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Sirococcus clavigignenti-juglandacearum
(butternut canker)

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Datasheet

Sirococcus clavigignenti-juglandacearum (butternut canker)

Summary

  • Last modified
  • 10 December 2020
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Sirococcus clavigignenti-juglandacearum
  • Preferred Common Name
  • butternut canker
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Fungi
  •     Phylum: Ascomycota
  •       Subphylum: Pezizomycotina
  •         Class: Sordariomycetes

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Pictures

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PictureTitleCaptionCopyright
Sirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on bark. Mississauga, Ontario, Canada. July 2016.
TitleSymptoms
CaptionSirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on bark. Mississauga, Ontario, Canada. July 2016.
CopyrightPublic Domain - Released by Reuven Martin/via iNaturalist - CC0
Sirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on bark. Mississauga, Ontario, Canada. July 2016.
SymptomsSirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on bark. Mississauga, Ontario, Canada. July 2016.Public Domain - Released by Reuven Martin/via iNaturalist - CC0
Sirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on bark. Medway, London, Ontario, Canada. February 2019.
TitleSymptoms
CaptionSirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on bark. Medway, London, Ontario, Canada. February 2019.
Copyright©Quinten Wiegersma/via iNaturalist - CC BY 4.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on bark. Medway, London, Ontario, Canada. February 2019.
SymptomsSirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on bark. Medway, London, Ontario, Canada. February 2019.©Quinten Wiegersma/via iNaturalist - CC BY 4.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on bark. Medway, London, Ontario, Canada. February 2019.
TitleSymptoms
CaptionSirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on bark. Medway, London, Ontario, Canada. February 2019.
Copyright©Quinten Wiegersma/via iNaturalist - CC BY 4.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on bark. Medway, London, Ontario, Canada. February 2019.
SymptomsSirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on bark. Medway, London, Ontario, Canada. February 2019.©Quinten Wiegersma/via iNaturalist - CC BY 4.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on bark. Stoney Creek, London, Ontario, Canada. March 2019.
TitleSymptoms
CaptionSirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on bark. Stoney Creek, London, Ontario, Canada. March 2019.
Copyright©Quinten Wiegersma/via iNaturalist - CC BY 4.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on bark. Stoney Creek, London, Ontario, Canada. March 2019.
SymptomsSirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on bark. Stoney Creek, London, Ontario, Canada. March 2019.©Quinten Wiegersma/via iNaturalist - CC BY 4.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on butternut (Juglans cinerea) bark. Goodhue County, Minnesota, USA. December 2013.
TitleSymptoms
CaptionSirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on butternut (Juglans cinerea) bark. Goodhue County, Minnesota, USA. December 2013.
Copyright©Steven Katovich, Bugwood.org - CC BY 3.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on butternut (Juglans cinerea) bark. Goodhue County, Minnesota, USA. December 2013.
SymptomsSirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on butternut (Juglans cinerea) bark. Goodhue County, Minnesota, USA. December 2013.©Steven Katovich, Bugwood.org - CC BY 3.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Symptoms. October 2006.
