Biology:Didymascella thujina

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Short description: Species of fungus

Didymascella thujina
Infected leaflets.jpg
Didymascella thujina on western red cedar leaflets. Yellow leaflets are infected by the fungus, whereas green leaflets are uninfected. Apothecia are reddish brown to dark brown in colour. The mature apothecia have a loosened host epidermal layer and the immature apothecia have not yet broken through the host epidermal layer.
Scientific classification edit
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Leotiomycetes
Order: Helotiales
Family: Cenangiaceae
Genus: Didymascella
Species:
D. thujina
Binomial name
Didymascella thujina
(Durand) Maire 1927
Synonyms

Keithia thujina E.J. Durand 1913

Didymascella thujina is an ascomycete fungus in the family Helotiaceae. D. thujina causes cedar leaf blight (also known as Keithia blight or Keithia leaf blight), a leaf disease, on western red cedar (Thuja plicata) and white cedar (T. occidentalis).

Taxonomy and nomenclature

The common name of Keithia blight or Keithia leaf blight was derived from the first generic designation for the fungus and remained in use for many years. Pier Andrea Saccardo erected the genus Keithia in 1892 for this fungus,[1] and in 1903 the genus Didymascella for the same fungus was published as new, twice in the same month.[2][3] René Maire in 1905 rejected the generic designation of Didymascella when he followed a suggestion that it was synonymous with Keithia.[4] In 1927, Maire again took-up the genus Didymascella when it was reported that Keithia was previously used for a genus of flowering plants.[5] The name Keithia thujina remained in use in the literature until 1960 when R. G. Pawsey corrected the name to Didymascella thujina.[6]

Distribution

North America

Didymascella thujina occurs on western red cedar (T. plicata) and T. plicata var. atrovirens on the west coast of North America, where it is a significant leaf blight. It also occurs in eastern white cedar (T. occidentalis) in eastern North America, although its effect is insignificant.[7] It also occurs on some varieties of ornamental Thuja.[8] Didymascella thujina was found occurring on Port Orford cedar (Chamaecyparis lawsoniana) seedlings in a nursery in Washington (state) , US.[9]

Didymascella thujina was reported occurring on Atlantic white cedar (Chamaecyparis thyoides) in the eastern US,[10] however, this fungus, which occurs on Chamaecyparis species, has since been reclassified as Didymascella chamaecyparisii.[11][12]

The name Keithia thujina was used by Elias Judah Durand in 1908 for the first record of the disease in the United States on eastern white cedar.[13] Durand in 1913, further described and illustrated Keithia thujina that was collected from mature trees of eastern white cedar in Wisconsin.[14] Durand felt that the disease only affected the host when environmental conditions favoured epidemics.[14] G. C. Carew noted cedar leaf blight on eastern white cedar in Newfoundland.[15]

From 1912 to 1915 the disease was reported as seriously affecting western red cedar in the western U.S. state of Idaho where it was widely distributed throughout the range of T. plicata, including the adjoining areas of central Oregon, western Montana, and southern British Columbia (B.C.).[16] W. A. Porter studied the occurrence and distribution of the disease in western red cedar forests in B.C.[17][18][19] Later surveys extended the range of occurrence on western red cedar throughout its coastal and interior ranges in B.C.[20] and Alaska.[21] Cedar leaf blight has been found on both 1 and 2 year-old container-grown western red cedar seedlings in B.C. nurseries,[22] and on western red cedar in bare root nurseries in California .[23]

Europe

Cedar leaf blight has been introduced into Europe probably being carried on western red cedar imported from North America.[24] The first European records were from Ireland where the disease destroyed nursery-grown T. plicata.[25][26][27] Soon after its discovery in Ireland the disease was found to be well established in England[28][29][30] and Scotland.[31][32][33] Later, cedar leaf blight was reported from the Netherlands[34] [34] and Denmark, where it was so serious that nurseries curtailed or stopped growing cedar.[35][36] Cedar leaf blight continued to spread to Norway,[37] Belgium,[38] France,[39] Switzerland,[24] Italy,[40] Germany,[8] Poland,[41] Spain,[42] Austria,[43] Slovakia,[44] and the Czech Republic.[45] In Germany, Peter Burmeister reported that D. thujina likely occurred on Chamaecyparis lawsoniana, but he was unable to confirm this.[8]

