Distribution of invasive pathogen of ash dieback disease Hymenoscyphus fraxineus in European part of Russia

As a result of the three-years long fixed-rout survey ash back disease caused by invasive ascomycete Hymenoscyphus fraxineus (T. Kowalski) Baral, Queloz, et Hosoya was detected on the territory of 31 subjects of the Russian Federation for the first time. This territory is one fifth part of European range of Fraxinus excelsior. Ash dieback appeared to be widespread pathology of ash at all examined regions of Russia. Genetic material of this pathogen was found in 163 from 178 analyzed samples with disease symptoms. Overall occurrence of the disease was 96,7%. Ash forests of Central and Southern Federal Districts were characterized by relatively low level of ash trees infestation (19,7 and 13,6% accordingly) in comparison with Northern Caucasus and Volga Districta were tee infestation has reached 27,9 and 29,0% accordingly. Levels of tree infestation of the most common ash species F. excelsior and F. pennsylvanica are not significantly different: 17,8 and 21,2% accordingly. The luck of information about this prominent pathology of ash can be partially explained by masking of its symptoms by damage of ash trees caused by emerald ash borer Agrilus planipennis Fairmaire, distributed on the territory of 20 European subjects of Federation and also by often ground fires. There is an urgent need of including this pathogen into the list of partially distributed quarantine organisms on the territory of the Eurasian economic unit. The main efforts should be concentrated on discovery of pathogen resistant genotypes and populations of ash for producing resistant plant forms, creation of genetic reservation zones and seed orchards.

1. Baranchikov Yu.N., Demidko D.A., Zvyagintsev V.B., Seraya L.G., Yaruk A.V. Na zapad poyekhal odin iz nikh, a na vostok – drugoy? Invaziynyye dal'nevostochnyye konsumenty yasenya v Yevropeyskoy chasti Rossii [One of them went West, and the other went East? Invasive Far Eastern consumers of ash in the European part of Russia]. Intensifikatsiya lesnogo khozyaystva Rossii: problemy i innovatsionnyye puti resheniya : mater. Vseros. konf. Krasnoyarsk: IL SO RAN, 2016, pp. 27–28. (In Russ.)

2. Biologicheskiye invazii v vodnykh i nazemnykh ekosistemakh. [Biological invasions in aquatic and terrestrial ecosystems]. Red. A.F. Alimov, N.G. Bogutskaya. M.–SPb., 2004. 436 p. (In Russ.)

3. Vasilyauskas A., Yuodval'kis A., Treygene A. Prichiny massovogo usykhaniya yasenya obyknovennogo v lesakh Litvy [Causes of mass dieback of the common ash in the forests of Lithuania]. Problemy lesnoy fitopatologii i mikologii: mater. V Mezhdunar. konf. M.: Institut lesovedeniya RAN. 2002, pp. 35–37. (In Russ.)

4. Davidenko Ye.V. Osnovnyye prichiny massovogo usykhaniya yasenya v tsentral'nykh i vostochnykh oblastyakh ukrainy [The main reasons for the mass drying up of ash in the central and eastern regions of Ukraine]. Izvestiya Sankt-Peterburgskoy lesotekhnicheskoy akademii, 2015, iss. 211, pp. 147–160. (In Russ.)

5. Zhigunov A.V., Semakova T.A., Shabunin D.A. Massovoye usykhaniye lesov na severo-zapade Rossii [Mass drying up of forests in the north-west of Russia]. Lesobiologicheskiye issledovaniya na severo-zapade tayezhnoy zony Rossii: itogi i perspektivy. Petrozavodsk: Izd-vo Karel'skogo nauchnogo tsentra RAN, 2007, pp. 42–52. (In Russ.)

6. Zvyagintsev V.B., Aliyev Kh.U., Seraya L.G., Baranchikov Yu.N. Sanitarnoye sostoyaniye posadok i yestestvennykh nasazhdeniy Fraxinus spp. na Sever-nom Kavkaze [Sanitary state of plantings and natural plantings of Fraxinus spp. in the North Caucasus]. Botanika v sovremennom mire: trudy XIV S"yezda Russkogo botanicheskogo obshchestva i konferentsii «Botanika v sovremen-nom mire» (g. Makhachkala, 18-23 iyunya 2018 g.). Makhachkala: ALEF, 2018, vol. 3, pp. 100–102. (In Russ.)