TitleSymptoms
CaptionSirococcus clavigignenti-juglandacearum (butternut canker); Symptoms. October 2006.
Copyright©Joseph O'Brien, USDA Forest Service/via Bugwood.org - CC BY 3.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Symptoms. October 2006.
SymptomsSirococcus clavigignenti-juglandacearum (butternut canker); Symptoms. October 2006.©Joseph O'Brien, USDA Forest Service/via Bugwood.org - CC BY 3.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on butternut (Juglans cinerea) bark. September 2005.
TitleSymptoms
CaptionSirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on butternut (Juglans cinerea) bark. September 2005.
Copyright©USDA Forest Service - Northeastern Area , USDA Forest Service/via Bugwood.org - CC BY 3.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on butternut (Juglans cinerea) bark. September 2005.
SymptomsSirococcus clavigignenti-juglandacearum (butternut canker); Symptoms on butternut (Juglans cinerea) bark. September 2005.©USDA Forest Service - Northeastern Area , USDA Forest Service/via Bugwood.org - CC BY 3.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Symptoms, cross-section of trunk. October 2006.
TitleSymptoms
CaptionSirococcus clavigignenti-juglandacearum (butternut canker); Symptoms, cross-section of trunk. October 2006.
Copyright©Joseph O'Brien, USDA Forest Service/via Bugwood.org - CC BY 3.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Symptoms, cross-section of trunk. October 2006.
SymptomsSirococcus clavigignenti-juglandacearum (butternut canker); Symptoms, cross-section of trunk. October 2006.©Joseph O'Brien, USDA Forest Service/via Bugwood.org - CC BY 3.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Dead Butternut trees (Juglans cinerea), killed by Sirococcus clavigigenti-juglandacearum. November 2008.
TitleField Symptoms
CaptionSirococcus clavigignenti-juglandacearum (butternut canker); Dead Butternut trees (Juglans cinerea), killed by Sirococcus clavigigenti-juglandacearum. November 2008.
Copyright©USDA Forest Service - Forest Health Protection Eastern Region - St. Paul, MN , USDA Forest Service/via Bugwood.org - CC BY 3.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Dead Butternut trees (Juglans cinerea), killed by Sirococcus clavigigenti-juglandacearum. November 2008.
Field SymptomsSirococcus clavigignenti-juglandacearum (butternut canker); Dead Butternut trees (Juglans cinerea), killed by Sirococcus clavigigenti-juglandacearum. November 2008.©USDA Forest Service - Forest Health Protection Eastern Region - St. Paul, MN , USDA Forest Service/via Bugwood.org - CC BY 3.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Butternut canker symptoms on butternut (Juglans cinerea) before (bottom) and after (top) bark is removed. West Lafayette, Indiana, USA. November 2012.
TitleSymptoms
CaptionSirococcus clavigignenti-juglandacearum (butternut canker); Butternut canker symptoms on butternut (Juglans cinerea) before (bottom) and after (top) bark is removed. West Lafayette, Indiana, USA. November 2012.
Copyright©Tom Creswell, Purdue University/via Bugwood.org - CC BY-NC 3.0
Sirococcus clavigignenti-juglandacearum (butternut canker); Butternut canker symptoms on butternut (Juglans cinerea) before (bottom) and after (top) bark is removed. West Lafayette, Indiana, USA. November 2012.
SymptomsSirococcus clavigignenti-juglandacearum (butternut canker); Butternut canker symptoms on butternut (Juglans cinerea) before (bottom) and after (top) bark is removed. West Lafayette, Indiana, USA. November 2012.©Tom Creswell, Purdue University/via Bugwood.org - CC BY-NC 3.0

