European Journal of Forest Research

, Volume 138, Issue 2, pp 263–274 | Cite as

First record of Entoleuca mammata in hybrid aspen plantations in hemiboreal Estonia and stand–environmental factors affecting its prevalence

  • Reimo LutterEmail author
  • Rein Drenkhan
  • Arvo Tullus
  • Katrin Jürimaa
  • Tea Tullus
  • Hardi Tullus
Original Paper


Entoleuca mammata [causing Hypoxylon canker (HC)] is one of the most serious pathogens that are colonising Populus species. The area of fast-growing hybrid aspen plantations has remarkably increased in northern Europe because of the high demand for woody biomass, but the prevalence of HC and the stand-related and environmental factors that favour its presence have rarely been monitored in such monocultural plantations. The presence of E. mammata in Estonia was proven by ITS sequence on hybrid aspen. Repeated monitoring after 4 years in 24 hybrid aspen plantations found that the share of visually damaged trees by HC increased from 0.6% (15-year-old trees) to 1.6% (19-year-old trees). The mortality rate of the infected trees during the 4 years was 100%. The probability of HC incidence was favoured by tree vigour and higher soil acidity. The higher susceptibility of more vigorous trees might be related to their trade-off between productivity and defence compounds. The share of trees with clear visual symptoms of HC can be considered marginal, but the aggressive nature of the pathogen suggests the need to extend the monitoring period, especially in recently thinned sites, and to expand the observations to native Populus tremula stands.


Populus Hypoxylon canker Invasive pathogen Molecular detection ITS sequence 



This work was supported by institutional research funding IUT (Grants IUT21-4 and IUT34-9), Estonian Research Council Grants PSG136 and PSG7 and the project P170053MIMK of the Estonian Ministry of Education and Research. We would also like to thank the anonymous reviewers for their valuable comments on the manuscript.