7. Zvyagintsev V.B., Baranov O.Yu., Panteleyev S.V. Rasprostranennost' nekroza vetvey yasenya, vyzvannogo invazivnym mikopatogenom Hymenoscyphus fraxineus Baral et al., v Podmoskov'ye i vdol' avtotrassy M1 [The prevalence of necrosis of ash branches caused by the invasive mycopathogen Hymenoscyphus fraxineus Baral et al. in the Moscow region and along the M1 highway]. Problemy lesnoy fitopatologii i mikologii: mater. 9-y Mezhdunar. Konf. / Red. V.G. Storozhenko, V.B. Zvyagintsev. Minsk: BGTU, 2015, pp. 87–89. (In Russ.)

8. Zvyagintsev V.B., Baranchikov Yu.N., Seraya L.G., Storozhenko V.G., Chebotarova V.V., Chebotarov P.A., Yaruk A.V. Osobennosti plodonosheniya Hymenoscyphus fraxineus v lesakh Minskoy vozvyshennosti i Srednerusskoy lesostepi [Features of fruiting Hymenoscyphus fraxineus in the forests of the Minsk Upland and the Central Russian forest-steppe]. Biologiya, sistematika i ekologiya gribov i lishaynikov v prirodnykh ekosistemakh i agrofitotsenozakh: mater. II Mezhdunar. konf. Minsk–Kamenyuki, 2016, pp. 100–104. (In Russ.)

9. Zvyagintsev V.B., Sazonov A.A. Novaya ugroza yasenevym lesam [A new threat to ash forests]. Lesnoye i okhotnich'ye khozyaystvo, 2006, no. 1, pp. 12–16. (In Russ.)

10. Zvyagintsev V.B., Sazonov A.A., Yaruk A.V., Avdeychik Ye.S. Osobennosti razvitiya i monitoring khalarovogo nekroza v yasenevykh nasazhdeniyakh i lesnykh pitomnikakh [Peculiarities of development and monitoring of halar necrosis in ash plantations and forest nurseries]. Monitoring i biologicheskiye metody kontrolya vrediteley i patogenov drevesnykh rasteniy: ot teorii k praktike: mater. Vseros. konf. Krasnoyarsk: IL SO RAN, 2016, pp. 83–84. (In Russ.)

11. Zvyagintsev V.B., Sharando A.V., Filippovich V.N. Rol' khalarovogo nekroza v protsesse degradatsii yasennikov Belarusi [The role of halar necrosis in the degradation of ash forests in Belarus]. Lesnoye i okhotnich'ye khozyaystvo, 2014, no. 9, pp. 8–11. (In Russ.)

12. Kolganikhina G.B., Panteleyev S.V. Pervoye obnaruzheniye opasnogo fitopatogennogo griba Hymenoscyphus fraxineus v Tellermanovskom lesu (yuzhnaya lesostep' yevropeyskoy chasti Rossii) [The first discovery of a dangerous phytopathogenic fungus Hymenoscyphus fraxineus in the Tellerman Forest (southern forest-steppe of the European part of Russia)]. Biologiya, sistematika i ekologiya gribov i lishaynikov v prirodnykh ekosistemakh i agrofitotsenozakh: mater. II Mezhdar. nauch. konf. Minsk. 2016, pp. 115–118. (In Russ.)

13. Musolin D.L., Bulgakov T.S., Selikhovkin A.V., Adamson K., Drenkkhan R., Vasaytis R. Dothistroma septosporum, D. pini i Hymenoscyphus fraxineus (Ascomycota) – patogeny drevesnykh rasteniy, vyzyvayushchiye ser'yeznuyu ozabochennost' v Yevrope [Dothistroma septosporum, D. pini and Hymenoscyphus fraxineus (Ascomycota) are tree plant pathogens of great concern in Europe]. VIII Chteniya pamyati Katayeva. Vrediteli i bolezni drevesnykh rasteniy Rossii: mater. Mezhdunar. konf. (Sankt-Peterburg, 18–20 noyabrya 2014 g.). SPb.: SPbGLTU. 2014, pp. 54–55. (In Russ.)

