Brenneria salicis (watermark)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Means of Movement and Dispersal
- Plant Trade
- Wood Packaging
- Environmental Impact
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Brenneria salicis (Day) Hauben et al.
Preferred Common Name
Other Scientific Names
- Bacterium saliciperda (Lindeijer) Burgvits 1935
- Bacterium salicis Day 1924
- Chromobacterium salicis (Day) Krasil'nikov 1949
- Erwinia amylovora var. salicis (Day) Martinec & Kocur 1963
- Erwinia salicis (Day) Chester
- Phytobacterium saliciperda (Lindeijer) Magrou & Prévot 1948
- Phytomonas saliciperda (Lindeijer) Magrou 1937
- Phytomonas salicis (Day) Magrou 1937
- Pseudobacterium salicis (Day) Krasil'nikov 1949
- Pseudomonas saliciperda Lindeijer 1932
International Common Names
- English: vascular: willow wilt; watermark disease of willow; willow vascular wilt; willow watermark disease
- French: coloration bactérienne du saule
Local Common Names
- Germany: Wasserzeichenkrankheit: Weide
- ERWISA (Erwinia salicis)
Summary of InvasivenessTop of page In Japan the pathogen behaves in an invasive manner, spreading rapidly in established stands of willow. It is currently restricted to areas of Hokkaido with a cool climate and this may be a key factor limiting spread. In Europe it has developed into a destructive epidemic only where large numbers of uniformly susceptible clones have been planted. There is no indication that it is expanding its geographic range within the continent.
Taxonomic TreeTop of page
- Domain: Bacteria
- Phylum: Proteobacteria
- Class: Gammaproteobacteria
- Order: Enterobacteriales
- Family: Enterobacteriaceae
- Genus: Brenneria
- Species: Brenneria salicis
Notes on Taxonomy and NomenclatureTop of page Erwinia salicis was accepted in the Approved Lists of Bacterial Names (Skerman et al., 1980). Subsequently, Hauben et al. (1998) proposed a new genus, Brenneria, and included the species as Brenneria salicis. The proposal of Brenneria was based on comparative analyses of 16S rDNA sequence data. A similar analysis by Spröer et al. (1999) did not support Brenneria as a natural group, and that of Kwon et al. (1997) suggested that E. salicis, E. rubrifaciens and E. nigrifluens formed a clade separate from the other Erwinia species.
DescriptionTop of page B. salicis is a Gram-negative, facultative anaerobic, non-sporing rod, motile with peritrichous flagella. Colonies on nutrient agar are 1-2 mm diameter after 4 days at 20°C, transparent to white, circular, convex and shining.
Many isolates, although not those from the Netherlands, produce yellow growth on autoclaved potato tissue.
DistributionTop of page In the UK the disease is mainly found in East Anglia, particularly in the counties of Essex and Suffolk. Isolated outbreaks have occurred somewhat further north in Leicestershire and west in Wiltshire. It is widespread in the Netherlands and is also found in parts of Belgium.
In Hokkaido, Japan, the disease occurs in the Taisetsu mountainous area (Kamikawa, Kamisihoro, Rubeshibe and Oketo) and in the upper part of the Nissho Pass (Hidaka).
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Japan||Present||Bradbury, 1986; EPPO, 2014|
|-Hokkaido||Present||Sakomoto et al., 1999|
|Austria||Absent, invalid record||Bradbury, 1986; EPPO, 2014|
|Belgium||Restricted distribution||Rijckaert et al., 1984|
|Hungary||Present||Németh et al., 1999; CABI/EPPO, 2006|
|Italy||Present||Grosso et al., 2011|
|Netherlands||Widespread||****||Gremmen and DeKam, 1970; Bradbury, 1986; EPPO, 2014|
|UK||Restricted distribution||Not invasive||Day, 1924; EPPO, 2014|
|-England and Wales||Restricted distribution||EPPO, 2014|
Risk of IntroductionTop of page In Europe the disease has spread little in the past 50 years, perhaps because the pathogen is now dispersed in all areas where Salix is grown. If susceptible willow cultivars were planted in northern Europe, serious losses to Salix might be expected.
