008.	©Prof. Halvor Solheim/NIBIO - All Rights Reserved
Title Symptoms Caption Hymenoscyphus fraxineus (ash dieback); ash die-back symptoms, caused by Chalara fraxinea; close-up of canker on an Ash sapling (Fraxinus excelsior). Vestby, Akershus, Norway. 29 May2008. Copyright ©Prof. Halvor Solheim/NIBIO - All Rights Reserved	Symptoms	Hymenoscyphus fraxineus (ash dieback); ash die-back symptoms, caused by Chalara fraxinea; close-up of canker on an Ash sapling (Fraxinus excelsior). Vestby, Akershus, Norway. 29 May2008.	©Prof. Halvor Solheim/NIBIO - All Rights Reserved
Title Symptoms Caption Hymenoscyphus fraxineus (ash dieback); ash die-back symptoms, caused by the fungal disease, Chalara fraxinea; canker and excavated necrosis on an Ash sapling. Rygge, Østfold, Norway. 26 May 2008. Copyright ©Prof. Halvor Solheim/NIBIO - All Rights Reserved	Symptoms	Hymenoscyphus fraxineus (ash dieback); ash die-back symptoms, caused by the fungal disease, Chalara fraxinea; canker and excavated necrosis on an Ash sapling. Rygge, Østfold, Norway. 26 May 2008.	©Prof. Halvor Solheim/NIBIO - All Rights Reserved
Title Symptoms Caption Hymenoscyphus fraxineus (ash dieback); ash die-back symptoms, caused by the fungal disease, Chalara fraxinea; typical necrosis, bisected. Ås, Akershus, Norway. 29 May 2008. Copyright ©Prof. Halvor Solheim/NIBIO - All Rights Reserved	Symptoms	Hymenoscyphus fraxineus (ash dieback); ash die-back symptoms, caused by the fungal disease, Chalara fraxinea; typical necrosis, bisected. Ås, Akershus, Norway. 29 May 2008.	©Prof. Halvor Solheim/NIBIO - All Rights Reserved
Title Symptoms Caption Hymenoscyphus fraxineus (ash dieback); ash die-back symptoms, caused by the fungal disease, Chalara fraxinea, showing an infected tree crown. Vestby, Akershus, Norway 03 June 2008. Copyright ©Prof. Halvor Solheim/NIBIO - All Rights Reserved	Symptoms	Hymenoscyphus fraxineus (ash dieback); ash die-back symptoms, caused by the fungal disease, Chalara fraxinea, showing an infected tree crown. Vestby, Akershus, Norway 03 June 2008.	©Prof. Halvor Solheim/NIBIO - All Rights Reserved
Title Phialides Caption Phialides from malt extract agar. Original x1000. Copyright ©USDA-ARS/Systematic Mycology & Microbiology Laboratory	Phialides	Phialides from malt extract agar. Original x1000.	©USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Phialide and conidia Caption Phialide and conidia from malt extract agar. Original x1000. Copyright ©USDA-ARS/Systematic Mycology & Microbiology Laboratory	Phialide and conidia	Phialide and conidia from malt extract agar. Original x1000.	©USDA-ARS/Systematic Mycology & Microbiology Laboratory
Title Phialide and conidia Caption Phialide and conidia from malt extract agar. Original x1000. Copyright ©USDA-ARS/Systematic Mycology & Microbiology Laboratory	Phialide and conidia	Phialide and conidia from malt extract agar. Original x1000.	©USDA-ARS/Systematic Mycology & Microbiology Laboratory

Identity

Preferred Scientific Name

• Hymenoscyphus fraxineus (T. Kowalski) Baral, Queloz & Hosoya

Preferred Common Name

• ash dieback

Other Scientific Names

• Chalara fraxinea T. Kowlowski 2006
• Hymenoscyphus albidus misapplied name (Kowalski and Holdenrieder)
• Hymenoscyphus pseudoalbidus V. Queloz et al. 2011

International Common Names

• French: Chalarose du frêne

Local Common Names

• Germany: schäden an eshen

Summary of Invasiveness

H. fraxineus is an anamorphic fungal pathogen that causes ash dieback. Due to the severity of ash dieback H. pseudoalbidus has been on the EPPO Alert list since 2007. It is not known what caused the emergence of this 'new' disease (NAPPO, 2009). Its spread in Europe is thought to be mainly by ascospores, but infected nursery saplings may carry the fungus to new areas. The entire natural range of known hosts, including North Africa, Russia and south-west Asia (USDA-ARS, 2009), is currently threatened by ash dieback, with large areas already affected (Pautasso et al., 2013). Little is known about the susceptibility of the other species of ash in temperate zones.

Taxonomic Tree

• Domain: Eukaryota
•     Kingdom: Fungi
•         Phylum: Ascomycota
•             Subphylum: Pezizomycotina
•                 Class: Leotiomycetes
•                     Subclass: Leotiomycetidae
•                         Order: Helotiales
•                             Family: Helotiaceae
•                                 Genus: Hymenoscyphus
•                                     Species: Hymenoscyphus fraxineus

Notes on Taxonomy and Nomenclature

The conidial anamorph of the causal agent of ash dieback was described by Kowalski (2006) as Chalara fraxinea, based on the structure of its phialides, which have a wide basal venter and a long collarette, enclosing a deep-seated site of conidial formation. Later, the apothecial teleomorph was reported to be a previously identified species of Hymenoscyphus, H. albidus (Kowalski and Holdenrieder, 2009b), that has been known from Europe since 1851 (Queloz et al., 2011). However, Queloz et al. (2011) presented molecular evidence for the existence of two morphologically very similar taxa, H. albidus and H. fraxineus (as H. pseudoalbidus). Inoculation experiments have shown that H. albidus is a non-pathogenic species, whereas H. fraxineus is a virulent species causing ash dieback on Fraxinus excelsior and F. angustifolia (Husson et al., 2011). Phylogenetic analysis showed that Japanese isolates previously recorded as Lambertella albida are conspecific with European H. fraxineus, although they appear more basal in the phylogenetic tree and show higher levels of genetic variation (Zhao et al., 2013). The sister species of H. fraxineus is the recently described H. albidoides, which has been isolated from the leaf litter of Picrasma quassioides in China (Zheng and Zhuang, 2013). The current preferred name for this pathogen is Hymenoscyphus fraxineus.