Other areas of the world

There is the risk of cedar leaf blight becoming established wherever Thuja species are introduced and grown, as is evidenced by its occurrence on Thuja species introduced into Europe. Thuja has been introduced to other countries, including India, Australia, Chile and Ukraine,[46] but at present D. thujina has not been reported as a disease.

Ecology

Most ecological observations on cedar leaf blight damage are its occurrence on western red cedar (Thuja plicata), which is the most susceptible host.[18][20][30][47] Cedar leaf blight is favoured by conditions of prolonged foliage wetness and where air movement is restricted, e.g., high seedling density in a nursery or seedlings over-grown by ground cover plants in reforestation sites.[48][49][50] Individual western red cedar trees vary in susceptibility to the disease and although all age classes are affected, seedlings and young trees suffer the most.[7][9][51][52][53] A physiological change in western red cedar appears to account for an increase in blight resistance for certain individual trees when they reach 4 or 5 years of age.[54] The use of degree days to establish biological events for Didymascella thujina, a foliar fungal leaf blight of Thuja plicata seedlings.[55] The consequence of cedar leaf blight infection of the foliage of mature cedar trees (greater than 50 years of age) is unknown, and given that mortality is rare, loss of incremental growth may be a chief result. However, cedar leaf blight may be a pioneering fungal pathogen that induces some stress on the host tree allowing a further succession of biotic or abiotic problems.

Epidemiology and symptoms

Germinating ascospores cause very early symptoms on mature foliage that appear as several small cream-coloured spots on the upper surface of individual cedar leaflets. These spots later develop into lesions, which coalesce as a discreet spot, but the entire leaf becomes brown contrasting with adjacent green, healthy leaves. Infected leaflets are scattered over a branch, but they only occur on the previous year's leaflets, and not the current year's growth. Mycelial growth occurs within individual leaflets and once sufficient growing degree days have accumulated under suitable environmental conditions, apothecia are formed.[12][56] A cross section of leaflet through an apothecium shows that the apothecium is initially covered by the leaf cuticle and a one-cell thick epidermal layer which is golden brown to brown in colour. The apothecium is raised slightly above the surrounding leaf tissue. When the epidermal covering breaks three quarters around the circumference of the apothecium, it lifts up as a scale, exposing the hymenial layer. As the exposed apothecium matures, it changes from golden brown to dark brown in colour. When moist, the cushion-like hymenial layer of the apothecium is golden-olive. At this point ascospores are released. When dry, apothecia appear much darker and the epidermal scale often folds back over the apothecium, and no further ascospores are released. Under repeated episodes of wetting and drying for up to week, ascospore release can occur. Discharged ascospores are covered with a sticky, mucilaginous coating that attach the ascospores to any type of surface.[12] Where ascospores stick to the host material, they produce a germ tube and directly penetrate the epidermis, and not through stomata. Affected leaflets often remain on the tree, weathering to a grey colour with dark cavities where spent apothecia have either shrivelled or fallen out. No anamorphic stage is known.

Diagnostic methods

An electrophoretic technique has been used to analyzed the proteins of disease-free and D. thujina-infected leaves of T. plicata, revealing differences in several protein bands. This suggests that distinct proteins of D. thujina origin can be identified by the SDS-PAGE technique.[57]

Control

The same conditions that make nursery production of seedlings successful — high densities, favourable temperatures and moisture, and intensive crop-management techniques — are also ideal for the cedar leaf blight fungus. Healthy trees result when pest management is integrated with other aspects of nursery culture throughout the crop cycle.