  1. Adamson K, Kalvina D, Drenkhan R, Gaitnieks T, Hanso M (2015) Diplodia sapinea is colonizing the native Scots pine (Pinus sylvestris) in the northern Baltics. Eur J Plant Pathol 143:343–350CrossRefGoogle Scholar
  2. Adamson K, Laas M, Drenkhan R, Hanso M (2018) Quarantine pathogen Lecanosticta acicola, observed at its jump from an exotic host to the native Scots pine in Estonia. Balt For 24:36–41Google Scholar
  3. Anderson GW, Anderson RL (1968) Relationship between density of quaking aspen and incidence of Hypoxylon canker. For Sci 14:107–112Google Scholar
  4. Bagga DK, Smalley EB (1973) The development of Hypoxylon canker of Populus tremuloides: role of interacting environmental factors. Phytopathology 64:658–662CrossRefGoogle Scholar
  5. Barker HL, Smith D, Stanosz G, Lindroth RL (2016) Host genetics and environment shape fungal pathogen incidence on a foundation forest tree species, Populus tremuloides. Can J For Res 46:1167–1172CrossRefGoogle Scholar
  6. Belanger RR, Manion PD, Griffin DH (1989) Hypoxylon mammatum ascospore infection of Populus tremuloides clones: effects of moisture stress in tissue culture. Phytopathology 79:315–317CrossRefGoogle Scholar
  7. Bier JL (1940) Studies in forest pathology. III. Hypoxylon canker on poplar. Technical Bulletin, Canadian Department of Agriculture No. 27, 40 ppGoogle Scholar
  8. Böhlenius H, Övergaard R, Asp H (2016) Grow growth response of hybrid aspen (Populus × wettsteinii) and Populus trichocarpa to different pH levels and nutrient availabilities. Can J For Res 46:1367–1374CrossRefGoogle Scholar
  9. Bruck RI, Manion PD (1980) Interacting environmental factors associated with the incidence of Hypoxylon canker on trembling aspen. Can J For Res 10:17–24CrossRefGoogle Scholar
  10. Bucciarelli B, Jung HG, Ostry ME, Anderson NA, Vance CP (1998) Wound response characteristics as related to phenylpropanoid enzyme activity and lignin deposition in resistant and susceptible Populus tremuloides inoculated with Entoleuca mammata (Hypoxylon mammatum). Can J Bot 76:1282–1289Google Scholar
  11. Chen F, Liu CJ, Tschaplinski TJ, Zhao N (2009) Genomics of secondary metabolism in populus: interactions with biotic and abiotic environments. Crit Rev Plant Sci 28:375–392CrossRefGoogle Scholar
  12. Christersson L (2010) Wood production potential in poplar plantations in Sweden. Biomass Bioenerg 34:1289–1299CrossRefGoogle Scholar
  13. Cole CT, Stevens MT, Anderson JE, Lindroth RL (2016) Heterozygosity, gender, and the growth-defense trade-off in quaking aspen. Oecologia 181:381–390CrossRefGoogle Scholar
  14. Dickmann DI, Kuzovkina J (2014) Poplars and willows of the world, with emphasis on silviculturally important species. In: Isebrands JG, Richardson J (eds) Poplars and willows: trees for society and the environment. FAO and CABI, London, pp 8–91CrossRefGoogle Scholar
  15. Donaldson JR, Kruger EL, Lindroth RL (2006) Competition- and resource-mediated tradeoffs between growth and defensive chemistry in trembling aspen (Populus tremuloides). New Phytol 169:561–570CrossRefGoogle Scholar
  16. Drenkhan R, Riit T, Adamson K, Hanso M (2016a) The earliest samples of Hymenoscyphus albidus vs. H. fraxineus in Estonian mycological herbaria. Mycol Prog 15:835–844CrossRefGoogle Scholar
  17. Drenkhan R, Tomešová-Haataja V, Fraser S, Bradshaw RE, Vahalík P, Mullett MS, Martín-García J, Bulman LS, Wingfield MJ, Kirisits T, Cech TL, Schmitz S, Baden R, Tubby K, Brown A, Georgieva M, Woods A, Ahumada R, Jankovský L, Thomsen IM, Adamson K, Marçais B, Vuorinen M, Tsopelas P, Koltay A, Halasz A, La Porta N, Anselmi N, Kiesnere R, Markovskaja S, Kačergius A, Papazova-Anakieva I, Risteski M, Sotirovski K, Lazarević J, Solheim H, Boroń P, Bragança H, Chira D, Musolin DL, Selikhovkin AV, Bulgakov TS, Keča N, Karadžić D, Galovic V, Pap P, Markovic M, Poljakovic Pajnik L, Vasic V, Ondrušková E, Piškur B, Sadiković D, Diez JJ, Solla A, Millberg H, Stenlid J, Angst A, Queloz V, Lehtijärvi A, Doğmuş-Lehtijärvi HT, Oskay F, Davydenko K, Meshkova V, Craig D, Woodward S, Barnes I (2016b) Global geographic distribution and host range of Dothistroma species: a comprehensive review. Forest Pathol 46:408–442CrossRefGoogle Scholar
  18. Drenkhan R, Adamson K, Drenkhan T, Agan A, Laas M (2017a) New problems in dendropathology—new and invasive pathogens. For Stud 67:50–71Google Scholar