Description

Colonies on malt extract agar (MEA) are cottony, white, orange-brown or fulvous brown, reverse brownish, grey sectors in areas associated with sporulation; sporulation can be induced by incubation at low temperatures; growth slow, about 1 mm per day at 20°C, although cultures grow faster and are more morphologically stable when grown on MEA containing ash leaves (Gross et al., 2012); pseudoparenchymatous stromata formed occasionally after prolonged incubation; hyphae 1.0-3.0 µm broad, subhyaline to olive-brown. Phialophores solitary and scattered, septate, branched or unbranched, olive-brown. Phialides subcylindrical to obclavate, 16-24 µm long, olive-brown; venter cylindrical to ellipsoid, 11-15 x 4-5 µm; collarettes cylindrical, 5-7 x 2.0–2.5 µm. Conidia short-cylindrical, hyaline to subhyaline, aseptate, smooth-walled, 2.0-4.0 x 2.0-2.5 µm, ends truncate or rounded, occasionally bearing small marginal frill, exuded in short chains or more often in droplets; first-formed conidia longer.

Ascomata apothecial scattered, superficial, white to cream, becoming cinnamon brown with age and drying, arising from blackened areas of fallen petioles or dead shoots; disk flat, 1.5-3.0 mm diameter, stipe 0.4-2.0 x 0.2-0.5 mm, enlarged or narrow at base, basal region frequently black. Paraphyses cylindrical, 2.0-2.5 µm thick, enlarged to 3 µm at apex, septate, hyaline, slightly yellowish. Asci cylindric-clavate, stipitate, 80-107 x 6-12 µm, eight-spored. Ascospores irregularly biseriate, fusiform-elliptical, broadly rounded above, narrow below, straight or slightly curved, 13-17 (-21) x 3.5-5.0 µm, hyaline and aseptate within ascus, becoming 1(-2)-septate and brownish on MEA.

For additional details, see White (1944), Kowalski (2006), Halmschlager and Kirisits (2008), Kirisits et al. (2009), Kowalski and Holdenrieder (2009b) and Kowalski and Bartnik (2010).

Distribution

Ash dieback disease was first observed in North and Central Europe in the 1990s and since then H. pseudoalbidus has spread throughout much of Europe. It has been found on Fraxinus mandshurica in Japan and China, where it appears to be non-pathogenic on its native host (Zhao et al., 2013, Zheng and Zhuang, 2014). Combined with the lack of resistance in European ash species this suggests an Asian origin for H. fraxineus.

Distribution Table

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.

History of Introduction and Spread

Ash dieback disease was first observed in North and Central Europe in the 1990s (Bakys et al., 2009a; Kowalski and Holdenrieder, 2009b). H. fraxineus (as Chalara fraxinea) was identified as the primary cause in Poland by Kowalski (2006), and was subsequently found in Germany (Schumacher et al., 2007), Sweden (Thomsen et al., 2007), Norway (Jankovský and Holdenrieder, 2009), Denmark (EPPO, 2009a), the Czech Republic (Jankovský and Holdenrieder, 2009), Austria (Halmschlager and Kirisits, 2008) and Hungary (Kirisits et al., 2009; Szabó, 2009). By November 2010, the disease had been reported from 22 European countries (Timmermann et al., 2011). The disease has since been recorded in the UK; for further information see: http://www.forestry.gov.uk/chalara.

Genotyping of herbarium specimens was initially thought to show that H. fraxineus had been present in Switzerland for at least 30 years prior to the outbreak of ash dieback (Queloz et al., 2011). However, further molecular analysis of the specimens revealed that they share 100% sequence similarity with H. albidus (Queloz et al., 2012) and there is therefore no evidence to contradict the view that H. fraxineus is a recent invasive species in Switzerland. Additional information is needed regarding the host range and distribution of the teleomorph (NAPPO, 2009).

Risk of Introduction

H. fraxineus could certainly be distributed from forest nurseries on infected saplings (Kirisits et al., 2009). Wind-blown ascospores could be dispersed locally, as occurs with the related pathogen Crumenulopsis sororia (Hayes, 1980). Ash seeds can be naturally infected with H. fraxineus, although the effect of infection on germination is not known (Cleary et al., 2013a). Despite trade in ash seed between Europe and North America the disease has not been reported in the USA. International concern with the invasive emerald ash borer beetle (Agrilus planipennis) (USDA/APHIS, 2009; CFIA, 2009; EPPO, 2009a) should enhance restrictions on, and inspection of, any ash (Fraxinus) logs or lumber that might carry the fungus over great distances.

Habitat List

Hosts/Species Affected

Only two Fraxinus species, F. excelsior (Kowalski, 2006) and F. angustifolia (Kirisits et al., 2009), are definitely known to be susceptible to the pathogen. The third species of ash native to Europe, F. ornus, was found to be less susceptible to the disease following field inoculations (Krautler and Kirisits, 2012). Other species in the same section of the genus (USDA-ARS, 2009) include: F. mandshurica, the cultivated F. holotricha in Europe; F.pallisiae, native to southeastern Europe; F.sogdiana in central Asia; and F. nigra, an ash native to North America (USDA-ARS, 2009). In Asia, H. fraxineus has only been recorded on F. mandshurica and F. chinensis. On these native hosts the fungus is apparently hemi-biotrophic and does not cause disease (Zhao et al., 2013). However, F. mandschurica was found to be mildly affected by ash dieback in south east Estonia (Drenkhan and Hanso, 2010). Three species of ash native to America have been investigated for susceptibility: F. nigra is badly affected, F. pennsylvanica shows slightly less severe symptoms whilst F. americana is the least affected (Drenkhan and Hanso, 2010). Stem inoculations of Acer pseudoplatanus and Sambucus nigra did not result in necrotic lesions (Kowalski and Holdenrieder, 2009a).

Host Plants and Other Plants Affected

Growth Stages

Symptoms

Ash trees of all ages are affected, although younger trees have been observed to succumb more rapidly. The disease first becomes visible in late summer as necrotic lesions form on leaflets. As the disease progresses symptoms include wilting and blackish discolouration of leaves, premature shedding of leaves, dieback of shoots, twigs and branches, necrosis of bark tissue, discrete necrotic cankers in the bark, diamond-shaped lesions on stems and a brownish to greyish discolouration of the inner bark and wood that often extends beyond the region of visible bark necrosis. Trees suffering from severe dieback may produce epicormic shoots (Halmschlager and Kirisits, 2008; Johansson et al., 2009; Kowalski and Holdenrieder, 2009a). Infection is non-systemic, however, in inoculated saplings, where mycelium has been observed in various tissue types including ray parenchyma, phloem fibres, and xylem vessels (Schumacher et al., 2010, Dal Maso et al., 2012, Cleary et al., 2013b). Hyphae grow intracellularly and occasionally form itrahyphal hyphae (Dal Maso et al., 2012). The fungus has been isolated from asymptomatic roots of inoculated ash (Fraxinus) saplings (Schumacher et al., 2010), but has also been found in dead roots of trees (Kowalski, 2006).