Chemical

Numerous studies were made with fungicides to control cedar leaf blight on nursery seedlings.[16][24][58][59][60][61][62][63][64][65][66][67][68][69] Very few fungicides were found to be effective, but of those that were effective, many and frequent applications were required for control of the disease in seedling nursery settings. If control of cedar leaf blight is through fungicides only, they must be applied early and through the length of the growing season of 1-year old seedling, and throughout the full growing season of 2-year old seedlings. The effect of the fungicide is to damage ascospores that are on the leaflet surface that drift into the growing areas during a spring release period and to damage the newly forming fruiting bodies and their ascospores forming in the fall on the foliage.

Growth conditions

Various modifications of cultural practices have been tried for the control of cedar leaf blight. In Britain, western red cedar seedlings were grown in nurseries isolated from known sources of inoculum, but the results were inconclusive.[70] Another suggestion was to grow Thuja in isolated nurseries.[71] Thuja would be raised from seed at isolated nurseries with a periodic clearance of all cedar stock before resowing. This was partly successful, but some outbreaks of cedar leaf blight still occurred.[65] Growing bareroot nursery or transplant cedar at reduced densities (seedlings per unit area), e.g., to decrease within canopy humidity, has provided some measure of blight control.[72][73][74] Growing cedar as a mixture with other species, both in seed and transplant beds, has also given some control of the disease.[24]

Older infected cedar stock or infected cedar trees surrounding a nursery can provide inoculum and the ascospores can travel through the air. Airborne ascospores can be kept out of cedar-rearing greenhouses by keeping a roof and side walls in place until after the spring ascospore release period. This practice directly prevents ascospores from coming in contact with the cedar crop.

Through the summer months (in the northern hemisphere) of July, August and September, when climatic conditions are warmer and drier, circulating dry air through the crop will decrease the time that foliage remains wet. As the crop matures, foliage density increases and moisture is retained on leaf surfaces, especially the lower branches. Free water is required for the germination and infection of leaves by D. thujina. Foliage wetness can be decreased by separating the growing containers, thus allowing a more efficient drying-out between waterings.

From October through to the end of November (in the northern hemisphere), air should be allowed to circulate through the crop, and where possible, seedlings should be protected from the rain. If infection has occurred fruiting bodies can form and disease spread will be encouraged by the presence of moisture on the infected foliage.

Seedlings held over for either growth for another year into the spring are particularly susceptible to cedar leaf blight infection and expression. Held-over seedlings must be protected throughout the previous growing season, or disease expression will occur early in the spring. The first signs of the disease are often subtle and overlooked in the early spring and the disease can easily spread. By applying fungicides to the crop in the first growing season and continuing through the second growing season, a disease-free crop of 2+0 western red cedar can be produced.

Resistance to cedar leaf blight

Resistance to cedar leaf blight is known in Thuja. B. Søegaard inoculated both cuttings from a mature western red cedar tree and seedlings from the same tree, and showed that the cuttings were more resistant than the seedlings.[54][75][76] Søegaard also determined that resistance is the result of a recessive gene in T plicata. Crossing T. plicata with a Japanese species Thuja standishii, where resistance was dominant, resulted in a 1:1 ratio of resistant to susceptible offspring.[75] Søegaard suggested that cuttings could be produced from such hybrids.[76]

Porter, in attempting to explain the variation in blight severity in British Columbia, collected T plicata cuttings and inoculated some in the field and others in the laboratory. Regardless of host origin, inoculation site or technique, no resistance was found. Based on these results Porter concluded that microclimate is mainly responsible for differences in blight severity.[17]

Variation in cedar leaf blight resistance of western red cedar populations is known to be related to seed origin. Trees from milder and wetter ecosystems are more resistant to cedar leaf blight when planted in similar areas, and also, low-elevation populations exhibit the most resistance to cedar leaf blight, while high-elevation populations show the least.[75]