Identity

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Preferred Scientific Name

  • Sirococcus clavigignenti-juglandacearum Nair, Kostichka and Kuntz

Preferred Common Name

  • butternut canker

International Common Names

  • French: chancre du noyer cendre

Local Common Names

  • Germany: Sirococcus-Krebs der Walnuss

EPPO code

  • SIROCJ (Sirococcus clavigignenti-juglandacearum)

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Fungi
  •         Phylum: Ascomycota
  •             Subphylum: Pezizomycotina
  •                 Class: Sordariomycetes
  •                     Subclass: Sordariomycetidae
  •                         Order: Diaporthales
  •                             Genus: Sirococcus
  •                                 Species: Sirococcus clavigignenti-juglandacearum

Notes on Taxonomy and Nomenclature

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The form-genus Sirococcus is probably heterogeneous (Castlebury et al., 2003), and the affinities of this fungus are not clear.

Description

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The pycnidia form in a thin, dark brown to black stroma of abundant, septate, branched mycelium beneath the outmost bark layer. Prominent hyphal pegs, measuring 1550-1900 x 450-510 µm, arise from this stroma. The pycnidia arise from the eustroma and are glabrous, non-rostrate, innate to erumpent and without a clypeus, globose to flattened. Pycnidia measure 90-320 x 100-375 µm, reaching 90-320 x 200-490 µm if confluent or multilocular. Walls multilayered, the outer becoming dark and coriaceous with age; cavity simple, convoluted or multilocular, uni- or multiostiolate; ostioles 8-30 µm in diameter; conidiophores 5-24 µm, simple or branched, septate with monophialidic, conidiogenous cells; conidia hyaline, two-celled, median-septate and fusiform, 9-17 x 1.0-1.5 µm, extruded singly or in chains through the ostiole in a glutinous beige to tan matrix, in cirri under moist conditions; cirri composed of coherent, vertically arranged spores, colourless and either thin or thick; during germination, germ tubes arise from the swollen cells either terminally or laterally (Nair et al., 1979).

Distribution

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S. clavigignenti-juglandacearum was first reported in Wisconsin, USA, in 1967 (Renlund, 1971). A pest alert announcing butternut decline was issued in 1976 (USDA, 1976). The origin and the original host plant of the fungus are not known, but there is evidence that it was introduced into the USA as a single isolate in the 1960s or earlier. The American population has a low level of genetic diversity, as confirmed by RAPD-PCR (Ostry and Skilling, 1995; Ostry, 1997b; Furnier et al., 1999). The pathogen spread rapidly across the USA and is now present in the entire native distribution area of J. cinerea (Tisserat and Kuntz, 1983a; USDA, 1995). In Canada (Ontario, Québec), it was detected for the first time in 1991 (Davis et al., 1992; Innes and Rainville, 1996). In 1995, infestation of a forest nursery was reported in Québec. In New Brunswick, the fungus was confirmed present for the first time in 1997 (Harrison et al., 1998).

Since the genus Juglans and the Juglandaceae are, besides North America and Europe, distributed in Asia and in South America, it must be presumed that S. clavigignenti-juglandacearum originates in one or other of the latter.

S. clavigignenti-juglandacearum is absent in the European and Mediterranean region. In North America it is present in Canada (at least in Ontario, Québec and New Brunswick), and in the USA (spread across the entire range of butternut).

Distribution Table

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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.

Last updated: 12 May 2022
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Europe

NetherlandsAbsent, Confirmed absent by survey

North America

CanadaPresent, Localized
-New BrunswickPresent
-OntarioPresent
-QuebecPresent
United States
-AlabamaPresent
-ArkansasPresent
-ConnecticutPresent
-DelawarePresent
-GeorgiaPresent
-IllinoisPresent
-IndianaPresent
-IowaPresent
-KentuckyPresent
-MainePresent
-MarylandPresent
-MassachusettsPresent
-MichiganPresent
-MinnesotaPresent
-MississippiPresent
-MissouriPresent
-New HampshirePresent
-New JerseyPresent
-New YorkPresent
-North CarolinaPresent
-OhioPresent
-PennsylvaniaPresent
-Rhode IslandPresent
-South CarolinaPresent
-TennesseePresent
-VermontPresent
-VirginiaPresent
-West VirginiaPresent
-WisconsinPresent

Risk of Introduction

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The status of the host plants of S. clavigignenti-juglandacearum in Europe, and their susceptibility to the fungus, are reviewed under Hosts. Economically, Juglans regia and J. nigra have the most valuable wood in Central Europe (Kucera, 1991; Beyse, 2001) and high-quality veneers make profits of more than 5000 EUR per m³. Wood of J. regia is used for high-quality cabinet making, musical instruments, crafts, stocks, etc. In France (Becquey, 1991), a campaign, funded by the EU, aims to produce high-quality Juglans wood for the furniture industry, by increasing the number and quality of walnut trees in Europe and standardizing walnut wood according to its use. It is planned to afforest agricultural lands with Juglans spp., according to new intensive sylvicultural systems. In Germany, walnut is also being promoted beyond its typical cultivation areas by the 'Interessengemeinschaft Nuss' (Kronauer, 1991; Anon., 1999). Nut and oil production are important industries in southern European countries (France, Hungary, Italy, Turkey).