List of Symptoms/Signs

Biology and Ecology

Life Cycle

Both the conidial anamorph and the apothecial teleomorph have been described for this species, but their roles in the life cycle and spread of the pathogen have not been fully determined. Unlike H. fraxineus, H. albidus does not form an anamorphic stage and this is one way to distinguish between the species (Kirisits et al., 2013).

Conidia are produced in culture (Kowalski, 2006; Halmschlager and Kirisits, 2008) and sporulation has been found on the surface of lesions on inoculated young trees, but is rarely observed in the field (Kowalski and Holdenrieder, 2009b). Production of conidia in culture is enhanced at low temperatures, but some isolates do sporulate at 23 to 25°C (Halmschlager and Kirisits, 2008; Jankovský and Holdenrieder, 2009; Szabó, 2009).

The fungus overwinters in the leaf litter, forming a black pseudosclerotial layer on ash rachises. Apothecia are produced between July and October, although this will vary according to climatic conditions (Kowalski and Holdenrieder, 2009b, Hietala et al., 2013). Apothecia were also found occasionally on shoots of dead seedlings in nurseries (Kowalski and Holdenrieder, 2009b). Gross et al. (2012) observed that UV light and moisture appear to be important for apothecial maturation. Ascospores are released in a diurnal pattern with a peak between 6am and 8am, possibly to coincide with morning dew and to prevent desiccation (Timmermann et al., 2011).

Ascospores adhere to leaflets and penetrate the cuticle via an appresorium and germ tube (Cleary et al., 2013b). Hyphae rapidly proliferate and the mycelium may spread from the leaf lamina via the rachis to the stem. However, this is a dead end for the pathogen and the life cycle is completed in the leaf litter after infected leaves are shed.

Molecular characterization of the mating type locus has shown that H. fraxineus is heterothallic, unlike H. albidus which is structurally homothallic (Gross et al., 2012). A multiplex PCR is available for mating type determination. Parental analysis of individual apothecia on single rachises revealed that rachises may be colonized by multiple genotypes which can either cross fertilize or be fertilized by external genotypes. It is therefore possible that conidia act as spermatia, although the timing of fertilization is not yet known (Gross et al., 2012).

Research into the vegetative incompatibility system in H. fraxineus is ongoing (Brasier and Webber, 2013). Initial results suggest that the majority of isolates from the UK are incompatible with each other, even when isolated from a small sample area, indicating a high degree of heterogeneity in the vic gene loci. It remains to be determined whether the vic system is active or inactive during the initial infection process, which would result in competition or cooperation, respectively, between juvenile mycelia. The latter might be a mechanism enabling different isolates to collaborate to overcome host resistance. Further work is needed to establish whether viruses can migrate between incompatible genotypes as this has implications for the potential to control the fungus through the use of hypovirulence-causing mycoviruses.

Physiology and Phenology

Differences in cultural morphology of isolates were illustrated in Halmschlager and Kirisits (2008) and Kowalski and Bartnik (2010). Ten isolates of H. fraxineus (as Chalara fraxinea), most of them from Germany, varied in extracellular oxidase activity (Schumacher et al., 2009). Kowalski and Bartnik (2010) found that colonies grew from 5 to 30°C with optimal growth for most isolates being 20°C. In this study temperature strongly influenced colony morphology.

The phytotoxin viridiol and related secondary metabolites have been implicated in pathogenicity (Grad et al., 2009, Andersson et al., 2010) although their role in the infection process has been cast into doubt following the finding that H. albidus also produces viridiol (Junker et al., 2013).

Associations

Other fungi, some of which may be opportunistic pathogens invading the lesions caused by H. fraxineus, are readily isolated from necrotic bark (Kowalski and Holdenrieder, 2009b; Schumacher et al., 2010). Root-infecting Phytophthora species were not found to be involved in the disease of ash dieback in Sweden (Bakys et al., 2009a; Schumacher et al., 2010).

Environmental Requirements

Abiotic stresses considered to be associated with ash dieback are drought, frost and changing winter conditions (Schumacher et al., 2007). As canker growth has been observed to be greater in winter, the fungus appears to be adapted to cold weather (Jankovský and Holdenrieder, 2009).

Climate

Means of Movement and Dispersal

Natural Dispersal

From a study in Norway, ascospores were considered to be the primary source initiating host infections and responsible for the rapid recent spread of H. fraxineus in Europe (Timmerman et al., 2011). The pattern of wider environment sites of infection in the UK matches predictions based on models of airborne incursion of ascospores from the continent (Castle and Cox, unpublished). Conidia are produced in droplets or chains (Kowalski, 2006; Talgø et al., 2009). Described as ‘sticky’ (Kowalski and Holdenrieder, 2009b), they would not appear to be adapted for airborne dispersal.

Vector Transmission

No vector is known (Kowalski and Holdenrieder, 2009b), but insects are known to have a role in the dispersal of conidia of other Chalara species (Kile, 1993). Some of these fungi produce attractive volatile compounds on infected trees (Kile, 1993). Fungal spores produced in liquid droplets are adapted for insect dispersal, and some scolytid beetle larvae develop in leaf petioles in the litter layer under trees (Crowson, 1984).

Accidental Introduction

The pathogen could be carried from nurseries in asymptomatic or overlooked infected saplings (Kirisits et al., 2009; Schumacher et al., 2010).

Pathway Causes

Pathway Vectors

Plant Trade

Impact Summary

Economic Impact

This fungus could cause losses of different severity depending on whether affected trees are in forests, planted as ornamentals, or raised in nurseries (Schumacher et al., 2010; Talgø et al., 2009). Kowalski (2006) reported that in Poland trees were killed in all age classes and regardless of site conditions. For more information on economic impacts in the UK, see Sansford (2013).

Risk and Impact Factors

• Invasive in its native range
• Reproduces asexually

• Pathogenic

• Difficult to identify/detect as a commodity contaminant
• Difficult to identify/detect in the field

Diagnosis

This fungus cannot be reliably isolated in culture (Lygis et al., 2005; Bakys et al., 2009a; Kowalski and Holdenrieder, 2009a) and is slow-growing (Kowalski and Holdenrieder, 2009b; Schumacher et al., 2010). Other fungi may overgrow it in culture or invade necrotic bark tissues in its cankers (Bakys et al., 2009b). Isolation from necrotic lesions has a higher success rate in autumn and winter, although isolation from pseudosclerotial rachises may be the most straightforward method (Gross and Holdenrieder, 2013).