  19. Drenkhan R, Solheim H, Bogacheva A, Riit T, Adamson K, Drenkhan T, Maaten T, Hietala AM (2017b) Hymenoscyphus fraxineus is a leaf pathogen of local Fraxinus species in the Russian Far East. Plant Pathol 66:490–500CrossRefGoogle Scholar
  20. Dudley MM, Burns KS, Jacobi WR (2015) Aspen mortality in the Colorado and southern Wyoming Rocky Mountains: extent, severity, and causal factors. For Ecol Manag 353:240–259CrossRefGoogle Scholar
  21. EPPO (2018) Hypoxylon mammatum. Data sheet on quarantine pests. Prepared by CABI and EPPO for the EU under the Contract 90/399003, 4 ppGoogle Scholar
  22. French JR, Hart JH (1978) Variation in resistance of trembling aspen to Hypoxylon mammatum identified by inoculating naturally occurring clones. Phytopathology 68:485–489CrossRefGoogle Scholar
  23. Frey BR, Lieffers VJ, Hogg EH, Landhäusser SM (2004) Predicting landscape patterns of aspen dieback: mechanisms and knowledge gaps. Can J For Res 34:1379–1390CrossRefGoogle Scholar
  24. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118CrossRefGoogle Scholar
  25. Griffin DH, Quinn KE, Gilbert GS, Wang CJK, Rosemarin S (1992) The role of ascospores and conidia as propagules in the disease cycle of Hypoxylon mammatum. Phytopathology 82:114–119CrossRefGoogle Scholar
  26. Hall TA (1999) BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid Sci 41:95–98Google Scholar
  27. Hanso M, Drenkhan R (2013) Simple visualization of climate change for improving the public perception in forest pathology. For Stud 58:37–45Google Scholar
  28. Hjelm K, Rytter L (2016) The influence of soil conditions, with focus on soil acidity, on the establishment of poplar (Populus spp.). New Forest 47:731–750CrossRefGoogle Scholar
  29. Hutchison LJ (1999) Wood-inhabiting microfungi isolated from Populus tremuloides from Alberta and northeastern British Columbia. Can J Bot 77:898–905Google Scholar
  30. Ilstedt B, Gullberg U (1993) Genetic variation in a 26-year old hybrid aspen trial in southern Sweden. Scand J For Res 8:185–192CrossRefGoogle Scholar
  31. Jaagus J, Mändla K (2014) Climate change scenarios for Estonia based on climate models from the IPCC Fourth Assessment report. Est J Earth Sci 63:166–180CrossRefGoogle Scholar
  32. Jegar M, Bragard C, Caffier D, Candresse T, Chatzivassiliou E, Dehnen-Schmutz K, Gilioli G, Gregoire JC, Miret JAJ, MacLeod A, Navajas Navarro M, Niere B, Parnell S, Potting R, Rafoss T, Rossi V, Urek G, Van Bruggen A, Van der Werf W, West J, Winter S, Boberg J, Gonthier P, Pautasso M (2017) Pest categorisation of Entoleuca mammata. EFSA J 15:4925Google Scholar
  33. Kasanen R, Hantula J, Kurkela T (2002) Neofabraea populi in hybrid aspen stands in southern Finland. Scand J For Res 17:391–397CrossRefGoogle Scholar
  34. Kasanen R, Hantula J, Ostry M, Pinon J, Kurkela T (2004) North American populations of Entoleuca mammata are genetically more variable than populations in Europe. Mycol Res 108:766–774CrossRefGoogle Scholar
  35. Lindroth RL, St Clair SB (2013) Adaptations of quaking aspen (Populus tremuloides Michx.) for defense against herbivores. For Ecol Manag 299:14–21CrossRefGoogle Scholar
  36. Lutter R, Tullus A, Kanal A, Tullus T, Tullus H (2016a) The impact of short-rotation hybrid aspen (Populus tremula L. × P. tremuloides Michx.) plantations on nutritional status of former arable soils. For Ecol Manag 362:184–193CrossRefGoogle Scholar
  37. Lutter R, Tullus A, Kanal A, Tullus T, Tullus H (2016b) The impact of former land-use type to above- and below-ground C and N pools in short-rotation hybrid aspen (Populus tremula L. × P. tremuloides Michx.) plantations in hemiboreal conditions. For Ecol Manag 378:79–90CrossRefGoogle Scholar
  38. Lutter R, Tullus A, Kanal A, Tullus T, Tullus H (2017) Above-ground growth and temporal plant-soil relations in midterm hybrid aspen (Populus tremula L. × P. tremuloides Michx.) plantations on former arable lands in hemiboreal Estonia. Scand J For Res 8:688–699CrossRefGoogle Scholar
  39. Mullett MS, Adamson K, Bragança H, Bulgakov TS, Georgieva M, Henriques J, Jürisoo L, Laas M, Drenkhan R (2018) New country and regional records of the pine needle blight pathogens Lecanosticta acicola, Dothistroma septosporum and Dothistroma pini. For Path 48:e12440CrossRefGoogle Scholar
  40. Osier TL, Lindroth RL (2006) Genotype and environment determine allocation to and costs of resistance in quaking aspen. Oecologia 148:293–303CrossRefGoogle Scholar
  41. Ostry ME (2013) Hypoxylon canker. In: Gonthier P, Nicolotti G (eds) Infectious forest diseases. CAB International United Kingdom, Wallingfork, pp 407–419CrossRefGoogle Scholar