It seems very likely that the fungus would, in southern Europe, encounter similar conditions to those in which it has been so damaging in North America. European Juglans spp. carry insects of the same families as those thought to act as vectors in North America (Schwenke, 1974). As in North America, reliable control measures are not available. Current American research on resistance in J. cinerea would not protect the Juglandaceae which grow in Europe.

According to Patterson (1993), S. clavigignenti-juglandacearum is much more aggressive than the fungi which caused chestnut blight (Cryphonectria parasitica; EPPO/CABI, 1997) and Dutch elm disease (Ophiostoma ulmi/Ophiostoma novo-ulmi). Furthermore, though the main pathways which were involved in the spread of these fungi (plants for planting, wood) are probably not of great importance in practice for S. clavigignenti-juglandacearum, the latter can be carried in infected nuts which carry a significant risk of casual introduction. There is general agreement among experts on the disease (e.g. Orchard, 1984; Fleguel, 1996; Nair, 1999) that the fungus presents a high risk to other continents and justifies phytosanitary measures. The seed transferability of the pathogen is one of the main risk factors to be considered when measures against the introduction of the fungus are taken. Thus, S. clavigignenti-juglandacearum presents a high risk to the European and Mediterranean region (Schröder et al., 2002) in that it is likely to kill large numbers of valuable trees used for economic production of wood, nuts and oil. It also threatens walnut as an amenity species widely planted throughout the European and Mediterranean region.

Hosts/Species Affected

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The main host is Juglans cinerea (butternut, white walnut, oilnut), which is native to North America. It is the only species that is killed by the pathogen, though other Juglans species and hybrids are diseased to varying degrees. Two other hosts are naturally infected in North America: Juglans nigra (black walnut) and Juglans ailanthifolia var. cordiformis (heartnut), but infrequently and only when standing among heavily infected butternut trees (Kuntz et al., 1979; Ostry, 1997a; Ostry et al., 1997). Some other Juglandaceae were found to be susceptible on artificial inoculation in laboratory experiments: Juglans regia, J. ailanthifolia, and various hybrids (Orchard et al., 1982). Laboratory experiments by Ostry (1997b) indicated that S. clavigignenti-juglandacearum might be able to survive on other Juglandaceous hosts (Carya spp.) and possibly other trees (Quercus, Prunus).

The most important potential host in the European and Mediterranean region is Juglans regia (walnut), an Asian species which is widely planted throughout most of Europe except the north. It needs mild winters without late frosts, and a climate which is not too dry. It can grow up to an elevation of 800 m, in the Alps up to 1200 m. Hungary, Turkey, Italy and France have commercial plantations of J. regia (Bernyi et al., 1991; Schütt et al., 1992), to produce nuts, oil or the valuable wood. In these countries and in many others, individual trees of J. regia are common in farms and gardens, providing nuts locally. Juglans nigra from North America, and J. × intermedia (J. regia × J. nigra), are also planted on a smaller scale, and used as rootstocks for J. regia.

Juglans spp. are also grown as amenity trees in parks and sold in nurseries (e.g. J. nigra, J. ailanthifolia). The main host of S. clavigignenti-juglandacearum (J. cinerea) is, however, only grown to a very limited extent in Europe.