Three PCR techniques for the detection of the fungus in infected plant tissue have been published, each using primers for sequences in the ITS region of rDNA to amplify DNA specific to H. fraxineus (Chandelier et al., 2009; Ioos et al., 2009; Johansson et al., 2009). The protocol of Johansson et al. (2009) uses the sequence of an intron in the region unique to this species within the genus Hymenoscyphus, whereas those of Chandelier et al. (2009) and Ioos et al. (2009, 2011) were tested against a number of Chalara species and other fungi that may be present in or on the lesions. The sequences of ITS regions of rDNA for the teleomorph and the anamorph are available in GenBank for comparison (NCBI, 2009).

Recently, Thi Lam Huong et al. (2013) demonstrated that H. fraxineus could be successfully identified in vitro and in vivo in infected ash leaves by mass spectrometry using specific secondary metabolites produced by the pathogen as markers for its presence.

Detection and Inspection

Trees can be observed for dieback symptoms, but these may be confused with those caused by other fungi or by insects, and H. fraxineus can be present in asymptomatic leaves (Bakys et al., 2009a,b). The other pathogens may be excluded from the diagnosis on the basis of the absence of their characteristic fruiting structures. However, the Chalara anamorph has seldom been observed sporulating in natural lesions (Kowalski and Holdenrieder, 2009a). The apothecia are produced on detached petioles in the leaf litter (Kowalski and Holdenrieder, 2009b), but may also occur on dead shoots (Kowalski and Holdenrieder, 2009a). Forestry Commission (2012) includes a pictorial guide and video of symptoms in the field.

Similarities to Other Species/Conditions

The Chalara anamorph of H. fraxineus can be distinguished from other Chalara species (Nag Raj and Kendrick, 1975; McKenzie et al., 2002) by its small, short cylindrical, aseptate conidia (Kowalski, 2006). The teleomorph is differentiated from most other Hymenoscyphus species by its occurrence on Fraxinus and the dark superficial layer produced on the substrate at the base of the apothecium (Kowalski and Holdenrieder, 2009b).  H. fraxineus can be distinguished from H. albidus by the presence of croziers at the ascus base which are absent in the latter (Zhao et al., 2013); by the shape of crystals within the tissues of the stipe base; by the outer layer of hyphae over the flanks of the ectal excipulum, which are parallel in H. albidoides and interwoven in H. fraxineus; and by the fact that unlike H. fraxineus, H. albidus does not form an anamorphic stage and this is one way to distinguish between the species (Kirisits et al., 2013; Zheng and Zhuang, 2013).

Unlike most other dieback and canker-causing pathogens known to affect Fraxinus (Sinclair and Lyon, 2005), this fungus does not sporulate in pycnidia or perithecia and produces no obvious stromata in or on infected stems or branches. Complicating the diagnosis, some of those other fungi, including Fusarium species and Botryosphaeriastevensii, may be isolated from necrotic bark lesions caused by H. fraxineus (Bakys et al., 2009a,b; Kowalski and Holdenrieder, 2009a; Schumacher et al., 2010).

Symptoms of ash dieback are similar to those caused by the emerald ash borer (Agrilus planipennis) (NAPPO, 2009), but the beetle is known to attack a wider range of Fraxinus species, and the larvae create S-shaped galleries in the sapwood, whereas emerging adults leave characteristic holes in the bark (APHIS, 2009; CFIA, 2009).

Prevention and Control

Prevention

SPS Measures

As ash (Fraxinus) saplings may be infected without showing symptoms, quarantines may be necessary to prevent additional distribution from affected nurseries in Europe. Restriction of the movement of other ash material may be useful or necessary due to the possible role of vectors (NAPPO, 2009).

Importation of Fraxinus species from European countries to the USA was prohibited already due to the occurrence of another pathogen, Pseudomonas savastanoi, that causes cankers and dwarfing (CFR, 2008a), and importation of ash plants from other countries was later prohibited in order to prevent further introductions of the emerald ash borer (Agrilus planipennis) (CFR, 2008b).

Control

Cultural Control and Sanitary Measures

Not enough is known of the biology of this pathogen to indicate the usefulness of particular methods. Avoidance of wounding and destruction of infected plants or plant parts are control measures suggested for other dieback and canker-causing fungi (Kile, 1993). Leaf scars have served as infection courts for artificial inoculation of saplings (Talgø et al., 2009).

Since the host can tolerate higher temperatures than the fungus, hot water treatments have been suggested for small plants (Hauptman et al., 2013). However, masking disease symptoms may facilitate long distance dispersal of the disease when treated seedlings are planted out. Infected trees should only be destroyed when there is limited recently introduced infected material and the surrounding wider environment is disease free. Otherwise trees should be left in place in order to identify potentially resistant stock.

Host Resistance

Variation in tolerance to disease has been found amongst clones and half-sib progeny in a number of sites (McKinney et al., 2011; Pliura, 2011; Kjær et al., 2012; Stener, 2012). These differences have a genetic basis and are heritable, suggesting the potential to breed a resistant ash population. However, tolerant trees have been found in low numbers in Denmark, where only 1% of trees in natural populations expected to produce tolerant offspring (Kjær et al., 2012). Other ash species in the section Fraxinus or other sections are being tested as sources of resistance (Drenkhan and Hanso, 2010).

A correlation has been found between early leaf senescence and resistance (McKinney et al., 2011, Stener, 2012). This could be an escape mechanism, indicating that site conditions influencing phenology are important. However, early senescing clones also develop smaller lesions, suggesting they possess a genetically determined defence mechanism (McKinney et al., 2012).

Gaps in Knowledge/Research Needs

As Schumacher et al. (2009) indicated, more research is needed concerning the source of inoculum, possible vectors, points of infection and the conditions of the infection process itself. Information on these may yield clues concerning the reason for the emergence of this disease (Kowalski and Holdenrieder, 2009b; NAPPO, 2009).

Variation in virulence amongst different strains of the pathogen requires further investigation, but see Bakys et al. (2009), Husson et al. (2011) and Kowalski and Holdenrieder (2009a). Furthermore, studies into disease severity along environmental gradients could offer insight into the role of the environment in determining disease outcome.

Virus mediated hypovirulence in European Castanea dentata has enabled this host to coexist with the otherwise highly destructive Chestnut canker pathogen, Cryphonectia parasitica. Work is therefore underway to identify viruses in H. fraxineus (Pliura et al., 2013).