In Japan the disease has only been known since 1993 when serious damage was found in several natural forests in Hokkaido. There is no record of planting material of Salix spp. having been introduced to the region (Y. Sakamoto, Hokkaido Research Center, Forestry and Forest Products Research Institute, Sapporo, Japan, personal communication, 2004) and its origin is unknown. There may well be the potential for further damage both in Japan, in other temperate areas of the Asia.
There is also a potential for damage in North America where the susceptibility of the willow species grown there is unknown.
B. salicis should be considered a quarantine pest for parts of temperate Asia and North America, and for temperate regions of the Southern Hemisphere where willows are grown as exotics.
HabitatTop of page Watermark disease occurs in both wild and cultivated willow in the lowland areas of several European countries and in natural forest in the mountainous areas of Hokkaido, the northern island of Japan.
Hosts/Species AffectedTop of page Only Salix species are recorded as susceptible hosts. In Europe, watermark disease has been recorded more frequently in S. alba than in any other species. No clones of S. alba show immunity, and S. alba var. caerulea and the Dutch clones Liempde, Drakenburg, Belders and Lichtenvoorde are particularly susceptible. Watermark has been commonly reported in S. alba x S. fragilis hybrids and in S. alba var. vitellina. It also occurs in S. caprea and S. fragilis but less frequently in S. cinerea, S. purpurea and S. triandra (Turner et al., 1992).
In Japan the disease occurs in three species: S. bakko, S. sachalinensis and S. kinuyanagi [S. schwerinii](Sakomoto et al., 1999).
Host Plants and Other Plants AffectedTop of page
|Salix alba (white willow)||Salicaceae||Main|
|Salix caprea (pussy willow)||Salicaceae||Wild host|
|Salix cinerea (grey sallow)||Salicaceae||Other|
|Salix fragilis (crack willow)||Salicaceae||Wild host|
|Salix purpurea (purple willow)||Salicaceae||Other|
|Salix triandra (almond willow)||Salicaceae||Other|
|Salix viminalis (osier)||Salicaceae||Main|
Growth StagesTop of page Vegetative growing stage
SymptomsTop of page During spring and summer, the leaves on some branches suddenly wilt and turn reddish-brown. These branches die and become leafless. The wood of affected branches and trunks shows a water-soaked brown or red-brown stain in the sapwood that is often restricted to the outermost annual rings but may sometimes cover the whole transverse section. Seriously diseased trees may die. Bacteria tend to ooze from the watermark-stained wood after cutting (Sakomoto et al., 1999). Sometimes recovery shoots develop on the affected branches but these often become affected subsequently.
List of Symptoms/SignsTop of page
|Leaves / abnormal colours|
|Leaves / abnormal leaf fall|
|Leaves / necrotic areas|
|Leaves / wilting|
|Stems / dieback|
|Stems / internal discoloration|
|Stems / ooze|
|Whole plant / plant dead; dieback|
Biology and EcologyTop of page B. salicis infects the xylem of willow. However, from the time of the first investigation of the disease in cricket bat willow plantations of eastern England, UK, it has been realized that, although large numbers of bacteria can be liberated from diseased trees to provide inoculum, the pathogen appears not to be readily transmissible to other willow plants. Attempts to inoculate the pathogen artificially into willow stems, whether via wounds, or through leaf and bud scars, have generally resulted in little disease expression. In studies in the Netherlands, many inoculation experiments involving different types of wounds resulted in about 10% success in terms of symptom development. Disease symptoms never appeared following the spraying of bacterial suspension onto leaf scars in autumn or buds and catkins in spring (Gremmen and De Kam, 1981). Results of this kind have led to the conclusion that the pathogen may dwell in a latent existence phase in the xylem, only developing to express disease under precise environmental conditions. Many trees with such latent infections may never show symptoms. This view is supported by data from immunological studies, which indicate that the bacterium is present in asymptomatic trees, including the coppice stools from which stem material is taken for propagation.