Disease impact

In North America western red cedar seedling mortality rates of up to 97% have been recorded, resulting in large economic losses to growers. Seedling mortality of nursery grown seedlings also occurs when they are planted into reforestation areas. The disease greatly reduces the number of plants suitable for planting. Harry H. Kope and D. Trotter have shown in younger (<4 years of age) western red cedar trees that growth and yield can be affected by cedar leaf blight.[76] A decrease of 30% in stem diameter, 50% in shoot biomass and 35% in roots biomass has been recorded for blight affected trees as compared to unblighted trees in reforestation sites.[55] This decrease in tree growth and yield can contribute to additional years of tree maintenance in reforestation sites, before the trees can compete with other plants and that the site is considered adequately reforested.[56]

Cedar leaf blight disease intensity is projected to increase under the moderate temperature and precipitation increases that climate models have forecast for the 2020s in coastal North America. To avoid significant mortality and growth reduction of planted western red cedar, it is recommended that reforestation efforts deploy adapted or disease resistant western red cedar seedlots in high risk environments common to coastal North America.[77]

References

  1. ↑ Saccardo PA, 1892. Sylloge Fungorum, 10: 49-50.
  2. ↑ 2Maire R, Dumee P, Lutz L, 1901. Prodrome d’une flore mycologique de la Corse. Bulletin de la Société Botanique de France. 1 (series 4): 179-247.
  3. ↑ Maire R, Saccardo PA, 1903. Sur un nouveau genre de Phacidiacées. Annales Mycologici, 1; 417-419.
  4. ↑ Maire R, 1905. Notes sur quelques champignons nouveaux ou peu connus. Bulletin de la Société Mycologique de France, 21 : 137-167.
  5. ↑ Maire R, 1927. Bulletin de la Société d’Histoire Naturelle Afrique du Nord, 18 : 117.
  6. ↑ Pawsey RG, 1960. An investigation into Keithia disease of Thuja plicata. Forestry, 33: 174-186.
  7. ↑ 7.0 7.1 Sinclair, Wayne A.; Lyon, Howard H. (2005). Diseases of Trees and Shrubs (Second ed.). Ithaca: Cornell University Press. p. 60. ISBN 978-0-8014-4371-8. 
  8. ↑ 8.0 8.1 8.2 Burmeister P, 1966. Beobachtangen über einige wichtige Pilzkrankheiten an Zierkoniferen im Oldenburgischen Baumschulgebiet. In: de Haas PG, ed. Die Gartenbaumwissenschaft, Bayerischer Landwirtschaftsverlag, Munich, 469-506.
  9. ↑ 9.0 9.1 Boyce JS, 1961. Forest Pathology. McGraw-Hill Book Company, Toronto.
  10. ↑ Adams JF, 1918. Keithia on Chamaecyparis thyoides. Torreya, 18: 157-160.
  11. ↑ Pantidou ME, Korf, RP, 1954. A revision of the genus Keithia. Mycologia, 46: 386-388.
  12. ↑ 12.0 12.1 12.2 Kope HH, 2000. Fungi Canadenses No. 343 Didymascella thujina. Canadian Journal of Plant Pathology, 22: 407-409.
  13. ↑ Durand EJ, 1909. Transactions of the Wisconsin Academy of Sciences, Arts and Letters, 16; 756.
  14. ↑ 14.0 14.1 Durand EJ, 1913. The genus Keithia. Mycologia, 5: 6-11.
  15. ↑ Carew GC. 1988. A new needle blight disease of Eastern white cedar in Newfoundland. Woody Points Newsletter, 18: 9-10.
  16. ↑ 16.0 16.1 Weir JR, 1916. Keithia thujina. The cause of a serious leaf disease of Western red cedar. Phytopathology, 6: 360-363.