A better understanding of the mechanism enabling the fungus to switch from hemi-biotrophic in its natural range to pathogenic on non-native hosts is needed (Gross et al., 2013). This would be facilitated by more detailed studies of the fungus in its natural range.

Genomic projects are underway to gain insights into host-pathogen interactions (MacLean et al., 2013). Some progress has already been made in identifying putative virulence factors. Clones of the known susceptible species and other Fraxinus species should be tested by inoculation to identify sources of resistance as well as to establish the possible host range for the pathogen in Europe and elsewhere.

The use of molecular methods to test nursery trees for infection may validate these molecular methods and provide data for determination of the need for quarantines to prevent spread of the fungus from nurseries.

References

Andersson PF, Johansson SBK, Stenlid J, Broberg A, 2010. Isolation, identification and necrotic activity of viridiol from Chalara fraxinea, the fungus responsible for dieback of ash. Forest Pathology, 40(1):43-46. http://www.blackwell-synergy.com/loi/efp

APHIS, 2009. Emerald ash borer. Emerald ash borer. Washington, D.C., USA: Animal and Plant Health Inspection Service, US Department of Agriculture, unpaginated. http://www.aphis.usda.gov/publications/plant_health/content/printable_version/EAB-GreenMenace-reprint-June09.pdf

Bakys R, Vasaitis R, Barklund P, Ihrmark K, Stenlid J, 2009. Investigations concerning the role of Chalara fraxinea in declining Fraxinus excelsior. Plant Pathology, 58(2):284-292. http://www.blackwell-synergy.com/loi/ppa

Bakys R, Vasaitis R, Barklund P, Thomsen IM, Stenlid J, 2009. Occurrence and pathogenicity of fungi in necrotic and non-symptomatic shoots of declining common ash (Fraxinus excelsior) in Sweden. European Journal of Forest Research, 128(1):51-60. http://springerlink.metapress.com/link.asp?id=110827

Baral HO, Galán R, López J, Arenal F, Villarreal M, Rubio V, Collado J, Platas G, Peláez F, 2006. Hymenoscyphus crataegi (Helotiales), a new species from Spain and its phylogenetic position within the genus Hymenoscyphus. Sydowia, 58(2):145-162

BPI (US National Fungus Collections), 2009. Fungal databases - specimens. Beltsville, Maryland, USA: Systematic Mycology and Microbiology Laboratory/Agricultural Research Service/USDA, unpaginated. http://www.nt.ars-grin.gov/fungaldatabases/specimens/specimens.cfm

Brasier C, Webber J, 2013. Vegetative incompatibility in the ash dieback pathogen Hymenoscyphus pseudoalbidus and its ecological implications. Fungal Ecology, 6:501-512

Breitenbach J, Kranzlin F, 1984. Fungi of Switzerland. Vol. 1. Ascomycetes. Lucerne, Switzerland: Mycological Society of Lucerne, 310 pp

CABI/EPPO, 2009. Chalara fraxinea. [Distribution map]. Distribution Maps of Plant Diseases, No.October. Wallingford, UK: CABI, Map 1060 (Edition 1)

CABI/EPPO, 2013. Hymenoscyphus pseudoalbidus. [Distribution map]. Distribution Maps of Plant Diseases, No.October. Wallingford, UK: CABI, Map 1060 (Edition 2)

Cannon PF, Hawksworth DL, Sherwood-Pike MA, 1985. The British Ascomycotina. An annotated checklist. Slough, UK: Commonwealth Agricultural Bureaux, VIII + 302 pp

CFIA, 2009. Agrilus planipennis (Fairmaire) - Emerald ash borer. Agrilus planipennis (Fairmaire) - Emerald ash borer. Ottawa, Ontario, Canada: Canadian Food Inspection Agency, unpaginated. http://www.inspection.gc.ca/english/plaveg/pestrava/agrpla/tech/agrplae.shtml

CFR, 2008. Foreign Quarantine Notices - Prohibited articles. Foreign Quarantine Notices - Prohibited articles. unpaginated. [US Code of Federal Regulations. Title 7, Chapter 3: APHIS/USDA, Part 319, Section 37.2.] http://edocket.access.gpo.gov/cfr_2008/janqtr/7cfr319.37-2.htm

CFR, 2008. RIN 0579-ac87: Importation of Ash Plants. Foreign Quarantine Notices - Prohibited articles. RIN 0579-ac87: Importation of Ash Plants. Foreign Quarantine Notices - Prohibited articles. unpaginated. [US Code of Federal Regulations. Title 7, Chapter 3: APHIS/USDA, Part 319, Section 37.2, Amendment. Accessed February 3, 2010.] http://www.setonresourcecenter.com/register/2008/dec/18/E8-30077.pdf

Chandelier A, Andre F, Laurent F, 2009. Detection of Chalara fraxinea in common ash (Fraxinus excelsior) using real time PCR. Forest Pathology:unpaginated

Chandelier A, Delhaye N, Helson M, 2011. First report of the ash dieback pathogen Hymenoscyphus pseudoalbidus (Anamorph Chalara fraxinea) on Fraxinus excelsior in Belgium. Plant Disease, 95(2):220. http://apsjournals.apsnet.org/loi/pdis

Cleary MR, Arhipova N, Gaitnieks T, Stenlid J, Vasaitis R, 2013. Natural infection of Fraxinus excelsior seeds by Chalara fraxinea. Forest Pathology, 43(1):83-85. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1439-0329

Cleary MR, Daniel G, Stenlid J, 2013. Light and scanning electron microscopy studies of the early infection stages of Hymenoscyphus pseudoalbidus on Fraxinus excelsior. Plant Pathology, 62(6):1294-1301. http://onlinelibrary.wiley.com/doi/10.1111/ppa.12048/full

Crowson RA, 1984. The associations of Coleoptera with Ascomycetes. In: Fungus-Insect Relationships. Perspectives in Ecology and Evolution [ed. by Wheeler, Q.\Blackwell, M.]. New York, NY, USA: Columbia University Press, 256-285

Davydenko, K., Vasaitis, R., Stenlid, J., Menkis, A., 2013. Fungi in foliage and shoots of Fraxinus excelsior in eastern Ukraine: a first report on Hymenoscyphus pseudoalbidus. Forest Pathology, 43(6), 462-467. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1439-0329 doi: 10.1111/efp.12055

DEFRA, 2018. Ash dieback found on three new host species of tree in the UK. Department for Environment, Food & Rural Affairs (DEFRA). August 7, 2018. https://www.gov.uk/government/news/ash-dieback-found-on-three-new-host-species-of-tree-in-the-uk--2