In Japan, a study entailing wound inoculation of 2-year-old seedlings of Salix sachalinensis and S. kinuyanagi [S. schwerinii] readily resulted in the development of typical symptoms within a few weeks (Sakomoto et al., 1999). However, further inoculation tests conducted in Sapporo in 1999 and 2003 were not successful and it has been suggested that climate may be a key factor in infection (Y. Sakamoto, Hokkaido Research Center, Forestry and Forest Products Research Institute, Sapporo, Japan, personal communication, 2004).
The idea that much disease dissemination occurs by the introduction of propagating material from several sources is supported by evidence that different strains (electrotypes) of the bacterium can be present in adjacent diseased cricket bat willows. This pattern would be unlikely if the spread of infection from tree-to-tree via aerosol- or splash-borne bacteria was occurring from a single source of inoculum.
Means of Movement and DispersalTop of page Natural Dispersal
Large numbers of bacteria can be liberated from diseased trees and, as immunological studies indicate, can be present on the foliage of adjacent healthy trees. However, in Europe, it appears that infection resulting from this source may be followed by long incubation periods before symptoms are expressed. This latent phase may never lead to the development of disease. In Japan the natural dispersal of air- or water-borne bacteria may lead to rapid disease development.
In Europe, various insects such as the willow and poplar borer (Cryptorhynchus lapathi) and the willow wood wasp (Xiphydria prolongata) have been studied but no evidence has been found to implicate them as vectors.
There is no evidence for transmission of the pathogen with seed.
The normal method of willow propagation is by vegetative means: lengths of stem being planted and allowed to root. Studies in the Netherlands on infected coppice stools showed that watermark symptoms appear in 3- to 4-year-old 'sets' (the stem sections used for propagation) but not in 1- and 2-year-old sets (DeKam, 1983). However, studies in the UK using ELISA have shown the presence of the bacterium in 1-year-old sets (Turner et al., 1992).
In the UK, during the 1980s, a serious outbreak of watermark disease occurred in a cricket bat willow plantation in Wiltshire that had been established with sets brought from the main willow-growing area of eastern England. Adjacent diseased trees proved to be affected with different strains (electrotypes) of the bacterium, a situation that pointed to an introduction of several genotypes of the bacterium in the planting material (Guven et al., 1999).
Movement in Trade
Evidence that the bacterium can be present in a latent form in propagating material has obvious implications for the movement of such material in trade.
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Stems (above ground)/Shoots/Trunks/Branches||Yes||Pest or symptoms usually invisible|
|Wood||Yes||Pest or symptoms usually invisible|
|Plant parts not known to carry the pest in trade/transport|
|Fruits (inc. pods)|
|Growing medium accompanying plants|
|True seeds (inc. grain)|
Wood PackagingTop of page
|Wood Packaging not known to carry the pest in trade/transport|
|Loose wood packing material|
|Processed or treated wood|
|Solid wood packing material with bark|
|Solid wood packing material without bark|
ImpactTop of page No precise figures are available on losses due to watermark disease. The disease has had a significant impact on the cricket bat willow-growing industry in eastern England, UK, itself responsible for some 90% of the world supply of blades for cricket bats (quantities of 'clefts' from which the bats are made are exported to other countries for the manufacture of the finished bat). In the 1930s more than one-eighth of the trees in commercial plantations were diseased and rendered useless for bat production. With the removal of diseased trees, losses dropped to ca 0.5% per annum by the 1980s. With some fluctuations, they have remained at that level for the past 20 years. Currently the principal expenditure is that for quarantine inspections of the whole cricket bat growing area. The owner of the diseased tree bears the cost of its destruction. In the Netherlands heavy losses were sustained from the 1960s to the 1990s as large numbers of diseased Salix alba 'Liempde' had to be removed.