14. Padutov V.Ye., Baranov O.Yu., Voropayev Ye.V. Metody molekulyarnogeneticheskogo analiza [Methods of molecular genetic analysis.]. Minsk.: Yunipol, 2007. 176 p. (In Russ.)

15. Stanivuković Z., Dragan K., Milenković I. Prvi nalaz parazitske gl̂ive Hymenoscyphus fraxineus (T. Kowalski) Baral, Queloz, Hosoya na be-lom ǰasenu u Bosni i Khertsegovini [First finding of parasitic fungus Hymenoscyphus fraxineus (T. Kowalski) Baral, Queloz, Hosoya in forests of Bosnia and Herzegovina]. Šumarstvo, 2014, no. 3/4, pp. 19–34.

16. Shabunin D.A., Semakova T.A., Davidenko Ye.V., Vasaitis R.A. Usykhaniye yasenya na territorii pamyatnika prirody «Dudergofskiye vysoty», vyzvannoye gribom Hymenoscyphus pseudoalbidus, i morfologicheskiye osobennosti yego askospor [Drying of ash on the territory of the natural monument "Duderhof Heights", caused by the fungus Hymenoscyphus pseudoalbidus, and the morphological features of its ascospores]. Trudy Sankt-Peterburgskogo nauchno-issledovatel'skogo instituta lesnogo khozyaystva, 2012, no. 1–2, pp. 70–79. (In Russ.)

17. Shchurov V.I., Zamotaylov A.S. Pervyye nakhodki yasenevoy izumrudnoy uzkoteloy zlatki Agrilus planipennis Fairmaire, 1888 (Coleoptera: Buprestidae) v Krasnodarskom kraye [The first finds of the ash emerald borer Agrilus planipennis Fairmaire, 1888 (Coleoptera: Buprestidae) in the Krasnodar Territory]. Biologicheskoye raznoobraziye Kavkaza i yuga Rossii : mater. XXIV Mezhdunar. nauch. konf. (g. Magas, 17–20 noyabrya 2022 g.). Magas, Makhachkala: Izd-vo ALEF, 2022, рр. 558–565. (In Russ.)

18. Yaruk A.V., Zvyagintsev V.B., Smuraga V.S., Shegunova M.A. Dinamika formirovaniya plodovykh tel griba Hymenoscyphus fraxineus Baral et al. in vivo v usloviyakh Belarusi [he dynamics of the formation of fruiting bodies of the fungus Hymenoscyphus fraxineus Baral et al. in vivo in the conditions of Belarus]. Lesnoye khozyaystvo: tez. 82-y nauch.-tekhn. konf. prof.-prep. sostava, nauch. sotrudnikov i aspirantov (s mezhdunarodnym uchastiyem), Minsk, 01-14 fevralya 2018 g [Elektronnyy resurs]. Minsk: BGTU, 2018, pp. 116–117. URL: https://www.belstu.by/Portals/0/userfiles/37/0001-Tezisi-LHF-2018.pdf (In Russ.)

19. Adamčíková K., Kádasi Horáková M., Jankovský L., Havrdová L. Identification of Hymenoscyphus fraxineus, the causal agent of ash dieback in Slovakia. Biologia, 2015, vol. 70, pp. 559–564.

20. Avancée de la chalarose en France, situation début 2017 (Электронный документ). Ministère de l'Agriculture. 2017. URL : http://agriculture.gouv.fr/avanceede-la-chalarose-en-france-situation-debut-2017). Проверено 23.07.2018.

21. Barić L., Županić M., Pernek M., Diminić D. Prvi nalazi patogene gljive Chalara fraxinea u Hrvatskoj–novog uzročnika odumiranja jasena (Fraxinus spp.). Šumarski list, 2012, vol. 136, no. 9–10, pp. 461–468.

22. Barklund P. Recent disease problems in Swedish forests. Forest pathology research in the Nordic and Baltic countries 2005: Proceedings from the SNS meeting in Forest Pathology at Skogbrukets Kursinstitutt, Biri, Norway. 2005, pp. 28–31.