Dennis RWG, 1956. A revision of the British Helotiaceae in the Herbarium of the Royal Botanic Gardens, Kew, with notes on related European species. Mycological Papers, 62:216 pp

Dennis RWG, 1956. A revision of the British Helotiaceae in the Herbarium of the Royal Botanic Gardens, Kew, with notes on related European species. Mycological Papers, CAB International Mycological Institute, 62, 216 pp

Drenkhan R, Adamson K, Hanso M, 2015. Fraxinus sogdiana, a Central Asian ash species, is susceptible to Hymenoscyphus fraxineus. Plant Protection Science, 51(3):150-152. http://www.agriculturejournals.cz/publicFiles/157005.pdf

Drenkhan R, Hanso M, 2010. New host species for Chalara fraxinea. New Disease Reports, 22:Article 16. http://www.ndrs.org.uk/article.php?id=22016

EPPO, 2009. 13th Meeting of the EPPO Panel on Quarantine Pests for Forestry. 13th Meeting of the EPPO Panel on Quarantine Pests for Forestry. Paris, France: European and Mediterranean Plant Protection Organization, unpaginated. http://www.eppo.org/MEETINGS/2009_meetings/forest_pests.htm

EPPO, 2009. Chalara fraxinea. Chalara fraxinea. Paris, France: European and Mediterranean Plant Protection Organization, unpaginated. http://www.eppo.org/QUARANTINE/Alert_List/fungi/Chalara_fraxinea.htm

EPPO, 2011. EPPO Reporting Service. EPPO Reporting Service. Paris, France: EPPO. http://archives.eppo.org/EPPOReporting/Reporting_Archives.htm

EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm

Forestry Commission, 2012. Chalara dieback of ash (Chalara fraxinea). UK: Forestry Commission. http://www.forestry.gov.uk/chalara

Grad B, Kowalski T, Kraj W, 2009. Studies on secondary metabolite produced by Chalara fraxinea and its phytotoxic influence on Fraxinus excelsior. Phytopathologia, 54:61-69

Gross A, Holdenrieder O, 2013. On the longevity of Hymenoscyphus pseudoalbidus in petioles of Fraxinus excelsior. Forest Pathology, 43(2):168-170. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1439-0329

Gross A, Holdenrieder O, Pautasso M, Queloz V, Sieber TN, 2014. Hymenoscyphus pseudoalbidus, the causal agent of European ash dieback. Molecular Plant Pathology, 15(1):5-21. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1364-3703

Gross A, Zaffarano PL, Duo A, Grünig CR, 2012. Reproductive mode and life cycle of the ash dieback pathogen Hymenoscyphus pseudoalbidus. Fungal Genetics and Biology, 49(12):977-986. http://www.sciencedirect.com/science/article/pii/S1087184512001582

Halmschlager E, Kirisits T, 2008. First report of the ash dieback pathogen Chalara fraxinea on Fraxinus excelsior in Austria. Plant Pathology, 57(6):1177. http://www3.interscience.wiley.com/cgi-bin/fulltext/121520330/HTMLSTART

Han JaeGu, Bhushan Shrestha, Hosoya T, Lee KangHyo, Sung GiHo, Shin HyeonDong, 2014. First report of the ash dieback pathogen Hymenoscyphus fraxineus in Korea. Mycobiology, 42(4):391-396. http://mycobiology.or.kr/search.php?where=aview&id=10.5941/MYCO.2014.42.4.391&code=0184MB&vmode=FULL

Hauptman T, 2011. Ash dieback around the world and in Slovenia. (Jesenov ozig po svetu in pri nas.) In: Zbornik Predavanj in Referatov, 10. Slovenskega Posvetovanja o Varstvu Rastlin, Podcetrtek, Slovenia, 1.-2. Marec 2011 [ed. by Macek, J.\Trdan, S.]. Ljubljana, Slovenia: Plant Protection Society of Slovenia, 247-251

Hauptman T, Piskur B, Groot Mde, Ogris N, Ferlan M, Jurc D, 2013. Temperature effect on Chalara fraxinea: heat treatment of saplings as a possible disease control method. Forest Pathology, 43(5):360-370. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1439-0329

Hayes AJ, 1980. Spore liberation in Crumenulopsis sororia. Transactions of the British Mycological Society, 74(1):27-40

Hietala AM, Solheim H, 2011. Hymenoscyphus species associated with European ash. Bulletin OEPP/EPPO Bulletin [EPPO Workshop on Chalara fraxinea, A Major Threat for Ash Trees in Europe, Oslo, Norway, 30 June-2 July 2010.], 41(1):3-6. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1365-2338

Hietala AM, Timmermann V, BØrja I, Solheim H, 2013. The invasive ash dieback pathogen Hymenoscyphus pseudoalbidus exerts maximal infection pressure prior to the onset of host leaf senescence. Fungal Ecology, 6(4):302-308. http://www.sciencedirect.com/science/article/pii/S1754504813000494

Husson C, Scala B, Caël O, Frey P, Feau N, Ioos R, Marçais B, 2011. Chalara fraxinea is an invasive pathogen in France. European Journal of Plant Pathology, 130(3):311-324. http://springerlink.metapress.com/link.asp?id=100265

Ioos R, Fourrier C, 2011. Validation and accreditation of a duplex real-time PCR test for reliable in planta detection of Chalara fraxinea. Bulletin OEPP/EPPO Bulletin [EPPO Workshop on Chalara fraxinea, A Major Threat for Ash Trees in Europe, Oslo, Norway, 30 June-2 July 2010.], 41(1):21-26. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1365-2338

Ioos R, Kowalski T, Husson C, Holdenrieder O, 2009. Rapid in planta detection of Chalara fraxinea by a real-time PCR assay using a dual-labelled probe. European Journal of Plant Pathology, 125(2):329-335. http://springerlink.metapress.com/link.asp?id=100265

IPPC, 2009. Chalara fraxinea. IPPC Official Pest Report, No. Sl-5/1. Rome, Italy: FAO.https://www.ippc.int/IPP/En/default.jsp

IPPC, 2013. Chalara fraxinea is present in Denmark. IPPC Official Pest Report, No. DNK-07/2. Rome, Italy: FAO. https://www.ippc.int/

Jankovský L, Holdenrieder O, 2009. Chalara fraxinea - ash dieback in the Czech Republic. Plant Protection Science, 45(2):74-78. http://www.cazv.cz