As far as is known the losses of willow in mountainous areas of Hokkaido, Japan, have had little economic impact.
Environmental ImpactTop of page The environmental impact of the disease is limited due to the rapid growth of willow, which results in rapid replacement of damaged and dead trees. The main environmental impact in Europe has probably been in the Netherlands where trees planted to enhance the urban environment have become diseased and have been felled. There is no environmental impact in Japan as yet.
DiagnosisTop of page Small pieces of tissue are excised from the margins of watermark-stained wood freshly removed from a diseased tree. Each piece is comminuted in a small quantity of sterile peptone water (1%). The resulting suspension is streaked on plates of surface-dried nutrient agar (NA) and incubated at 20°C. The development of largely unmixed bacterial colonies after 4-6 days is a good indication that the pathogen has been isolated. Single colonies are re-streaked on fresh NA plates for further investigation. Demonstration that the bacterium is a Gram-negative, facultative anaerobic, non-sporing rod, motile with peritrichous flagella with small colonies that are transparent to white, circular, convex and shining on nutrient agar. Erwinia herbicola, a common contaminant of necrotic plant tissue, is identical in these tests but produces bright yellow-pigmented colonies.
There are reliable immunological methods, such as ELISA, that can confirm the identity of the pathogen including strains obtained from symptomless plants. Highly specific and sensitive molecular probes based on unique DNA sequences obtained by DNA subtraction methods can readily be developed for the pathogen. These methods are only used when a high level of confidence in identification is necessary to support eradication programmes or quarantine restrictions that may involve compensation.
Detection and InspectionTop of page Field detection relies upon the symptoms described above. Where the disease is covered by a statutory order, as in the UK, inspection has concentrated on commercial cricket bat willow plantations with a history of the disease and on wild willow in the vicinity.
Similarities to Other Species/ConditionsTop of page No similar disease syndrome is known in Salix.
Prevention and ControlTop of page In England, UK, control is by the removal of diseased trees. Removal is enforced by law in certain counties where cricket bat willow is grown commercially. These statutory powers were first conferred by the Forestry Commission on Essex County Council in the form of the Watermark Disease (Essex) Order 1933. Essex County Council was thereby given authority to appoint officers to enter premises for the purpose of inspecting willows, shrubs, stools and sets, and to serve notices requiring the destruction of all infected plants. Similar Orders were then brought into force in certain other counties. In Essex, regular and systematic inspections of trees and set beds were started in the late 1950s. The present practice is for staff to inspect annually plantations that contain more than 250 trees in Essex and, on an agency basis, in Suffolk and Bedfordshire also. The enforced destruction of watermarked willow has been associated with a reduction in disease from more than 12% of the crop in 1933 to less than 0.5% at present.
Set beds have been checked for latent infection by the ELISA method and badly affected beds taken out of production.
In the Netherlands, there has been no organized programme of eradication. In ornamental plantings, highly susceptible clones are replaced by less susceptible ones.
ReferencesTop of page
Day WR, 1924. The watermark disease of cricket bat willow (Salix caerulea). Oxford, UK: Oxford University Press. Oxford Forestry Memoirs No 3.
EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm
Gremmen J; DeKam M, 1970. Erwinia salicis as the cause of dieback in Salix alba in the Netherlands and its identity with Pseudomonas saliciperda. Netherlands Journal of Plant Pathology, 76:249-252.
Grosso S; Mason G; Ortalda E; Scortichini M, 2011. Brenneria salicis associated with watermark disease symptoms on Salix alba in Italy. Plant Disease, 95(6):772-773. http://apsjournals.apsnet.org/loi/pdis
Guven K; Davis JML; Turner JG, 1999. Geographical distribution of Erwinia salicis strains, the cause of watermark disease of willows. European Journal of Forest Pathology, 29:347-363.