23. Cech T.L. Blattkrankheiten und vorzeitiger Laubfall – eine Folge des kühlfeuchten Sommers 2005. Aktuelle Schäden an Bäumen im Stadtbereich, 2005, vol. 34, p. 11.

24. Chalara fraxinea occurs in France (Электронный документ) // EPPO Reporting Service. 2010. URL: https://gd.eppo.int/media/data/reporting/rs-2010-02-en.pdf). Проверено 23.07.2018.

25. Chandelier A., Delhaye N., Helson M. First report of the ash dieback pathogen (anamorph Chalara fraxinea) on Fraxinus excelsior in Belgium. Plant Disease, 2011, vol. 95 (2), p. 220.

26. Cleary M.R., Arhipova N., Gaitnieks T., Stenlid J., Vasaitis R. Natural infection of Fraxinus excelsior seeds by Chalara fraxinea. Forest Pathology, 2011, vol. 43 (1), pp. 83–85.

27. Davydenko K., Vasaitis R., Stenlid J., Menkis A. Fungi in foliage and shoots of Fraxinus excelsior in eastern Ukraine: a first report on Hymenoscyphus pseudoalbidus. Forest Pathology, 2013, vol. 43 (6), pp. 462-467. (In Russ.)

28. Davydenko K., Skrylnyk Y., Borysenko O., Menkis A., Vysotska N., Meshkova V., Olson Å., Elfstrand M., Vasaitis R.. Invasion of emerald ash borer Agrilus planipennis and ash dieback pathogen Hymenoscyphus fraxineus in Ukraine – A concerted action. Forests, 2022, vol. 13 (5), p. 789. URL: https://doi.org/10.3390/f13050789 (In Russ.)

29. First report of Chalara fraxinea in Guernsey [Электронный документ] EPPO Reporting Service, 2012. URL: https://gd.eppo.int/media/data/reporting/rs-2012-11-en.pdf. Проверено 23.07.2018.

30. First report of Chalara fraxinea in the Netherlands (Электронный документ). EPPO Reporting Service, 2010. URL https://gd.eppo.int/reporting/article-608. Проверено 23.07.2018.

31. Gardes M., Bruns T.D. ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Molecular Ecology, 1993, vol. 2, no. 2, pp. 113–118.

32. Grosdidier M., Ioos R., Husson C., Cael O. Scordia T., Marçais B. Tracking the invasion: dispersal of Hymenoscyphus fraxineus airborne inoculum at different scales. FEMS Microbiology Ecology, 2018, vol. 94, iss. 5, 1. URL: https://doi.org/10.1093/femsec/fiy049

33. Gross A., Hosoya T., Queloz V. Population structure of the invasive forest pathogen Hymenoscyphus pseudoalbidus. Molecular Ecology, 2014, vol. 23, pp. 2943–2960.

34. Halmschlager E., Kirisits T. First report of the ash dieback pathogen Chalara fraxinea on Fraxinus excelsior in Austria. Plant Pathology, 2008, vol. 57, no. 6, p. 1177.

35. Hauptman T., Piškur B., Groot M., Ogris N., Ferlan M., Jurc D. Temperature effect on Chalara fraxinea: heat treatment of saplings as a possible disease control method. Forest Pathology, 2013, vol. 43, no. 5, pp. 360–370.

36. Heydeck P., Bemmann M., Kontzog H.-G. Triebsterben an Gemeiner Esche (Fraxinus excelsior) im nordostdeutschen Tiefland. Forst und Holz, 2005, vol. 60, pp. 505–506.

37. Hymenoscyphus fraxineus found for the first time in Emilia-Romagna region (IT) (Электронный документ). EPPO Reporting Service, 2015. URL: https://gd.eppo.int/reporting/article-5138. Проверено 23.07.2018.

38. Ioos R., Kowalski T., Husson C., Holdenrieder O. Rapid in planta detection of Chalara fraxinea by a real-time PCR assay using a dual-labelled probe. European Journal of Plant Pathology, 2009, vol. 125, no. 2, pp. 329–335.

39. Jankovský L., Holdenrieder O. Chalara fraxinea – ash dieback in the Czech Republic. Plant Protection Science, 2009, vol. 45, no. 2, pp. 74–78.

