Silver-Leaf Disease: An Epidemic in Northern Birch

In Europe, as Percival indicated ​[25], decline and dieback diseases of trees have been perplexing. However, in 1902, he successfully inoculated plum trees with pieces of tissue taken from fungal basidiocarps that grew on root segments of a diseased plum tree. Soon thereafter, Pickering ​[26, 27]​ and Brooks ​[4–6]​ corroborated Percival’s work, and thereby proved that Chondrostereum purpureum was pathogenic to plum trees. By 1911, Brooks ​[5]​ reached the conclusion, “. . . that this fungus is the agent chiefly responsible for the havoc wrought by the malady in the fruit-growing districts of this country [England].”  

At the start, great emphasis was placed on protecting food production, and so Brooks with others continued to inoculate fruit trees and study disease progress ​[7–10]​. Thus, C. purpureum gained a reputation for causing silver-leaf disease in rosaceous fruit trees ​[5–7, 16, 17, 25–27]​. Fresh wounds made mostly from pruning and grafting set the stage for infection and death that frequently reached epidemic proportions ​[6, 7, 10]​.

The presence of C. purpureum (Figs. 1 & 2) on other broad-leaved trees was not entirely overlooked. In 1911, Brooks ​[5]​ stated, “On portions of the stool of the silvered Sycamore tree to which reference has previously been made, Stereum purpureum was growing, but in this connection it should be stated that similar stools of Birch close by and on which this fungus was also found bore shoots with normal foliage.” Brooks ​[6]​ then successfully inoculated laburnums with fruiting body tissue derived from a diseased plum, and these plants later produced silvered foliage. By this time, silvered leaves were a hallmark of this disease. Additional inoculations were successfully made on plum trees, and basidiocarps were recorded on the dead wood/bark of “Plum, Apple, Red Current, Willow . . ., Poplar . . ., Birch, Beech, Sycamore and Laburnum” ​[6]​. Later, Brooks and Bailey ​[7]​ observed silvered shoots “. . . arising from stools of poplar trees and on each of the five stumps from which such shoots arose, Stereum purpureum was growing abundantly. These stools formed part of a row of poplars, the intact trees of which showed normal foliage.” In 1919, further inoculations included, in addition to plum varieties, cherry, red currant, horse chestnut, mock orange, and gooseberry ​[7]​. All of these plants exhibited silvered foliage. Plants that likewise were successfully inoculated, but failed to show silvered leaves, were black currant, beech, elm, sycamore, cherry laurel, and Portugal laurel. Brooks and Storey ​[10]​ observed “sucker” shoots with silvered leaves from stumps of elm and hawthorn, and as well, they observed beech and birch trees apparently killed by S. purpureum. Silver-leaf symptoms, except in hawthorn and rosaceous species, failed to develop in these trees ​[10]​. By 1953 in Denmark ​[13]​, the host range included ash, walnut, and many additional shrubs. (The host substrates mentioned for C. purpureum are informed by some of the early literature and are not complete.)              

Fig. 1. Chondrostereum purpureum growing on a Populus x candicans (Aurora) stump on the Bath University campus, Bath, UK, December 1991.
Fig. 2. Effused-reflexed fruiting bodies of C. purpureum on aspen logging debris at the Lakehead Univ. woodlot, Sept. 1993.

Around the turn of the 19th century in North America, birch dieback disease was reported ​[2]​ to be killing thousands of trees in towns and cities in Canada and the United States from the Great Lakes to the eastern seaboard. Initially, the deaths were confined largely to cut-leaf birch, Betula alba. Later, Swaine and Maheux in 1918, reported dying in stands of yellow and white birch in the Ottawa watershed [fide Balch and Prebble ​[2]​]. In both situations, the native bronze birch borer Agrilus anxius was considered the primary agent responsible for the die-off. However, in the ensuing decades, as the realization that many trees with typical birch dieback symptoms died without any sign of borer attack, this perspective shifted ​[19]​. [Indeed, indications of borer attack in Thunder Bay were rare (E. Setliff and J. McLaughlin, personal observations)]. At present, the conclusion is that the borer is a secondary killer of predisposed trees in both rural cut-overs and urban areas.

Studies of silver-leaf disease began in Canada in 1909 when H.T. Güssow identified Stereum purpureum growing on an apple branch ​[32]​. A recent German emigrant, he had spent time in England and was aware of the work by the British on silver-leaf disease. The branch was given to him by Professor H.W. Smith in Nova Scotia ​[32]​. Appointed the first Dominion of Canada Botanist, Güssow alerted growers of the threat of silver-leaf disease in fruit orchards ​[15–17]​. He observed silver-leaf in orchards from Nova Scotia to British Columbia. However, he failed to go beyond contemporary thinking that the hazard was confined to fruit trees.