Host Plants and Other Plants Affected

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Plant nameFamilyContextReferences
Carya cordiformis (bitternut hickory)JuglandaceaeUnknown
Carya illinoinensis (pecan)JuglandaceaeUnknown
Carya ovata (shagbark hickory)JuglandaceaeUnknown
Castanea dentata (American chestnut)FagaceaeUnknown
Castanea mollissima (hairy chestnut)FagaceaeUnknown
Corylus americana (American hazel)BetulaceaeUnknown
Corylus cornuta (beaked hazel)BetulaceaeUnknown
Juglans (walnuts)JuglandaceaeUnknown
Juglans ailantifolia var. cordiformisJuglandaceaeOther
Juglans cinerea (butternut)JuglandaceaeMain
Juglans nigra (black walnut)JuglandaceaeOther
Juglans regia (walnut)JuglandaceaeMain
Prunus serotina (black cherry)RosaceaeUnknown
Quercus alba (white oak)FagaceaeUnknown
Quercus macrocarpa (mossy-cup oak)FagaceaeUnknown
Quercus rubra (northern red oak)FagaceaeUnknown
Quercus velutina (black oak)FagaceaeUnknown

Symptoms

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Cankers can occur on all woody parts of J. cinerea, including twigs, branches, stems and buttress roots. Stem cankers, usually many per tree, separate or joined together, can be present on all sides of the trunk, especially the lower portion. Trees of all ages and sizes, regardless of site conditions, can be infected. Tisserat and Kuntz (1984) found that the disease develops in a characteristic pattern. Young cankers are elongated, sunken areas, which usually originate at leaf scars, lenticels, lateral buds, stomata, bark wounds, natural bark cracks, and even sporadically at points apparently free of any injury. These initial cankers are generally found in the lower crowns. In spring, an inky black, watery exudate issues from canker fissures. In summer, dry sooty black patches remain, often with a whitish margin. If the bark is removed, a brown to black elliptical area of killed cambium can be seen. Small branches and young saplings die rapidly, but most stem cankers of older trees become perennial. These occur mostly on the lower stem and on exposed parts of the roots. Older cankers are surrounded by layers of callus and are vertically oriented, large, open or partly covered by shredded bark. Trees are killed progressively as cankers girdle the stem or kill the crown of the tree. Trunk sprouts and branch suckers often emerge below the girdled area but are infected subsequently and rapidly killed (Kuntz et al., 1979; Ostry, 1997b). Fruits from infected trees are sound and edible according to Kuntz et al. (1979). For a detailed description of symptoms on J. regia and J. nigra, see Orchard (1984).

Another fungus, Melanconis juglandis (anamorph: Melanconium oblongum Berk.), often causes secondary infection (Nicholls et al., 1978), and has been confused with S. clavigignenti-juglandacearum. M. juglandis does not cause cankers. Its anamorphic fruiting bodies appear as very small, dark, smooth bumps on the bark, releasing inky black masses of spores. Spores are usually asymmetrically ovoid, dark and non-septate (Nicholls et al., 1978).

List of Symptoms/Signs

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SignLife StagesType
Stems / canker on woody stem

Biology and Ecology

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S. clavigignenti-juglandacearum was first described by Nair et al. (1979), and its pathogenicity has been demonstrated according to Koch's postulates. Up to now, the teleomorph of the fungus has not been discovered (Furnier et al., 1999). Conidia develop beneath infected bark in sticky masses. Stromatal pegs lift and rupture the bark and, under moist conditions, millions of conidia are extruded in colourless cirri from globose to flattened, single or confluent pycnidia borne in the stroma among the hyphal pegs. These conidia are dispersed by rain splash and wind in little droplets or as aerosols during rainfall (Kuntz et al., 1979; Tisserat and Kuntz, 1983b). Relative humidity of 95-100% was found to aid successful infection greatly (Federspiel and Nair, 1982). Conidia are transported by run-off water from infected branches to tree trunks, infecting wounds and other openings. This results in multiple stem cankers.

The tree is first infected through buds and openings like lenticels, cracked bark, or leaf scars (Kuntz et al., 1979; Ostry, 1997b). Cankers on twigs start to develop, usually in the lower crown, due to the favourable microclimatic conditions in this part of the tree (the branches in the lower crown tend to retain the moisture necessary for spore germination for longer periods than in the upper crown; Tisserat and Kuntz, 1984). Spores of S. clavigignenti-juglandacearum require at least 16 h of dew at 20°C to germinate on the bark of J. cinerea.

