European Journal of Forest Research

, Volume 132, Issue 5–6, pp 865–876 | Cite as

Temporal development of ash dieback symptoms and spatial distribution of collar rots in a provenance trial of Fraxinus excelsior

  • Rasmus EnderleEmail author
  • Franziska Peters
  • Aikaterini Nakou
  • Berthold Metzler
Original Paper


European ash (Fraxinus excelsior) is threatened by Hymenoscyphus pseudoalbidus, the agent of ash dieback disease. Beside ordinary ash dieback symptoms, collar rots have been reported on declining ashes as an additional problem of increasing severity. Since 2009, ash dieback has been surveyed annually in a provenance trial on four different sites in southwest Germany (Metzler et al. in Ger J For Res 183:168–180, 2012). The trial was established in 2005. Data of tree growth, ash dieback symptoms and collar rot prevalence were collected by surveying the trial in summer 2012 and compared with previously published data of the trial. Evaluations revealed a continuous and considerable increase in dieback severity since 2009. The results suggest that the infection process has not come to a standstill yet. Up to 2012, 6 % of the trees remained symptomless, whereas mortality added up to 9 %. There were significant differences in ash dieback severity between the investigated provenances. Collar rot prevalence ranged from 19 to 59 % between study sites. Moreover, high spatial dependency of collar rot prevalence could be detected within sites. Collar rots were more abundant on trees of severe ash dieback intensity, but could also be detected on 15 % of otherwise healthy trees. Mycelium from collar rots could be identified by means of RFLP analyses and sequencing of the ITS region as most likely belonging to Armillaria gallica. The possible roles of Armillaria spp. and H. pseudoalbidus in collar rot formation are discussed.


Ash dieback Hymenoscyphus pseudoalbidus Fraxinus excelsior Armillaria gallica Collar rot Provenance trial 