Fig. 3. An individual tree presumably killed by silver-leaf disease in Thunder Bay, Ontario. September 1992.
Fig. 4. Roadside right-of-way along Rt. 622 near U.S. border with MN that shows dead birch in various stages of deterioration. Aug. 27, 1992.

What was to be an epidemic upsurge of canopy decline and dieback in birch stands was first noticed in 1932 in south-central New Brunswick ​[2]​. Betula alleghaniensis, B. papyrifera, and B. populifolia were affected. The disease was described as appearing to “radiate” outward in all directions so that by 1939-40 the outer boundaries were the eastern border of Maine, northern New Brunswick plus adjacent Quebec, and northern Nova Scotia ​[11]​. According to Balch and Prebble ​[2]​, “. . . most stands of mature birch in this general region (some 15 000 square miles) took on a brownish to greyish appearance caused by the dying of foliage and branches.  The condition was still more noticeable and wide-spread in 1939, when dead branches were more evident, but browning foliage was rather less conspicuous.”; hence the popular name birch dieback. By this time, merchantable birch trees in New Brunswick were mostly gone. The disease is now found throughout the range of birch in the north temperate forests of Canada in urban (Fig. 3) ​[21, 22]​ and rural ​[30]​ areas (Fig. 4). The pattern of disease development supported the idea of an infectious agent being involved ​[18, 19]​. Also observed was disease movement from cut-over to uncut areas ​[19]​. Presently, with the discovery of a frequent association of the wound pathogen C. purpureum with canopy and trunk death in birch trees, the etiology of the disease becomes persuasive and provides a credible explanation for birch dieback specifically in the Thunder Bay District, Ontario ​[21, 22, 30]​, and globally in cool temperate regions ​[29]​. The conclusion is that C. purpureum is the major cause of the widespread birch dieback disease in North America.

Predisposition of birch trees, especially from wounding, favors both the bronze birch borer and C. purpureum but perhaps not equally. Minute to small wounds in otherwise healthy trees probably provide for early infection by basidiospores. Thus, C. purpureum becomes more of a primary agent for birch dieback disease than the bronze birch borer. However, in warmer regions in the United States below the Great Lakes, the borer may be favored more so than in the colder regions of Canada. The interaction between the bronze borer and C. purpureum, with the latter being a potential attractant, remains to be studied.

Abiotic environmental factors play an important role in disease development, and there are many papers that focus on this aspect of birch dieback ​[1, 3, 11, 12, 14, 20, 28]​. Now with newer insights into C. purpureum as a virulent pathogen of B. papyrifera ​[21, 22, 30]​, how climate influences the silver-leaf disease epidemic of birch over the entirety of Canada will require additional research and consideration.

One intriguing aspect of C. purpureum is its ability to produce toxic “macerating” enzymes ​[23, 24]​ (23, 24). These toxins act on woody/leaf tissue in the canopy and potentially in the root system at a distance from where the fungus is located in the tree. In their investigations of root systems, Hawboldt and Greenidge ​[18, 19]​ considered rootlet mortality a symptom of birch decline, and suggested that it occurred prior to above ground symptoms.

The failure to discover C. purpureum as a frequent component of dying and dead birch trees in Canada derives from horticultural perceptions established in England, a mostly non-forested country. In Canada, the boreal and northern hardwood forests, with ongoing large-scale logging operations and severe winters, present an entirely different set of environmental conditions that influence the severity and often epidemic nature of the disease.  

The ForPathNotes publication initiative was created as a means for providing fast and efficient global communication about tree diseases. With the finding that the elusive C. purpureum is often associated with birch trees as a wound pathogen, a new perspective as to the primary cause of birch dieback emerges ​[29]​. This viewpoint is strongly supported by the successful inoculation of B. papyrifera ​[22]​ with C. purpureum. In essence, birch dieback in cities and decadence of birch in cut-overs and in forests are victims of silver-leaf disease. ForPathNotes in the following links provide corroborating pictorial support for the observations made of serious dieback in a northern Wisconsin apple orchard ​[31]​ in 1972 and silver-leaf disease of birch in the Thunder Bay District of northwestern Ontario between 1985 to 2002 ​[21, 22, 30]​.

