Ash Dieback

Apothecia, pseudosclerotia, hyphae, conidiophores (reduced to phialides), and conidia of Hymenoscyphus fraxineus. In the upper left phialides, conidia can be seen ready to emerge from the collarettes. Photos courtesy of Prof. Tadeusz Kowalski, Dept of Forest Pathology, University of Agriculture, Kraków.

The invasive disease, ash dieback, has devasted ash forests and landscape plantings from Ireland to Moscow. The disease is also known as “Chalara ash dieback”, based on the genus the pathogen was in when first described ​[11]​. That name is still used sometimes to distinguish the disease from ash dieback caused by other agents ​[1]​.

The disease type is a bit ambiguous. Initially a foliage disease, it often develops into a shoot blight and ultimately a branch and stem canker, causing branch dieback along the way.

Hosts

The most widespread and important ash species in Europe, Fraxinus excelsior (common ash, European ash), is highly susceptible. Fraxinus angustifolia (narrow-leaved ash), native to the continent and widely planted in the UK, is also susceptible. Fraxinus ornus (manna ash) is only infected in the foliage, so somewhat less susceptible.

Fraxinus excelsior occupies only 1% of forest area in Europe, but it is locally important and contributes to the economy of rural communities ​[22]​. It is used mostly for flooring and furniture. It is also an important component in planted landscapes (amenity plantings).

Asian ash species have only minor infections on leaves and petioles. Shoot dieback can occur in association with leaf infections, but appears to be caused by other fungi ​[3]​. In general these species are highly tolerant of infection and suffer little significant damage, having evolved with the fungus over thousands of years.

Pathogen

The fungus has suffered through several nomenclatural and identity issues, but is now known as Hymenoscyphus fraxineus (phylum Ascomycota, subphylum Pezizomycotina, class Leotiomycetes, order Helotiales, family Helotiaceae). It was shown to be pathogenic to F. excelsior shortly after its discovery ​[16]​. The ascoma is a white, stalked apothecium (mostly up to 3 mm in diameter, rarely 8 mm), a bowl-shaped structure with the hymenium on the upper surface, mounted on a stipe ​[6, 17]​. Densities of apothecia in areas of active disease can reach over 13 million ha-1 at one time ​[13]​!

The fungus also sporulates asexually with structures that fit the traditional form-genus Chalara. Most hyphae are hyaline, but dark hyphae produce the conidia on exposed conidiophores (not in a conidioma) ​[11]​. The conidiophores are mostly reduced to a single brown phialide (special type of conidiogenous cell), but some have a few cells at the base and may be branched. The phialide pumps out large numbers of spores that accumulate in a slimy drop at the tip, but under some conditions they emerge in a chain.

Environment

The disease is generally more severe on moist than on dry sites ​[22]​. Moist soils allow prolific fruiting and high inoculum. Precipitation and high humidity also facilitate infection. Even in moist sites, conditions drier than normal can lead to increased wilting and dieback ​[22]​.

Cool temperatures also favor fruiting, sporulation, and infection. Hot, dry sites or periods are unfavorable for inoculum production and infection, but they may increase damage to already-infected trees. Most isolates have optimum and maximum growth temperatures of 20 and 25 C, respectively, but there is ±5 C variation among isolates ​[12]​.

Damage and mortality decrease with tree age and increase with stand density ​[22]​.

Disease Cycle

Ascospores are the most important inoculum ​[23]​. They are produced in small white apothecia on the rachis (the central stalk of the compound leaf) of infected, fallen leaves from the previous year or up to 5 years earlier ​[8]​. They are fired upwards and wind‐dispersed during the summer, generally between June and September, with a maximum in early August in Norway ​[23]​. They can travel tens of kilometers, remaining viable.

Conidia are thought to function as spermatia (male gametes) that fertilize the primordial female organ, the ascogonium. However, it was found that a very small proportion of conidia are capable of germinating on and infecting ash leaves ​[5]​. Soil inoculated with conidia apparently developed mycelia, and seedlings could be infected when grown in infested soil ​[5]​. It is not clear to what extent conidia are dispersed by insects, wind, or rain-splash. Asexual reproduction is favored by low temperatures ​[12]​.