  17. ↑ 17.0 17.1 Porter WA, 1957. Biological studies on Western red cedar blight caused by Keithia thujina Durand. Canada Department of Agriculture, Forest Biology Division, Interim Report, Victoria, B.C., 25.
  18. ↑ 18.0 18.1 Wood C, 1986. Distribution maps of common tree diseases in British Columbia. Information Report, BC-X-281, Victoria, B.C.
  19. ↑ Finck KE, Humphreys P, Hawkins GV, 1989. Field guide to pests of managed forests of British Columbia. Joint Publication. No. 16. FRDA I.
  20. ↑ 20.0 20.1 Foster RE, Wallis GW, 1969. Common tree diseases of British Columbia. Forestry Branch Publications. No. 1245. Department of Fisheries and Forestry, Victoria, B.C., Canada.
  21. ↑ Anonymous, 1985. Insects and diseases of Alaskan forests. Alaska Region Report Number 181. USDA Forest Service.
  22. ↑ Dennis J, Sutherland JR, 1989. Keithia Blight. Seed and Seedling Extension Topics. No. 2:1 Province of British Columbia, Ministry of Forests, Victoria, B.C., 15
  23. ↑ Frankel SJ, 1990. Evaluation of fungicides to control cedar leaf blight on Western red cedar at Humboldt nursery. Forest Pest Management Report. No. 90-01. USDA Forest Service, Pacific Southwest Region, 4.
  24. ↑ 24.0 24.1 24.2 24.3 Peace JR, 1955. Observations on Keithia thujina and on the possibility of avoiding attack by growing Thuja in isolated nurseries. Report on Forest Research. Forestry Commission, London, 144-148.
  25. ↑ Pethybridge GH, 1919. A destructive disease of seedling trees of Thuja gigantea Nutt. Quarterly Journal of Forestry, 13: 93-97.
  26. ↑ Forbes AC, 1920. Occurrence of Keithia thujina in Ireland. The Gardeners’ Chronicles, 68: 228-229.
  27. ↑ Forbes AC, 1921. Keithia thujina in Ireland. Quarterly Journal of Forestry, 15: 73-75.
  28. ↑ Loder EG, 1919. Keithia thujina at Leonardslee. Quarterly Journal of Forestry, 13: 287.
  29. ↑ Miles AC, 1922. Keithia on Thuya plicata. The Gardeners’ Chronicles, 73: 353.
  30. ↑ 30.0 30.1 Boyce JS, 1927. Observations on forest pathology in Great Britain and Denmark. Phytopathology, 17: 1-18.
  31. ↑ Alcock NL, 1928. Keithia thujina Durand: A disease of nursery seedlings of Thuja plicata, Scottish Forestry Journal, 42: 77-79.
  32. ↑ Laing EV, 1929. Notes from the Forestry Department, Aberdeen University. Scottish Forestry Journal, 43: 48-51.
  33. ↑ Wilson M, 1937. The occurrence of Keithia tsugae in Scotland. Scottish Forestry Journal, 51: 46-47.
  34. ↑ Poetern van N, 1931. Verslag over de werksamheden van den plantenziektenkundigen dienst in het jaar 1930. Meded. Plantenziektenkdg, Dienst. Wageningen, No. 64.
  35. ↑ Buchwald NF, 1936. En ny svampesygdom i Danmark. Didymascella thujina paa Thuja plicata. Dansk Skovforenings Tidsskrift, 21: 51-59.
  36. ↑ Ferdinandsen NC, Jorgensen CA, 1938. Skovtraernes Sygdomme, Copenhagen, 181-182.
  37. ↑ Jorstad J, Roll-Hasen F, 1943. Melding om sykdommer pa skogtraes i arene. 1936 - 1941, National Samlinge Rikstrykkeri, Oslo, 25.
  38. ↑ Boudru M, 1945. La rouille des aiguilles du Thuja géant (Thuja plicata Don.). Bulletin de la Société royale forestiere de Belgique, 52 : 69-75.
  39. ↑ Anonymous, 1953. Notes phytosanitaires. Evolution des maladies des plantes en 1951. Annales de L’institut national de recherche agronomique, serie C (Annales des Épiphyties) : 511-515.