Our special thanks go to Hermann Schott for his great commitment during the surveys every year. For supporting the surveys, we thank Katarina Töpfner, Daniel Zapf, Ricardo Rivero, Jürgen Wahl and Christa Wessel. Tangible support in laboratory work was provided by Gudrun Seiffert. Furthermore, we thank the involved forestry officers of the forest departments Rastatt, Emmendingen and Ortenaukreis, and anonymous reviewers for valuable comments on the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Bakys R, Vasaitis R, Barklund P, Ihrmark K, Stenlid J (2009) Investigations concerning the role of Chalara fraxinea in declining Fraxinus excelsior. Plant Pathol 58:284–292CrossRefGoogle Scholar
  2. Bakys R, Vasiliauskas A, Ihrmark K, Stenlid J, Menkis A, Vasaitis R (2011) Root rot, associated fungi and their impact on health condition of declining Fraxinus excelsior stands in Lithuania. Scand J For Res 26:128–135CrossRefGoogle Scholar
  3. Bakys R, Vasaitis R, Skovsgaard JP (2013) Patterns and severity of crown dieback in young even-aged stands of European ash (Fraxinus excelsior L.) in relation to stand density, bud flushing phenotype and season. Plant Protect Sci (in press)Google Scholar
  4. Cambardella CA, Moorman TB, Novak JM, Parkin TB, Karlen DL, Turco RF, Konopka AE (1994) Field-scale variability of soil properties in Central Iowa soils. Soil Sci Soc Am J 58:1501–1511CrossRefGoogle Scholar
  5. Cressie NAC (1991) Statistics for spatial data. Wiley, New YorkGoogle Scholar
  6. Dutter R (1985) Geostatistik. Teubner, StuttgartCrossRefGoogle Scholar
  7. Fink S (1999) Pathological and regenerative plant anatomy. Borntraeger, StuttgartGoogle Scholar
  8. Goudet M, Piou D (2012) La Chalarose du Frêne: que sait-on? Revue forestière française 64(1):27–40Google Scholar
  9. Gregory SC, Rishbeth J, Shaw CG III (1991) Pathogenicity and virulence. In: Kile GA (ed) Shaw III CG. Armillaria root disease, Agric. Handb. 691, Washington DC, pp 76–87Google Scholar
  10. Guillaumin JJ, Rykowski K (1980) Studium infekcji orzecha włoskiego (Juglans regia L.) przez opieńkę miodową [Armillaria mellea (Vahl) Quél.] w warunkach doświadczenai modelowego. Folia For Pol 24:191–213Google Scholar
  11. Husson C, Caël O, Grandjean JP, Nageleisen LM, Marçais B (2012) Occurrence of Hymenoscyphus pseudoalbidus on infected ash logs. Plant Pathol 61:889–895CrossRefGoogle Scholar
  12. Isaaks EH, Srivastava RM (1989) An introduction to applied geostatistics. Oxford university press, New YorkGoogle Scholar
  13. 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. Evol Appl 5:219–228CrossRefGoogle Scholar
  14. Kowalski T (2006) Chalara fraxinea sp. nov. associated with dieback of ash (Fraxinus excelsior) in Poland. For Pathol 36:264–270CrossRefGoogle Scholar
  15. Lochman J, Sery O, Mikes V (2004) The rapid identification of European Armillaria species from soil samples by nested PCR. FEMS Microbiol Lett 237:105–110PubMedCrossRefGoogle Scholar
  16. Lygis V, Vasiliauskas R, Stenlid J (2005) Wood-inhabiting fungi in stems of Fraxinus excelsior in declining ash stands of northern Lithuania, with particular reference to Armillaria cepistipes. Scand J For Res 20:337–346CrossRefGoogle Scholar
  17. Matheron G (1971) The theory of regionalized variables and their applications: Ecole des Mines. Fontainbleau, FranceGoogle Scholar
  18. McKinney LV, Nielsen LR, Hansen JK, Kjær ED (2011) Presence of natural genetic resistance in Fraxinus excelsior (Oleaceae) to Chalara fraxinea (Ascomycota): an emerging infectious disease. Heredity 106:788–797PubMedCrossRefGoogle Scholar
  19. Meisel JE, Turner MG (1998) Scale detection in real and artificial landscapes using semivariance analysis. Landsc Ecol 13(6):347–362CrossRefGoogle Scholar
  20. Metzler B, Enderle R, Karopka M, Töpfner K, Aldinger E (2012) Entwicklung des Eschentriebsterbens in einem Herkunftsversuch an verschiedenen Standorten in Süddeutschland. Ger J For Res (AFJZ) 183:168–180Google Scholar
  21. Metzler B, Baumann M, Baier U, Heydeck P, Bressem U, Lenz H (2013) Bundesweite zusammenstellung: handlungsempfehlungen beim eschentriebsterben. AFZ-Der Wald 68(5):17–20Google Scholar
  22. Orlikowski LB, Ptaszek M, Rodziewicz A, Nechwatal J, Thinggaard K, Jung T (2011) Phytophthora root and collar rot of mature Fraxinus excelsior in forest stands in Poland and Denmark. For Pathol 41:510–519CrossRefGoogle Scholar
  23. Pautasso M, Aas G, Queloz V, Holdenrieder O (2013) European ash (Fraxinus excelsior) dieback—a conservation biology challenge. Biol Conserv 158:37–49CrossRefGoogle Scholar
  24. Pliūra A, Lygis V, Suchockas V, Bartkevičius E (2011) Performance of twenty four European Fraxinus excelsior populations in three Lithuanian progeny trials with a special emphasis on resistance to Chalara fraxinea. Balt For 17(1):17–34Google Scholar
  25. Queloz V, Grünig CR, Berndt R, Kowalski T, Sieber TN, Holdenrieder O (2011) Cryptic speciation in Hymenoscyphus albidus. For Pathol 41:333–342CrossRefGoogle Scholar
  26. Rishbeth J (1985) Infection cycle of Armillaria and host response. Eur J For Pathol 15(5–6):332–341CrossRefGoogle Scholar
  27. Rutkewitz J (2012) Untersuchungen zur Ursache von Stammfußnekrosen an Eschen. Bachelor Thesis, University FreiburgGoogle Scholar
  28. Schumacher J, Kehr R, Leonhard S (2010) Mycological and histological investigations of Fraxinus excelsior nursery saplings naturally infected by Chalara fraxinea. For Pathol 40:419–429CrossRefGoogle Scholar
  29. Skovsgaard JP, Thomsen IM, Skovgaard IM, Martinussen T (2010) Associations between symptoms of dieback in even-aged stands of ash (Fraxinus excelsior L.). For Pathol 40:7–18CrossRefGoogle Scholar
  30. Stener LG (2013) Clonal differences in susceptibility to the dieback of Fraxinus excelsior. Scand J For Res 28(3):1–12. doi: 10.1080/02827581.2012.735699 CrossRefGoogle Scholar
  31. Thomas HE (1934) Studies on Armillaria mellea (Vahl) Quél., infection parasitism and host resistance. J Agric Res 48:187–218Google Scholar
  32. Wargo PM (1978) Judging vigour of deciduous hardwoods. Agric Info Bull 418:1–16Google Scholar
  33. Wargo PM, Harrington TC (1991) Host stress and susceptibility. In: Kile GA (ed) Shaw III CG. Armillaria root disease, Agric. Handb. 691, Washington DC, pp 88–101Google Scholar
  34. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. New York, pp 315–322Google Scholar
  35. Zhao Y, Hosoya T, Baral HO, Hosaka K, Kakishima M (2012) Hymenoscyphus pseudoalbidus, the correct name for Lambertella albida reported from Japan. Mycotaxon 122(1):25–41CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Rasmus Enderle
    • 1
    Email author
  • Franziska Peters
    • 1
  • Aikaterini Nakou
    • 1
  • Berthold Metzler
    • 1
  1. 1.Department Forest ProtectionForest Research Institute Baden-WuerttembergFreiburgGermany

Personalised recommendations