  1. Silver-leaf disease of apple trees in Wisconsin: the birch connection  
  2. A pictorial account of Betula papyrifera dieback and death in Thunder Bay, Ontario  
  3. A pictorial account of Chondrostereum purpureum killing paper birch trees on the Lakehead University campus, Thunder Bay  
  4. Birch dieback: symptoms and signs of Chondrostereum purpureum  
  5. Wounds as avenues for infection by Chondrostereum purpureum  
  6. Chondrostereum purpureum: sources of basidiospore inoculum  
  7. The age of old-growth Betula papyrifera in northwestern Ontario  
  8. Casual observations of silver-leaf disease on birch/poplar in Europe  

Acknowledgments

My thanks go to Jim Worrall and his web site forestpathology.org for making this presentation possible. Also, thanks go to Karen Nakasone, Center for Forest Mycology Research, U.S. Forest Products Laboratory, Madison, WI for assistance in acquiring literature through the University of Wisconsin’s Steenbock Memorial Library. My observations of silver-leaf disease in England and Europe were made possible by a sabbatical leave from Lakehead University, that allowed me to establish a base in the laboratory of Alan Rayner, Bath University, Bath, UK. For this privilege, I am most grateful. Thanks also go to Meindert de Jong who introduced me to some if his biocontrol of wild cherry trials in the Netherlands. The editorial comments provided by Jim Worrall and Dorene Setliff are warmly acknowledged as is the field assistance of my daughter Alissa Setliff and the interest and support of my students.