  40. ↑ Vegni G, Ferro G, 1964. Control of Didymascella (Keithia) thujina dieback of Thuja with zineb. Rivista di Patologia Vegetale, Pavia (Ser. III) 4: 171-176.
  41. ↑ Benben K, 1969. Studies on diseases of North American trees acclimatized in Poland. Prace Instytutow I Laboratoriow Badawczych Przemyslu Spozywczego No 373/375: 129-143.
  42. ↑ Fernandez-Magan FJ, 1974. New attacks on Thuja in Galician nurseries. Anales del Instituto Nacional de Investigaciones Agrarias, Recursos Naturales, 1 : 187-199.
  43. ↑ Pardatscher G, 1977. Planzenschutz bei Gartenkoniferen. (Plant protection with garden conifers). Besseres Obst, 22 : 29-30 + 45-46.
  44. ↑ Holubcik M, 1978. Moznosti sl’achtenia lesnych drevin na odolnost’ proti biotickym a abiotickym cinitel’om. (Possibilities in the breeding of forest trees for resistance to biotic and abiotic factors). Vedecke prace vyskumneho ustavu lesneho hospodarstva vo zvolene, 26: 213-232.
  45. ↑ Prihoda A, 1986. Zasychani vetvi zeravu (Thuja). (Die-back of arbor-vitae (Thuja ) branches.) Sbornik UVTIZ, Zahradnictvi, 13: 307-315.
  46. ↑ Minter DW, 1997. IMI Descriptions of Fungi and Bacteria No. 1334, Didymascella thujina.
  47. ↑ Lainer L, 1964. Une maladie des jeunes plants de Thuyas en pepinieres. Phytoma 155: 23-27.
  48. ↑ Kope HH, Sutherland J, 1994. Keithia blight: A review of the disease, and research on container-grown, Western redcedar in British Columbia, Canada. In Proceedings of the second meeting of IUFRO Working Party, S2.07-09 (Diseases and Insects of nurseries).
  49. ↑ Kope HH, Sutherland J, Trotter D, 1996. Influence of cavity size, seedling growing density and fungicide applications on Keithia blight of western redcedar seedling growth and field performance. New Forests, 11: 137-147.
  50. ↑ Rankin WH, 1927. Manual of Tree Diseases. New York, NY: MacMillan Co.
  51. ↑ Phillips DH, Burdekin DA, 1982. Diseases of Forest and Ornamental Trees. London: The MacMillan Press Ltd.
  52. ↑ Kope HH, Dennis J, 1992. Keithia blight on Western Red Cedar nursery seedlings. Seed and Seedling Extension Topics. No. 5:(l); Province of British Columbia, Ministry of Forests, Victoria, B.C. 11.
  53. ↑ Søegaard B, 1969. Resistance studies in Thuja. Det Forstlige Forsogsvoesen i Danmark. No. 245, 31: 287-396.
  54. ↑ 54.0 54.1 Søegaard B, 1956. Leaf blight resistance in Thuja. Yearbook 1956. Royal Veterinary and Agricultural College, Copenhagen, Denmark. 30-48.
  55. ↑ In: Proceedings of the 7th International Congress of Plant Pathology, August, 9-16, 1998, Edinburgh, Scotland.
  56. ↑ 56.0 56.1 Kope HH, Ekramoddoullah AKM, Sutherland JR, 1998. Analysis of proteins of disease-free and Didymascella thujina-infected leaves of western red-cedar (Thuja plicata). Plant Disease, 82:210-212.
  57. ↑ Pawsey RG, 1962b. Rotation sowing of Thuja in selected nurseries to avoid infection by Keithia thujina. Quarterly Journal of Forestry, 52: 206-210.
  58. ↑ Burdekin DA, 1969. Needle blight of Western Red Cedar caused by Didymascella thujina. Report on Forestry Research. Forestry Commission, London, pp. 108.
  59. ↑ Pawsey RG, 1964. Cycloheximide fungicide trials against Didymascella thujina on Western red cedar, Thuja plicata. Report on Forest Research. Forestry Commission, London, 141-150.