On the leaf surface, ascospores usually morph directly into appressoria without producing a germ tube ​[19]​. They directly penetrate an epidermal cell beneath the appressorium. Hyphae invade intracellularly and can penetrate up to 5 cells deep biotrophically, that is, the host cells remain alive ​[18, 19]​. Necrosis begins behind that biotrophic invasion zone. Invasion proceeds into the rachis and petiole. If the leaf is not shed before the fungus reaches the shoot, the fungus may proceed into the shoot. It appears that most, if not all, shoot and stem infections take this route ​[10]​ (but see discussion of basal lesions in next section).

Whether infected leaves are shed prematurely or not, they end up on the ground to provide new inoculum for future years. Pseudosclerotia (black layers of fungal tissue also incorporating host tissue) form crusts on the surface of the rachis. The asexual stage and apothecia arise from the pseudosclerotia.

Signs and Symptoms

Signs include the apothecia as well as the pseudosclerotia, both described and shown above.

Symptoms (see photos below): In mid- to late summer, small, brown lesions appear on the leaves. They expand and become brown to black and necrotic. The tree often drops infected leaves prematurely, which, if successful, prevents the pathogen from progressing through the petioles into the subtending shoots. Infected shoots show light to dark brown, elongated lesions (cankers). From there, it may infect the stem. Elongate, diamond-shaped cankers are formed on the stem around branches from which the fungus entered. Eventually wilting and branch dieback appear.

In twigs, branches, and stems, the fungus can colonize both wood and bark, causing cankers. When a canker girdles a branch, foliage distal to the canker wilts and the branch dies back. Perennial cankers can form on larger branches and stems.

Severe dieback is often accompanied by basal lesions with H. fraxineus at the root collar, but they can appear on asymptomatic trees also, even saplings. It is unclear how root-collar infections develop, but there is some evidence that they arise from infections that enter the roots or root collar (Tadeusz Kowalski, personal communication), perhaps by soil-borne infection from conidia as described above. Some photos show lesions that appear to be moving up the stem from beneath the soil level (e.g., ​[10]​).

Distribution and Damage

The fungus is native to Asia (Korea, northeastern China, far eastern Russia, and Japan), where it causes very minor disease. It was somehow introduced to Europe. The disease first appeared in Poland in 1992 ​[11]​. It quickly spread across the continent, and England’s first detection was in 2012, although it was there at least by 2005 ​[24]​.

The disease is very damaging throughout Europe. Over 80% of young ash in Norway were killed as the pathogen invaded. The disease threatens 95% of European ash trees. However, there is substantial genetic variation in susceptibility of Fraxinus excelsior ​[4]​.

Young or coppiced trees can be killed quite quickly ​[1]​. Older trees take longer to die and may persist in a weakened state for some time. Armillaria root disease, most commonly caused by A. gallica and A. cepistipes, is a common secondary agent contributing to death of larger trees with Chalara ash dieback ​[1, 22]​.

Management

Management strategies of course depend on the severity of damage, local climate, and stand type ​[9, 22]​. In general, trees that are healthy or lightly damaged should be retained for propagation of resistance. In stands with severe disease, harvest of remaining commercial timber before the value decreases further will reduce losses. Such stands should be replanted to other species. Where ash is planted, it should be at low density ​[9]​.

In non-commercial forests of high value for habitat conservation, letting natural succession proceed unhindered may be the best option ​[22]​. Risks posed by dead ash trees for operational staff, forest visitors and infrastructure must be minimized through appropriate hazard tree management.

Other Issues

Population genetics

Analysis suggests that the European population arose from two distinct individuals from Asia ​[20]​. The source population is as much as 8 times more diverse than that in Europe, raising concerns that another introduction could create a population with even more virulence. Indeed, Japanese isolates are significantly more virulent to F. excelsior than are European isolates ​[7]​. Thus, another introduction could result in killing of even the small proportion of ash that are currently resistant.

Risk to North America?

Ash species in North America (NA) are currently being hammered by the exotic, invasive emerald ash borer. Do we now have to worry about Hymenoscyphus fraxineus being introduced? The bad news is that the widely planted American species, Fraxinus pennsylvanica (green ash), is susceptible, but the good news is that it is substantially less so then F. excelsior ​[15]​. However, another study seemed to show the two tree species were about equally susceptible to European isolates ​[7]​. Alarmingly, 12 of 75 F. pennsylvanica obtained for the study were already infected on arrival at the Swiss laboratory. With regard to Japanese isolates, F. pennsylvanica was susceptible, but less so than F. excelsior ​[7]​.