In infected suckers, twigs and branches, cell walls of the bark are degraded, macerated and rapidly broken up entirely, resulting in a dark brown sticky residue and a brown exudate. The fungal hyphae penetrate the phloem parenchyma intracellularly and between the phloem fibre elements intercellularly. They advance intracellularly through the uni- and multiseriate xylem ray cells and parenchyma cells. In infected J. cinerea and J. nigra, hyphae in the xylem ray cells appeared larger and darker than those in xylem parenchyma cells. From the xylem, hyphae progress finally into other bark and wood tissues (Kuntz et al., 1979; Nair, 1999). Hyphae also grow beyond cankered tissue, creating new cankers when reaching the cambium (Sinclair et al., 1987).

The fungus is able to sporulate on standing or felled dead trees for at least 20 months (Tisserat and Kuntz, 1982, 1984). Outside the host, conidia can survive for at least 8 h in cool and cloudy weather (Tisserat and Kuntz, 1983c). The pathogen remains viable in diseased tissue and in culture down to 0°C and below. The fungus is seedborne, at least in seeds of J. cinerea and J. nigra (Orchard, 1984; Innes, 1997). This partially explains why J. cinerea does not regenerate after early infection and killing of trees (Ostry, 1997b). In a glasshouse experiment, seedlings of J. cinerea were killed soon after emergence from seeds derived from infected trees that were stratified with intact husks (Orchard, 1984). Additionally, the seedlings are highly susceptible to the fungus and die quickly after infection. It is accordingly not likely that young plants would carry the pathogen if traded as plants for planting. There is no evidence that the fungus can spread on seed or seedlings of J. ailanthifolia.

 

Means of Movement and Dispersal

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The fungus apparently spread rapidly in the USA and Canada. However, infected trees and/or seed were probably moving freely in trade long before the disease was recognized. The pathogen may have gone undetected, as J. cinerea is not very commonly grown. After identification of the fungus, survey intensity increased and this may have given an impression of rapid spread (Cree, 1995).

Spores are dispersed by rain or mist over short distances. By wind, spores can be transported up to 45 m (Tisserat et al., 1981; Tisserat, 1982). Small droplets or aerosols with conidia may be swept above the tree canopy by turbulent air and may possibly spread by wind over distances of more than 1 km (Tisserat and Kuntz, 1983c). Insects, including sap and tissue feeders, are thought to be responsible for long-distance spread of the fungus. Birds may also be vectors. Additionally, insects or birds may, by causing wounds, increase points for infection (Ostry et al., 1994; Nair, 1999). Ostry (1997b) found the fungus on the beetles Laemophlaeus fasciatus, Laemophloeus testareus (Laemophloeidae) and Bactridium spp. (Monotomidae). Halik and Bergdahl (1996; 2002), Bergdahl and Halik (1997) and Katovich and Ostry (1998) found it on Acoptus suturalis (Curculionidae), Astylopsis macula (Cerambycidae), Cossonus platalea (Curculionidae), Eubulus parochus (Curculionidae), Hyperplatys maculata (Cerambycidae), Laemophlaeus biguttatus (Laemophloeidae), and Glischrochilus quadrisignatus (Nitidulidae). Up to 44% of the collected specimens of A. macula and 38% of the specimens of E. parochus carried conidia of S. clavigignenti-juglandacearum. However, disease transmission by these insects does not seem to have been demonstrated.

According to Orchard (1984) and Innes (1997), the fungus can be internally seedborne on J. cinerea and J. nigra, surviving in the cotyledons of infected seed stratified at 4°C up to 18 months (Prey et al., 1997). Seedlings from infected seeds develop basal lesions, stem cankers, stroma, pycnidia and hyphal pegs and die rapidly (Orchard, 1984). Thus, internally infected seeds from infected trees could be present an important pathway for moving S. clavigignenti-juglandacearum to new areas. Movement of scion wood and other propagative material, as well as untreated logs and firewood with bark from diseased trees, may add to the dispersal of the fungus.