40. Johansson S.B.K., Vasaitis R., Ihrmark K., Barklund P., Stenlid J. Detection of Chalara fraxinea from tissue of Fraxinus excelsior using species-specific ITS primers. Forest Pathology, 2010, vol. 40 (2), pp. 111–115.

41. Kádasi-Horáková M., Adamčíková K., Pastirčáková K., Longauerová V., Maľová M. Natural infection of Fraxinus angustifolia by Hymenoscyphus fraxineus in Slovakia. Baltic Forestry, 2017, vol. 23(1), pp. 52–55.

42. Keča N., Kirisits T., Menkis A. First Report of the Invasive Ash Dieback Pathogen Hymenoscyphus fraxineus on Fraxinus excelsior and F. angustifolia in Serbia. Baltic Forestry, 2017, vol. 23, no. 1, pp. 56–59.

43. Kirisits T., Matlakova M., Mottinger-Kroupa S., Cech T.L., Halmschlager E. The current situation of ash dieback caused by Chalara fraxinea in Austria. SDÜ Faculty Forestry Journal, Serial A special issue, 2009, pp. 97–119.

44. Kowalski T. Chalara fraxinea sp. nov. associated with dieback of ash (Fraxinus excelsior) in Poland. Forest Pathology, 2006, vol. 36, no. 4, pp. 264–270.

45. Laiviņš M., Priede А., Puðpure I. Spread of Hymenoscyphus fraxineus in Latvia: Analysis based on Dynamics of Young Ash Stands. Proceedings of the Latvian academy of sciences. Section B, 2016, vol. 70, no. 3(702), pp. 124–130.

46. Luchi N., Ghelardini L., Santini A., Migliorini D., Capretti P. First record of ash dieback caused by Hymenoscyphus fraxineus on Fraxinus excelsior in the Apennines (Tuscany, Italy). Plant Disease, 2016, vol. 100(2), p. 535.

47. McCracken A.R., Douglas G.C., Ryan C., Destefanis, M., Cooke L.R. Ash dieback on island of Ireland. Dieback of European Ash (Fraxinus spp.): Consequences and Guidelines for Sustainable Management, The Report on European Cooperation in Science & Technology (COST) Action FP1 103 FRAXBACK. V.R. and E.R. Swedish University of Agricultural Sciences: 2017, pp. 125–139.

48. McKinney L.V., Nielsen L.R., Collinge D.B., Thomsen I.M., Hansen J.K., Kjær E.D. The ash dieback crisis: genetic variation in resistance can prove a long-term solution. Plant Pathology, 2014, vol. 63, pp. 485–499.

49. Meier F., Engesser R., Forster B., Odermatt O., Angst A. Protection des forêts – Vue d’ensemble 2007 (Электронный документ). Birmensdorf: Institut fédéral de recherches sur la forêt, la neige et le paysage WSL, 2008. URL: http://www.wsl.ch/forschung/forschungsunits/walddynamik/waldschutz/wsinfo/fsueb/fsub07f.pdf. Проверено 15.05.2018.

50. Milenković I., Jung T., Stanivuković Z., Karadžić D. First report of Hymenoscyphus fraxineus on Fraxinus excelsior in Montenegro. Forest Pathology, 2017, vol. 47, no. 5, p. e12359.

51. Musolin D.L., Selikhovkin A.V., Shabunin D.A., Zviagintsev V.B., Baranchikov Y.N. Between ash dieback and emerald ash borer: two Asian invaders in Russia and the future of ash in Europe. Baltic Forestry, 2017, vol. 23 (1), pp. 316–333. (In Russ.)

52. New data on quarantine pests and pests of the EPPO Alert List (Электронный документ). EPPO Reporting Service, 2014. URL: https://gd.eppo.int/reporting/article-2836. Проверено 15.05.2018.

53. Nielsen L.R., McKinney L.V., Hietala A.M., Kjær E.D. The susceptibility of Asian, European and North American Fraxinus species to the ash dieback pathogen Hymenoscyphus fraxineus reflects their phylogenetic history. Eur. J. Forest Res., 2017, vol. 136, pp. 59–73. URL https://doi.org/10.1007/s10342-016-1009-0

54. Ogris N., Hauptman T., Jurc D. Chalara fraxinea causing common ash dieback newly reported in Slovenia. Plant Pathology, 2009, vol. 58(6), p. 1173.