In another study ​[21]​, disease was observed in a Danish arboretum exposed to high inoculum and including eight NA species. American species were generally less damaged than F. excelsior. Most of the 11 F. pennsylvanica and the 10 F. americana (white ash, probably the most important ash in NA) had 10% crown damage, but one F. americana was apparently killed by the disease. In stem inoculations, all NA species developed lesions; mean lesion lengths for F. excelsior, F. americana and F. pennsylvanica were 7.4, 3.2, and 4.7 cm, respectively. Other NA species had longer lesions. In leaf inoculations with ascospores, NA species generally showed symptoms similar to F. excelsior. Overall, NA species F. nigra and F. quadrangulata were highly susceptible. Others were susceptible to leaf infection but may be less so to shoot infection ​[21]​.

The disease was also found on planted American species in a heavily diseased area in Estonia ​[2]​. As seen in Denmark, F. nigra was very susceptible, with symptoms like F. excelsior. Fraxinus americana had relatively minor damage, similar to the Asian F. mandschurica: wilting/necrosis of leaves and minor shoot/twig dieback and bark necrosis. Fraxinus pennsylvanica was intermediate in susceptibility, with symptoms similar to F. nigra, but with fewer dead shoots in the canopy.

So, yes, North Americans should certainly try to keep it out — from both Europe and Asia.

There are other Hymenoscyphus spp. in Europe, and one might wonder what would happen if they got to NA. Hymenoscyphus albidus is native to Europe and harmless there. It is also non-pathogenic to F. pennsylvanica ​[7, 15]​. Hymenoscyphus pusillus is a new species found thus far only on F. pennsylvanica in Europe ​[14]​. It appears to be a saprobe but possibly is endophytic. Is it native to NA, but has not been found there?

Acknowledgment: Dr. Tadeusz Kowalski, Dept. of Forest Pathology, University of Agriculture, Kraków, kindly provided helpful comments on the text, in addition to providing all the photographs.

  • Mature Fraxinus excelsior with severe ash dieback. Photo courtesy of Prof. Tadeusz Kowalski, Dept of Forest Pathology, University of Agriculture, Kraków.