Hauben L; Moore ERB; Vauterin L; Steenackers M; Mergaert J; Verdonck L Swings J, 1998. Phylogenetic position of phytopathogens within Enterobacteriaceae. Systematic and Applied Microbiology, 21:384-397.
Huvenne H; Goeminne G; Maes M; Messens E, 2008. Identification of quorum sensing signal molecules and oligolignols associated with watermark disease in willow (Salix sp.). Journal of Chromatography, B, 872(1/2):83-89. http://www.sciencedirect.com/science?_ob=ArticleURL&_udi=B6X0P-4T0WJWY-1&_user=6686535&_coverDate=09%2F01%2F2008&_rdoc=11&_fmt=high&_orig=browse&_srch=doc-info(%23toc%237220%232008%23991279998%23696506%23FLA%23display%23Volume)&_cdi=7220&_sort=d&_docanchor=&_ct=27&_acct=C000066028&_version=1&_urlVersion=0&_userid=6686535&md5=2c2fc11b23693bc20da4506460ca526b
Huvenne H; Messens E; Maes M, 2005. Watermark disease in willow and its relation to Brenneria salicis dominance in the wood. Communications in Agricultural and Applied Biological Sciences, 70(3): 111-113.
Huvenne H; Messens E; Maes M, 2009. Willow wood sap promotes the density-dependent pathogenesis of Brenneria salicis. Environmental Microbiology, 11(6):1463-1472. http://www.blackwell-synergy.com/loi/emi
Kwon SoonWo; Go SeungJoo; Kang HeeWan; Ryu JinChang; Jo JinKi, 1997. Phylogenetic analysis of Erwinia species based on 16S rRNA gene sequences. International Journal of Systematic Bacteriology, 47(4):1061-1067; 53 ref.
Maes M; Huvenne H; Messens E, 2009. Brenneria salicis, the bacterium causing watermark disease in willow, resides as an endophyte in wood. Environmental Microbiology, 11(6):1453-1462. http://www.blackwell-synergy.com/loi/emi
Németh J; Csonka I; Szabó L, 1999. Erwinia salicis okozta fapusztulás fehérfuz állományban. In: Sáringer Gy, Balázs K, Szemessy A, eds. 45. Növényvédelmi Tudományos Napok, 45th Plant Protection Days, Budapest 1999. február 23-24. pp. 119.
Rijckaert C; van Tomme R; Steenackers V; Deley J, 1984. The occurrence of watermark disease of willows (Salix) in Belgium. Meded Faculty Landbouwnwetensch Rijksuniversit Gent, 49(26):509-515.
Sakamoto Y, 2004. Hokkaido Research Center, Forestry & Forest Products research Institute, Sapporo, Japan. http://www.ffpri-hkd.affrc.go.jp/group/jubyo/sakamoto/index-e.html.
Sakomoto Y; Takikawa Y; Sasaki K, 1999. Occurrence of watermark disease of willows in japan. Plant Pathology, 48:613-619.
Spröer C; Mendrock U; Swiderski J; Lang E; Stackebrandt E, 1999. The phylogenetic position of Serratia, Buttiauxella and some other genera of the family Enterobacteriaceae. International Journal of Systematic Bacteriology, 49(4):1433-1438; 34 ref.
Turner JG; Davis JML; Guven K, 1992. Watermark disease of tree willows. Proceedings of the Royal Society of Edinburgh 98B, 105-117.
Zheng HuaYing; Dai YuSheng; Xie ChunXia; Guo TongBin; Wang ZhenYing, 2006. Studies on the cause of formation of poplar red core wood. Journal of Nanjing Forestry University (Natural Sciences Edition), 30(2):82-84. http://njlydxxb.periodicals.net.cn/default.html
Distribution MapsTop of page
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