  60. ↑ Phillips DH, 1965. Needle blight (Didymascella thujina [Dur.] Maire, syn. Keithia thujina Dur.) of Western Red Cedar (Thuja plicata). Report on Forest Research. Forestry Commission, London, 63.
  61. ↑ Phillips DH, 1966. Needle blight (Didymascella thujina [Dur.] Maire, Keithia thujina Dur.) of Thuja. Report on Forest Research. Forestry Commission, London, 73.
  62. ↑ Burdekin DA, 1968. Needle blight of Western Red Cedar caused by Didymascella thujina. Report on Forestry Research. Forestry Commission, London, pp. 109.
  63. ↑ Phillips DH, 1967. Needle blight of Western Red Cedar caused by Didymascella thujina (Keithia thujina). Report on Forestry Research. Forestry Commission, London, 100.
  64. ↑ Burdekin DA, Phillips DH, 1971. Chemical control of Didymascella thujina on Western red cedar in forest nurseries. Annals of Applied Biology, 67:131-136.
  65. ↑ 65.0 65.1 Boudier B, 1983. Didymascella thujina principal ennemi du Thuya dans l'ouest de la France. Phytoma - Defense des cultures, novembre, 51-56.
  66. ↑ Frankel SJ, 1991. Timing and applications of triadimefon (Bayleton) needed for control of cedar leaf blight on Western red cedar at Humboldt nursery. Forest Pest Management Report. No. 91-01. USDA Forest Service, Pacific Southwest Region. 4.
  67. ↑ Frankel SJ, 1992. Additional studies on rate and number of Triadimefon (Bayleton 25% WP) applications needed for control of cedar leaf blight on Western red cedar at Humboldt nursery. Forest Pest Management Report. No. 92-02. USDA Forest Service, Pacific Southwest Region. 5.
  68. ↑ Kope HH, Trotter D, 1998a. Evaluation of mancozeb and propiconazole to control Keithia leaf blight of container-grown western red cedar. The Forestry Chronicle, 74: 583-587.
  69. ↑ Peace JR, 1958. The raising of Thuja in isolated nurseries to avoid infection by Keithia thujina. Scottish Forestry, 12: 7-10.
  70. ↑ Pawsey RG, 1962a. Control of Keithia thujina Durand by cycloheximide and derivatives. Nature, 194: 109.
  71. ↑ Keatinge G, 1948. Keithia thujina. Quarterly Journal of Forestry, 42: 199-200.
  72. ↑ Evans JDD, 1950. Red cedar and European larch in mixture. Quarterly Journal of Forestry, 44: 137-142.
  73. ↑ Penistan MJ, 1966. Rubbish to seed stand (Western red cedar). Quarterly Journal of Forestry, 60: 237.
  74. ↑ Søegaard B, 1954. Resistance tests against infection by Didymascella thujina (Durand) Maire in Thuja plicata Lamb. 8th International Congress in Botany, Paris, 120-122.
  75. ↑ 75.0 75.1 75.2 Russell J, Kope HH, Ades P, Collinson, H. 2007. Variation in cedar leaf blight (Didymascella thujina) resistance of western red cedar (Thuja plicata). Canadian Journal of Forest Research, 37: 1978-1986.
  76. ↑ 76.0 76.1 76.2 Kope HH, Trotter D, 1998b. The use of degree days to establish biological events for Didymascella thujina, a foliar fungal leaf blight of Thuja plicata seedlings. In: Proceedings of the 7th International Congress of Plant Pathology, August, 9-16, 1998, Edinburgh, Scotland.
  77. ↑ Gray LK, Russell JH, Yanchuk AD, Hawkins BJ, 2013. Predicting the risk of cedar leaf blight (Didymascella thujina) in British Columbia under future climate change. Agriculture and Forest Meteorology, 180: 152-163.

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