Impact

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S. clavigignenti-juglandacearum is a very aggressive plant pest. From 1981 to 1996, in the USA, it killed 58% of the trees of J. cinerea in Wisconsin and 84% in Michigan (Ostry, 1997b). Cummings-Carlson (1993) reported that 91% of J. cinerea trees in Wisconsin were already infested at the time of her survey. In North and South Carolina, the fungus had eliminated J. cinerea to a large extent by 1977 (Anderson and Lamadeleine, 1977) and 77% of J. cinerea trees had been killed in North Carolina and Virginia by 1994 (USDA, 1995; Tainter and Baker, 1996). In USA, good-quality wood of J. cinerea is second in economic value only to J. nigra (Peterson, 1977), for use in interior woodwork, household woodenware, furniture, cabinetry and dye production. Nuts present an important source of wildlife food.

S. clavigignenti-juglandacearum presents a threat to biodiversity in North America. Due to the extensive mortality caused by the fungus and the large amount of already infected trees, J. cinerea was listed as a threatened and endangered species in the USA (Category 2 - more information required prior to formal listing; Ostry et al., 1994), but this category has been eliminated and currently J. cinerea has no official listing status. In Canada, butternut was listed as an endangered species by the Committee on the Status of Endangered Wildlife in Canada (COSEWIC) in November 2003.

Detection and Inspection

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S. clavigignenti-juglandacearum is easily isolated on common nutrient agar media (e.g. potato dextrose agar, malt agar, nutrient dextrose agar) from bark and wood. It grows best at 24-28°C, in light or dark, producing beige to tan colonies, commonly advancing as irregular fans along the margins, darkening the underlying agar subsequently from amber to dark brown. The fungus forms hyphal pegs and pycnidia in culture. It sporulates profusely in the light or dark especially on thin, drying agar cultures (Nair et al., 1979; Kuntz et al., 1979; Nair, 1999). In water, the spores swell slightly in width and shrink in length and look like two spear heads butted together.

Artificial inoculation of J. cinerea, as described by Federspiel and Nair (1982) and Gabka (1996), leads to blackening of the inner bark tissue in 6 days (8 for J. nigra). Removal of the bark reveals a brown to black elliptical area of killed cambium (Ostry, 1997b).

Prevention and Control

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Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Up to now, there is no effectively applied control against S. clavigignenti-juglandacearum. The fungicides benomyl and chlorothalonil have been found to be effective preventive products in laboratory experiments (Nicholls, 1979), but were not approved in the field. Even if an effective mechanical method, fungicide or biocontrol agent existed, it would be difficult to apply it due to the scattered distribution of susceptible trees. Removal of recently killed and visibly infected trees may reduce the amount of inoculum only locally (Nair, 1999).
The only possibility for successful control of the fungus seems to be the selection of resistant forms. Resistance varies greatly between individual trees and is possibly heritable (Ostry, 1997b). Studies are in progress to find, graft, propagate and plant resistant trees of J. cinerea in the USA (Ostry, 1997b).

Phytosanitary Measures

S. clavigignenti-juglandacearum was added in 2005 to the EPPO A2 action list, and EPPO member countries are thus recommended to regulate it as a quarantine pest. Suggested measures could include the prohibition of import of host plants for planting (including seeds) from countries where the pest occurs, or as appropriate origin from a pest-free area or pest-free place of production. It may be noted that J. regia is produced in USA nearly entirely in California, where natural infestation of J. regia has not yet been observed and the fungus does not occur (movement of Juglans spp. from eastern USA to California is restricted).

As a preventive measure in the European and Mediterranean region, countries could restrict the planting of J. cinerea and avoid planting other Juglans spp. in the vicinity of J. cinerea. If the fungus is locally introduced into Europe, measures may also be needed for movement of walnut wood.