Johansson SBK, Vasaitis R, Ihrmark K, Barklund P, Stenlid J, 2009. Detection of Chalara fraxinea from tissue of Fraxinus excelsior using species-specific ITS primers. Forest Pathology:unpaginated

Junker C, Mandey F, Pais A, Ebel R, Schulz B, 2013. Hymenoscyphus pseudoalbidus and Hymenoscyphus albidus: viridiol concentration and virulence do not correlate. Forest Pathology

Keca, N., Kirisits, T., Menkis, A., 2017. First report of the invasive ash dieback pathogen Hymenoscyphus fraxineus on Fraxinus excelsior and F. angustifolia in Serbia. Baltic Forestry, 23(1), 56-59. http://www.balticforestry.mi.lt

Kile GA, 1993. Plant diseases caused by species of Ceratocystis sensu stricto and Chalara. In: Ceratocystis and Ophiostoma: Taxonomy, Ecology, and Pathogenicity [ed. by Wingfield, M. J.\Seifert, K. A.\Webber, J. F.]. St. Paul, Minnesota, USA: The American Phytopathological Society, 173-183

Kirisits T, Dämpfle L, Kräutler K, 2013. Hymenoscyphus albidus is not associated with an anamorphic stage and displays slower growth than Hymenoscyphus pseudoalbidus on agar media. Forest Pathology, 43(5):386-389. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1439-0329

Kirisits T, Matlakova M, Mottinger-Kroupa S, Halmschlager E, Lakatos F, 2009. Chalara fraxinea associated with dieback of narrow-leafed ash (Fraxinus angustifolia). New Disease Reports, 19:1-2

Kirisits, T., Schwanda, K., 2015. First definite report of natural infection of Fraxinus ornus by Hymenoscyphus fraxineus. Forest Pathology, 45(5), 430-432. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1439-0329 doi: 10.1111/efp.12211

Kjær ED, McKinney LV, Nielsen LR, Hansen LN, Hansen JK, 2012. Adaptive potential of ash (Fraxinus excelsior) populations against the novel emerging pathogen Hymenoscyphus pseudoalbidus. Evolutionary Applications, 5(3):219-228. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1752-4571

Korf RP, 1982. New combinations and a new name for discomycetes illustrated by Boudier in the Icones Mycologicae. Mycotaxon, 14:1-2

Kowalski T, 2006. Chalara fraxinea sp. nov. associated with dieback of ash (Fraxinus excelsior) in Poland. Forest Pathology, 36(4):264-270

Kowalski T, Bartnik C, 2010. Morphological variation in colonies of Chalara fraxinea isolated from ash (Fraxinus excelsior L.) stems with symptoms of dieback and effects of temperature on colony growth and structure. Acta Agrobotanica, 63(1):99-106. http://www.arspolona.com.pl

Kowalski T, Holdenrieder O, 2009. Pathogenicity of Chalara fraxinea. Forest Pathology, 39(1):1-7. http://www.blackwell-synergy.com/loi/efp

Kowalski T, Holdenrieder O, 2009. The teleomorph of Chalara fraxinea, the causal agent of ash dieback. Forest Pathology, 39(5):304-308. http://www.blackwell-synergy.com/loi/efp

Kräutler K, Kirisits T, 2012. The ash dieback pathogen Hymenoscyphus pseudoalbidus is associated with leaf symptoms on ash species (Fraxinus spp.). Journal of Agricultural Extension and Rural Development, 4:261-265

Lizon P, 1992. The genus Hymenoscyphus (Helotiales) in Slovakia, Czechoslovakia. Mycotaxon, 45:1-59

Luchi N, Ghelardini L, Santini A, Migliorini D, Capretti P, 2016. First record of ash dieback caused by Hymenoscyphus fraxineus on Fraxinus excelsior in the Apennines (Tuscany, Italy). Plant Disease, 100(2):535-536. http://apsjournals.apsnet.org/loi/pdis

Lygis V, Vasiliauskas R, Larsson KH, Stenlid J, 2005. Wood-inhabiting fungi in stems of Fraxinus excelsior in declining ash stands of northern Lithuania, with particular reference to Armillaria cepistipes. Scandinavian Journal of Forest Research, 20(4):337-346

MacLean D, Yoshida K, Edwards A, Crossman L, Clavijo B, Clark M, Swarbreck D, Bashton M, Chapman P, Gijzen M, Caccamo M, Downie A, Kamoun S, Saunders DGO, 2013. Crowdsourcing genomic analyses of ash and ash dieback - power to the people. Gigascience, 2(2):(12 February 2013). http://www.gigasciencejournal.com/content/pdf/2047-217X-2-2.pdf

Maso Edal, Fanchin G, Accordi SM, Scattolin L, Montecchio L, 2012. Ultrastructural modifications in Common ash tissues colonised by Chalara fraxinea. Phytopathologia Mediterranea, 51(3):599-606. http://www.fupress.com/pm/

McKenzie EHC, Pinnoi A, Wong MKM, Hyde KD, Gareth Jones EB, 2002. Two new hyaline Chalara species, and a key to species described since 1975. Fungal Diversity, 11:129-139

McKinney LV, Nielsen LR, Hansen JK, Kjær ED, 2011. Presence of natural genetic resistance in Fraxinus excelsior (Oleraceae) to Chalara fraxinea (Ascomycota): an emerging infectious disease. Heredity, 106(5):788-797. http://www.nature.com/hdy

McKinney LV, Thomsen IM, Kjær ED, Nielsen LR, 2012. Genetic resistance to Hymenoscyphus pseudoalbidus limits fungal growth and symptom occurrence in Fraxinus excelsior. Forest Pathology, 42(1):69-74. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1439-0329

Milenkovic, I., Jung, T., Stanivukovic, Z., Karadžic, D., 2017. First report of Hymenoscyphus fraxineus on Fraxinus excelsior in Montenegro. Forest Pathology, 47(5), e12359. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1439-0329

Nag Raj TR, Kendrick WB, 1975. A monograph of Chalara and allied genera. Waterloo, Ontario, Canada: Wilfred Laurier University Press, 200 pp

Nag Raj TR, Kendrick WB, 1993. The anamorph as generic determinant in the holomorph: the Chalara connection in the Ascomycetes, with special reference to the Ophiostomatoid fungi. In: Ceratocystis and Ophiostoma: Taxonomy, Ecology, and Pathogenicity [ed. by Wingfield, M. J.\Seifert, K. A.\Webber, J. F.]. St. Paul, Minnesota, USA: The American Phytopathological Society, 61-70