References

  1. 1.
    Auclair AND, Worrest RC, LaChance D, Martin HC. 1992. Climatic perturbation as a general mechanism of forest dieback. In: Forest Decline Concepts, eds Manion PD, LaChance D, pp. 38–58. St. Paul, Minnesota, USA: APS Press, the American Phytopathological Society.
  2. 2.
    Balch RE, Prebble JS. 1940. The bronze birch borer and its relation to the dying of birch in New Brunswick forests. The Forestry Chronicle 16(3):179–201 <http://pubs.cif-ifc.org/doi/10.5558/tfc16179-3>.
  3. 3.
    Braathe P. 1957. Is there a connection between the birch dieback and the March thaw of 1936? The Forestry Chronicle 33(4):358–363 <http://pubs.cif-ifc.org/doi/10.5558/tfc33358-4>.
  4. 4.
    Brooks FT. 1910. Some observations on the silver-leaf disease of fruit trees. Report of the 80th Meeting of the British Association for the Advancement of Science, Transactions of Section K, pp. 776–777.
  5. 5.
    Brooks FT. 1911. “Silver-leaf” disease. The Journal of Agricultural Science 4(2):133–144 <10.1017/S0021859600001611>.
  6. 6.
  7. 7.
    Brooks FT, Bailey MA. 1919. Silver-leaf disease, III. (Including observations upon the injection of trees with antiseptics). The Journal of Agricultural Science 9(3):189–215 <10.1017/S0021859600004792>.
  8. 8.
    Brooks FT, Moore WC. 1923. On the invasion of woody tissues by wound parasites. Transactions of the Cambridge Philosophical Society (Biology Series) 1:56–68.
  9. 9.
    Brooks FT, Moore WC. 1926. Silver-leaf disease.—V. Journal of Pomology and Horticultural Science 5(2):61–97 <10.1080/03683621.1925.11513289>.
  10. 10.
    Brooks FT, Storey HH. 1924. Silver-leaf disease.—IV. Journal of Pomology and Horticultural Science 3(3):117–141 <10.1080/03683621.1924.11513257>.
  11. 11.
    Clark J, Barter GW. 1958. Growth and climate in relation to dieback of yellow birch. Forest Science 4:343–364.
  12. 12.
    Clark J, Gibbs RD. 1957. Studies in tree physiology: IV. Further investigations of seasonal changes in moisture content of certain Canadian forest trees. Canadian Journal of Botany 35(2):219–253 <10.1139/b57-021>.
  13. 13.
    Gram E, Weber A. 1953. Plant Diseases in Orchard, Nursery and Garden Crops. Translated from 2nd Danish edition by E Ramsden; ed. RWG Dennis. New York: Philosophical Library.
  14. 14.
    Greenidge KNH. 1953. Further studies of birch dieback in Nova Scotia. Canadian Journal of Botany 31(5):548–559 <10.1139/b53-044>.
  15. 15.
    Güssow HT. 1910. The problems of plant diseases. ‘Silver leaf’ of fruit trees of very serious importance. Evidence of Mr. H.T. Güssow, Dominion botanist before the Select Standing Committee on Agriculture and Colonization 1909 – 1910. Appendix No. 1. , pp. 64–66. Ottawa, Ontario, Canada: CH Parmelee, Printer to the King’s Most Excellent Majesty.
  16. 16.
    Güssow HT. 1911. Preliminary note on ‘silver leaf’ disease of fruit trees. Phytopathology 1:177–179.
  17. 17.
    Güssow HT. 1911. Silver leaf disease of fruit trees. (An appeal for the co-operation of Canadian fruit growers in preventing the spread of this dangerous pest). Census and Statistics Monthly for August 4, pp. 1–2.
  18. 18.
    Hawboldt LS, Greenidge KNH. 1952. Dieback of yellow birch and rootlet mortality in Nova Scotia. Canadian Department of Agriculture, Science Services, Division of Forest Biology, Bi-Monthly Progress Report 8(6).
  19. 19.
    Hawboldt LS, Skolko AJ. 1948. Investigation of yellow birch dieback in Nova Scotia in 1947. Journal of Forestry 46(9):659–671 <10.1093/jof/46.9.659>.
  20. 20.
    Jones EA, Reed DD, Mroz GD, Liechty HO, Cattelino PJ. 1993. Climate stress as a precursor to forest decline: paper birch in northern Michigan, 1985–1990. Canadian Journal of Forest Research 23(2):229–233 <10.1139/x93-030>.
  21. 21.
    McLaughlin JA. 1990. Chondrostereum purpureum associated with decline of Betula papyrifera in Thunder Bay, Ontario. Plant Dis. 74(4):331 <10.1094/PD-74-0331E>.
  22. 22.
    McLaughlin JA. 1991. A study of Chondrostereum purpureum and its role in the decline of white birch in Thunder Bay. MScF thesis. Lakehead University.
  23. 23.
    Miyairi K, Fujita K, Okuno T, Sawai K. 1977. A toxic protein causative of silver-leaf disease symptoms on apple trees. Agricultural and Biological Chemistry 41(10):1897–1902 <10.1080/00021369.1977.10862783>.
  24. 24.
    Miyairi K, Okuno T, Sawai K. 1985. Purification and properties of endopolygalacturonase i from Stereum purpureum , a factor inducing silver-leaf symptoms on apple trees. Agricultural and Biological Chemistry 49(4):1111–1118 <10.1080/00021369.1985.10866847>.
  25. 25.
    Percival J. 1902. “Silver-leaf” disease. Journal of the Linnean Society of London, Botany 35(245):390–395 <10.1111/j.1095-8339.1902.tb00600.x>.
  26. 26.
    Pickering S. 1906. Silver-leaf. Report of the Woburn Experimental Fruit Farm 6:210–224.
  27. 27.
    Pickering S. 1910. Silver-leaf disease. Report of the Woburn Experimental Fruit Farm 12:1–34.
  28. 28.
    Redmond DR. 1955. Studies in forest pathology: XV. Rootlets, mycorrhiza, and soil temperatures in relation to birch dieback. Canadian Journal of Botany 33(6):595–627 <10.1139/b55-048>.
  29. 29.
    Setliff EC. 2002. The wound pathogen Chondrostereum purpureum, its history and incidence on trees in North America. Australian Journal of Botany 50(5):645–651 <10.1071/BT01058>.
  30. 30.
    Setliff EC, McLaughlin JA. 1991. Preliminary assessment of Chondrostereum purpureum associated with post-logging decadence. Canadian plant disease survey 71(1):136 <https://phytopath.ca/wp-content/uploads/2014/10/cpds-archive/vol71/cpds_vol71_no1_(129-136)1991.pdf>.
  31. 31.
    Setliff EC, Wade EK. 1973. Stereum purpureum associated with sudden decline and death of apple trees in Wisconsin. Plant Disease Reporter 57(5):473–474 <https://babel.hathitrust.org/cgi/pt?id=chi.23658044&seq=497>.
  32. 32.
    Smith HW. 1909. Report of the Professor of Biology. In: Appendix No. 8. Part I. Agriculture. Review of the Work of the Agricultural Department of the Government of Nova Scotia, 1909, pp. 26–38. Halifax, Nova Scotia: Nova Scotia Secretary of Agriculture <https://0-nsleg–edeposit-gov-ns-ca.legcat.gov.ns.ca/deposit/b10419482_1909.pdf>.

Leave a Comment