  42. Ostry ME, Anderson NA (1979) Hypoxylon canker incidence on pruned and unpruned aspen. Can J For Res 9:290–291CrossRefGoogle Scholar
  43. Ostry ME, Anderson NA (1995) Infection of Populus tremuloldes by Hypoxylon mammatum ascospores through Saperda inornata gails. Can J For Res 25:813–816CrossRefGoogle Scholar
  44. Ostry ME, Anderson NA (2009) Genetics and ecology of the Entoleuca mammata-Populus pathosystem: implications for aspen improvement and management. For Ecol Manag 257:390–400CrossRefGoogle Scholar
  45. Ostry ME, LeBoldus JM (2016) Hypoxylon canker of aspen. In: Bergdahl AD, Hill A (eds) Diseases of trees in the great plains. U.S. Department of Agriculture, Forest Service Rocky Mountain Research Station, pp 97–99Google Scholar
  46. Pinon J (1979) The origin and the main characters of French isolates of Hypoxylon mammatum (Wahl) Miller. Eur J For Pathol 9:129–142CrossRefGoogle Scholar
  47. Pitt D, Weingartner D, Greifenhagen S (2001) Precommercial thinning of trembling aspen in northern Ontario: part 2—interactions with Hypoxylon canker. For Chron 77:902–910CrossRefGoogle Scholar
  48. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  49. Robinson KM, Ingvarsson PK, Jansson S, Albrectsen BR (2012) Genetic variation in functional traits influences arthropod community composition in aspen (Populus tremula L.). PLoS ONE 7:e37679CrossRefGoogle Scholar
  50. Rogers JD, Ju YM (1996) Entoleuca mammata Comb. Nov. for Hypoxylon mammatum and the genus Entoleuca. Mycotaxon 59:441–448Google Scholar
  51. Rytter L, Ingerslev M, Kilpeläinen A, Torssonen P, Lazdina D, Löf M, Madsen P, Muiste P, Stener LG (2016) Increased forest biomass production in the Nordic and Baltic countries – a review on current and future opportunities. Silva Fenn 50:1–33CrossRefGoogle Scholar
  52. Stanturf JA, van Oosten C, Netzer A, Coleman MD, Portwood CJ (2001) Ecology and silviculture of poplar plantations. In: Dickmann DI, Isebrands JG, Eckenwalder JE, Richardson J (eds) Poplar culture in North America. NRC Research Press, Ottawa, pp 155–206Google Scholar
  53. Stener LG, Karlsson B (2004) Improvement of Populus tremula × P. tremuloides by phenotypic selection and clonal testing. For Genet 11:13–27Google Scholar
  54. Stenlid J, Oliva J (2016) Phenotypic interactions between tree hosts and invasive forest pathogens in the light of globalization and climate change. Philos Trans R Soc B 371:20150455CrossRefGoogle Scholar
  55. Tarand A, Jaagus J, Kallis A (2013) Eesti kliima minevikus ja tänapäeval. Tartu Ülikooli Kirjastus, Tartu, p 631Google Scholar
  56. Tullus A, Tullus H, Vares A, Kanal A (2007) Early growth of hybrid aspen (Populus tremula L. × P. tremuloides Michx.) plantations on former agricultural lands in Estonia. For Ecol Manag 245:118–129CrossRefGoogle Scholar
  57. Tullus A, Rytter L, Tullus T, Weih M, Tullus H (2012) Short-rotation forestry with hybrid aspen (Populus tremula L. × P. tremuloides Michx.) in northern Europe. Scand J For Res 27:10–29CrossRefGoogle Scholar
  58. Tullus T, Tullus A, Roosaluste E, Lutter R, Tullus H (2015) Vascular plant and bryophyte flora in mid-term hybrid aspen plantations on abandoned agricultural land. Can J For Res 45:1183–1191CrossRefGoogle Scholar
  59. Wall A, Hytönen J (2005) Soil fertility of afforested arable land compared to continuously forested sites. Plant Soil 275:247–260CrossRefGoogle Scholar
  60. Weih M (2004) Intensive short rotation forestry in boreal climates: present and future perspectives. Can J For Res 34:369–1378CrossRefGoogle Scholar
  61. 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 sequencing guide to methods and applications. Academic Press, San Diego, pp 315–322Google Scholar
  62. Wingfield MJ, Brockerhoff EG, Wingfield BD, Slippers B (2015) Planted forest health: the need for a global strategy. Science 349:832–836CrossRefGoogle Scholar
  63. Wu HX (2018) Benefits and risks of using clones in forestry—a review. Scand J For Res. Google Scholar
  64. Zeps M, Adamovics A, Smilga J, Sisenis L (2016) Productivity and quality of hybrid aspen at the age of 18 years. Res Rural Dev 2:55–61Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Chair of Silviculture and Forest Ecology, Institute of Forestry and Rural EngineeringEstonian University of Life SciencesTartuEstonia
  2. 2.Department of Botany, Institute of Ecology and Earth SciencesUniversity of TartuTartuEstonia

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