References

  1. 1.
  2. 2.
    Drenkhan R, Hanso M. 2010. New host species for Chalara fraxinea. New Disease Reports 22(1):16–16 <10.5197/j.2044-0588.2010.022.016>.
  3. 3.
    Drenkhan R, Solheim H, Bogacheva A, Riit T, Adamson K, Drenkhan T, Maaten T, Hietala AM. 2017. Hymenoscyphus fraxineus is a leaf pathogen of local Fraxinus species in the Russian Far East. Plant Pathology 66(3):490–500 <10.1111/ppa.12588>.
  4. 4.
    Enderle R, Nakou A, Thomas K, Metzler B. 2015. Susceptibility of autochthonous German Fraxinus excelsior clones to Hymenoscyphus pseudoalbidus is genetically determined. Annals of Forest Science 72(2):183–193 <10.1007/s13595-014-0413-1>.
  5. 5.
    Fones HN, Mardon C, Gurr SJ. 2016. A role for the asexual spores in infection of Fraxinus excelsior by the ash-dieback fungus Hymenoscyphus fraxineus. Scientific Reports 6(1):34638 <10.1038/srep34638>.
  6. 6.
    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 <10.1111/mpp.12073>.
  7. 7.
    Gross A, Sieber TN. 2016. Virulence of Hymenoscyphus albidus and native and introduced Hymenoscyphus fraxineus on Fraxinus excelsior and Fraxinus pennsylvanica. Plant Pathology 65(4):655–663 <10.1111/ppa.12450>.
  8. 8.
    Kirisits T, Woodward S. 2015. Ascocarp formation of Hymenoscyphus fraxineus on several-year-old pseudosclerotial leaf rachises of Fraxinus excelsior. Forest Pathology 45(3):254–257 <10.1111/efp.12183>.
  9. 9.
    Klesse S, Abegg M, Hopf SE, Gossner MM, Rigling A, Queloz V. 2021. Spread and severity of ash dieback in Switzerland – tree characteristics and landscape features explain varying mortality probability. Frontiers in Forests and Global Change 4:645920 <10.3389/ffgc.2021.645920>.
  10. 10.
    Koehl A. 2018. Confirmation of the colonization path of Hymenoscyphus fraxineus from leaves to shoots in Fraxinus excelsior. Master Biologie, Agrosciences thesis. Université de Rennes <https://dumas.ccsd.cnrs.fr/dumas-01962507>.
  11. 11.
    Kowalski T. 2006. Chalara fraxinea sp. nov. associated with dieback of ash ( Fraxinus excelsior ) in Poland. Forest Pathology 36(4):264–270 <10.1111/j.1439-0329.2006.00453.x>.
  12. 12.
    Kowalski T, Bartnik C. 2010. Morphologial 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://agro.icm.edu.pl/agro/element/bwmeta1.element.dl-catalog-d653b081-f72d-4915-8b93-78261c4e7dec/c/a99_106.pdf>.
  13. 13.
    Kowalski T, Białobrzeski M, Ostafińska A. 2013. The occurrence of Hymenoscyphus pseudoalbidus apothecia in the leaf litter of Fraxinus excelsior stands with ash dieback symptoms in southern Poland. Acta Mycologica 48(2):135–146 <10.5586/am.2013.031>.
  14. 14.
    Kowalski T, Bilański P. 2018. Hymenoscyphus pusillus , a new species on leaves of Fraxinus pennsylvanica in Poland. Forest Pathology, p. e12481 <10.1111/efp.12481>.
  15. 15.
    Kowalski T, Bilański P, Holdenrieder O. 2015. Virulence of Hymenoscyphus albidus and H. fraxineus on Fraxinus excelsior and F. pennsylvanica. PLoS ONE 10(10):e0141592 <10.1371/journal.pone.0141592>.
  16. 16.
    Kowalski T, Holdenrieder O. 2009. Pathogenicity of Chalara fraxinea. Forest Pathology 39(1):1–7 <10.1111/j.1439-0329.2008.00565.x>.
  17. 17.
    Kowalski T, Holdenrieder O. 2009. The teleomorph of Chalara fraxinea, the causal agent of ash dieback. Forest Pathology 39(5):304–308 <10.1111/j.1439-0329.2008.00589.x>.
  18. 18.
    Mansfield J, Brown I, Papp‐Rupar M. 2019. Life at the edge – the cytology and physiology of the biotroph to necrotroph transition in Hymenoscyphus fraxineus during lesion formation in ash. Plant Pathology 68(5):908–920 <10.1111/ppa.13014>.
  19. 19.
    Mansfield JW, Galambos N, Saville R. 2018. The use of ascospores of the dieback fungus Hymenoscyphus fraxineus for infection assays reveals a significant period of biotrophic interaction in penetrated ash cells. Plant Pathology 67(6):1354–1361 <10.1111/ppa.12844>.
  20. 20.
    McMullan M, Rafiqi M, Kaithakottil G, Clavijo BJ, Bilham L, Orton E, Percival-Alwyn L, Ward BJ, Edwards A, et al. 2018. The ash dieback invasion of Europe was founded by two genetically divergent individuals. Nature Ecology & Evolution 2(6):1000–1008 <10.1038/s41559-018-0548-9>.
  21. 21.
    Nielsen LR, McKinney LV, Hietala AM, Kjær ED. 2017. The susceptibility of Asian, European and North American Fraxinus species to the ash dieback pathogen Hymenoscyphus fraxineus reflects their phylogenetic history. European Journal of Forest Research 136(1):59–73 <10.1007/s10342-016-1009-0>.
  22. 22.
    Skovsgaard JP, Wilhelm GJ, Thomsen IM, Metzler B, Kirisits T, Havrdová L, Enderle R, Dobrowolska D, Cleary M, et al. 2017. Silvicultural strategies for Fraxinus excelsior in response to dieback caused by Hymenoscyphus fraxineus. Forestry: An International Journal of Forest Research 90(4):455–472 <10.1093/forestry/cpx012>.
  23. 23.
    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*: Ash dieback: pathogen spread and ascospore dispersal. EPPO Bulletin 41(1):14–20 <10.1111/j.1365-2338.2010.02429.x>.
  24. 24.
    Wylder B, Biddle M, King K, Baden R, Webber J. 2018. Evidence from mortality dating of Fraxinus excelsior indicates ash dieback (Hymenoscyphus fraxineus) was active in England in 2004–2005. Forestry: An International Journal of Forest Research 91(4):434–443 <10.1093/forestry/cpx059>.