55. Ogris N., Hauptman T., Jurc D., Floreancig V., Marsich F., Montecchio L. First report of Chalara fraxinea on common ash in Italy. Plant Disease, 2010, 94, p. 133.

56. Orlova-Bienkowskaja M.J., Bienkowski A.O. Southern range expansion of the emerald ash borer, Agrilus planipennis, in Russia threatens ash and olive trees in the Middle East and Southern Europe. Forests, 2022, no. 13. 541 p. URL: https:// doi.org/10.3390/f13040541

57. Ploompuu T. Hüvasti, Eesti saarikud! Eesti Loodus, 2007, vol. 58 (8), pp. 14–15.

58. Rytkönen A., Lilja A., Drenkhan R., Gaitnieks T., Hantula J. First record of Chalara fraxinea in Finland and genetic variation among isolates sampled from Åland, mainland Finland, Estonia and Latvia. Forest Pathology, 2011, no. 41(3), pp. 169–174.

59. Santini A., Ghelardini L., De Pace C. et al. Biogeographical patterns and determinants of invasion by forest pathogens in Europe. New Phytologist, 2013, vol. 197, pp. 238–250.

60. Schumacher J., Wulf A., Leonhard S. Erster Nachweis von Chalara fraxinea T. Kowalski sp. nov. Deutschland – ein Verursacher neuartiger Schäden an Eschen. Nachrichtenblatt des Deutschen Pflanzenchutzdienstes (Braunschweig), 2007, vol. 59(6), pp. 121–123.

61. Skovsgaard J.P., Thomsen I.M., Skovgaard I.M., Martinussen T. Associations among symptoms of dieback in even‐aged stands of ash (Fraxinus excelsior L.). Forest Pathology, 2010, vol. 40, no. 1, pp. 7–18.

62. Solheim H. Dramatisk økning av askeskuddsjuke. Park & Аnlegg, 2009, vol. 8 (6), pp. 49–50.

63. Solheim H., Hietala A. M. Spread of Ash Dieback in Norway. Baltic Forestry, 2017, vol. 23, pp. 144–149.

64. Stroheker S., Queloz V., Nemesio-Gorriz M. First report of Hymenoscyphus fraxineus causing ash dieback in Spain. New Disease Reports. 2021 Oct; 44 (2): e12054.

65. Szabó I. A magas kôris Chalara fraxinea okozta hajtásés vesszôpusztulásának megjelenése magyarországon. Növényvédelem, 2008, vol. 44(9), pp. 444–446.

66. Talgø V., Sletten A., Brurberg M.B., Solheim H., Stensvand A. Chalara fraxinea isolated from diseased ash in Norway. Plant Disease, 2009, vol. 93(5). 548 p. URL: https://apsjournals.apsnet.org/doi/10.1094/PDIS-93-5-0548A.

67. Timmermann V., Borja I., Hietala A.M., Kirisits T., Soldheim S. Ash dieback: pathogen spread and diurnal patterns of ascospore dispersal, with special emphasis on Norway. Bulletin OEPP. 2011, vol. 41(1), pp. 14–20.

68. Tomiczek C.H., Cech T.L., Krehan H.A., Perny B.E., Steyrer G.O. Überblick über die Forstschutzsituation 2004 in Österreich. Forstschutz Aktuell, 2005, vol. 33, pp. 3–8.

69. Webber J., Hendry S. Rapid assessment of the need for a detailed pest risk analysis for Chalara fraxinea. Forest Research, UK. 2012. 15 p.

70. White T.J., Bruns T.D., Lee S.B., Taylor J.W. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications, 1990, pp. 315–322.

71. Zviagintsev V.B., Baranov O.Yu., Мelnik L.F. Pathogenic fungal diseases of branches of the ash in the drying out plantations in Belarus. Fungi and lichens in the Baltics and Beyond: XVIII Symposium of the Baltic Mycologists and Lichenologists Lithuania, Dubingiai, September 19–23, 2011, p. 21.