NAPPO, 2009. Chalara fraxinea Kowalski. Phytosanitary alert system. Chalara fraxinea Kowalski. Phytosanitary alert system. Ottawa, Canada: North American Plant Protection Organization, unpaginated. http://www.pestalert.org/viewNewsAlert.cfm?naid=69

NCBI, 2009. Entrez cross-database search engine. Entrez cross-database search engine. Bethesda, Maryland, USA: National Center for Biotechnology Information, U.S. National Library of Medicine, unpaginated. http://www.ncbi.nlm.nih.gov/sites/gquery

Ogris N, Hauptman T, Jurc D, 2009. Chalara fraxinea causing common ash dieback newly reported in Slovenia. Plant Pathology, 58(6):1173. http://www.blackwell-synergy.com/loi/ppa

Ogris N, Hauptman T, Jurc D, Floreancig V, Marsich F, Montecchio L, 2010. First report of Chalara fraxinea on common ash in Italy. Plant Disease, 94(1):133. http://apsjournals.apsnet.org/loi/pdis

Pautasso M, Aas G, Queloz V, Holdenrieder O, 2013. European ash (Fraxinus excelsior) dieback - a conservation biology challenge. Biological Conservation, 158:37-49. http://www.sciencedirect.com/science/article/pii/S0006320712003813

Pliu¯ra A, Lygis V, Suchockas V, Bartkevicius E, 2011. Performance of twenty four European Fraxinus excelsior populations in three Lithuanian progeny trials with a special emphasis on resistance to Chalara fraxinea. Baltic Forestry, 17(1):17-34, 162-163. http://www.balticforestry.mi.lt

Queloz V, Grünig CR, Berndt R, Kowalski T, Sieber TN, Holdenrieder O, 2011. Cryptic speciation in Hymenoscyphus albidus. Forest Pathology, 41(2):133-142. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1439-0329

Queloz V, Grünig CR, Berndt R, Kowalski T, Sieber TN, Holdenrieder O, 2012. Corrigendum. Forest Pathology, 42:353-353

Rytkönen A, Lilja A, Drenkhan R, Gaitnieks T, Hantula J, 2011. First record of Chalara fraxinea in Finland and genetic variation among isolates sampled from Aland, mainland Finland, Estonia and Latvia. Forest Pathology, 41(3):169-174. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1439-0329

Sansford CE, 2013. Pest Risk Analysis for Hymenoscyphus pseudoalbidus (anamorph Chalara fraxinea) for the UK and the Republic of Ireland. Pest Risk Analysis for Hymenoscyphus pseudoalbidus. UK: Forestry Commission. https://secure.fera.defra.gov.uk/phiw/riskRegister/downloadExternalPra.cfm?id=3848

Sarbhoy AK, Lal G, Varshney JL, 1971. Fungi of India (1967-71). New Delhi, India: Navyug Traders, 148 pp

Schumacher J, Kehr R, Leonhard S, 2009. Mycological and histological investigations of Fraxinus excelsior nursery saplings naturally infected by Chalara fraxinea. Forest Pathology:unpaginated

Schumacher J, Kehr R, Leonhard S, 2010. Mycological and histological investigations of Fraxinus excelsior nursery saplings naturally infected by Chalara fraxinea. Forest Pathology, 40(5):419-429. http://onlinelibrary.wiley.com/doi/10.1111/j.1439-0329.2009.00615.x/full

Schumacher J, Wulf A, Leonhard S, 2007. First record of Chalara fraxinea T. Kowalski sp. nov. in Germany - a new agent of ash decline. (Erster Nachweis von Chalara fraxinea T. Kowalski sp. nov. in Deutschland - ein Verursacher neuartiger Schäden an Eschen.) Nachrichtenblatt des Deutschen Pflanzenschutzdienstes, 59(6):121-123

Sinclair WA, Lyon H, 2005. Diseases of Trees and Shrubs. Second edition. Ithaca, New York: Cornell University Press, 660 pp

Stener LG, 2013. Clonal differences in susceptibility to the dieback of Fraxinus excelsior in southern Sweden. Scandinavian Journal of Forest Research, 28(3):205-216. http://www.tandfonline.com/loi/sfor20

Szabó I, 2009. First report of Chalara fraxinea affecting common ash in Hungary. Plant Pathology, 58(4):797. http://www.blackwell-synergy.com/loi/ppa

Talgø V, Sletten A, Brurberg MB, Solheim H, Stensvand A, 2009. Chalara fraxinea isolated from diseased ash in Norway. Plant Disease, 93(5):548. http://apsjournals.apsnet.org/loi/pdis

Thi Lam Huong Pham, Zaspel I, Schuemann M, Stephanowitz H, Krause E, 2013. Rapid in-vitro and in-vivo detection of Chalara fraxinea by means of mass spectrometric techniques. American Journal of Plant Sciences, 4(2A):444-453. http://www.scirp.org/journal/PaperInformation.aspx?PaperID=28471

Thomsen IM, Skovsgaard JP, Barklund P, Vasaitis R, 2007. Fungal disease is the cause of ash dieback. Skoven, 39:234-236

Timmermann V, Børja I, Hietala AM, Kirisits T, Solheim H, 2011. Ash dieback: pathogen spread and diurnal patterns of ascospore dispersal, with special emphasis on Norway. Bulletin OEPP/EPPO Bulletin [EPPO Workshop on Chalara fraxinea, A Major Threat for Ash Trees in Europe, Oslo, Norway, 30 June-2 July 2010.], 41(1):14-20. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1365-2338

USDA-ARS, 2009. Germplasm Resources Information Network (GRIN). Online Database. Beltsville, Maryland, USA: National Germplasm Resources Laboratory. https://npgsweb.ars-grin.gov/gringlobal/taxon/taxonomysearch.aspx

Zhao YanJie, Hosoya T, Baral HO, Hosaka K, Kakishima M, 2012. Hymenoscyphus pseudoalbidus, the correct name for Lambertella albida reported from Japan. Mycotaxon, 122:25-41. http://www.ingentaconnect.com/content/mtax/mt/2012/00000122/00000001/art00004

Zheng HuanDi, Zhuang WenYing, 2014. Hymenoscyphus albidoides sp. nov. and H. pseudoalbidus from China. Mycological Progress, 13(3), 625-638. http://link.springer.com/article/10.1007%2Fs11557-013-0945-z doi: 10.1007/s11557-013-0945-z

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Contributors

12/12/13 Reviewed by:

Jessica Needham, Consultant, UK and Joan Webber, Forest Research, UK

02/04/10 Original text by:

Distribution Maps