References

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Anderson RL, LaMadeleine LA, 1977. The Occurrence of Butternut Decline in the United States. Northeast Area State and Private Forestry Survey Report S-2 -77. Washington, USA: USDA Forest Service

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Broders, K. D., Boland, G. J., 2010. Molecular diagnostic assay for detection of the butternut canker pathogen Sirococcus clavigignenti-juglandacearum. Plant Disease, 94(8), 952-958. doi: 10.1094/PDIS-94-8-0952

Broders, K. D., Boland, G. J., 2011. Reclassification of the butternut canker fungus, Sirococcus clavigignenti-juglandacearum, into the genus Ophiognomonia. Fungal Biology, 115(1), 70-79. doi: 10.1016/j.funbio.2010.10.007

Broders, K. D., Boraks, A., Sanchez, A. M., Boland, G. J., 2012. Population structure of the butternut canker fungus, Ophiognomonia clavigignenti-juglandacearum, in North American forests. Ecology and Evolution, 2(9), 2114-2127. doi: 10.1002/ece3.332

CABI/EPPO, 2008. Sirococcus clavigignenti-juglandacearum. [Distribution map]. Distribution Maps of Plant Diseases, April (Edition 1). Wallingford, UK: CABI, Map 1027

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Nair VMG, Kostichka CJ, Kuntz JE, 1979. Sirococcus clavigignenti-juglandacearum: an undescribed species causing canker on butternut. Mycologia, 71(3):641-646

Nicholls TH, 1979. Butternut canker. In: Walnut Insects and Diseases. General Technical Report NC 52. St Paul, USA: USDA Forest Service, North Central Forest Experiment Station, 73-82

Nicholls TH, Kessler KJ Jr, Kuntz JE, 1978. How to identify butternut canker. 1978, 5pp

Orchard LP, 1984. Butternut Canker; Host Range, Disease Resistance, Seedling-Disease Reactions, and Seed-Borne Transmission. PhD thesis. University of Wisconsin, Madison, USA

Orchard LP, Kuntz JE, Kessler KJ, 1982. Reactions of Juglans species to butternut canker and implications for disease resistance. In: Black Walnut for the Future. USDA. Forest Service General Technical Report NC 74, 27-31. USDA, Washington, USA

Ostry ME, 1997. Butternut canker: history, biology, impact, and resistance. General Technical Report - North Central Forest Experiment Station, USDA Forest Service, No. NC-191:192-199; 22 ref

Ostry ME, 1997. Sirococcus clavigignenti-juglandacearum on heartnut (Juglans ailantifolia var. cordiformis). Plant Disease, 81(12):1461; 2 ref

Ostry ME, Katovich S, Anderson RL, 1997. First report of Sirococcus clavigignenti-juglandacearum on black walnut. Plant Disease, 81(7):830; 2 ref

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Distribution References

Broders K D, Boland G J, 2010. Molecular diagnostic assay for detection of the butternut canker pathogen Sirococcus clavigignenti-juglandacearum. Plant Disease. 94 (8), 952-958. DOI:10.1094/PDIS-94-8-0952

Broders K D, Boland G J, 2011. Reclassification of the butternut canker fungus, Sirococcus clavigignenti-juglandacearum, into the genus Ophiognomonia. Fungal Biology. 115 (1), 70-79. DOI:10.1016/j.funbio.2010.10.007

Broders K D, Boraks A, Sanchez A M, Boland G J, 2012. Population structure of the butternut canker fungus, Ophiognomonia clavigignenti-juglandacearum, in North American forests. Ecology and Evolution. 2 (9), 2114-2127. DOI:10.1002/ece3.332

CABI, EPPO, 2008. Sirococcus clavigignenti-juglandacearum. [Distribution map]. In: Distribution Maps of Plant Diseases, Wallingford, UK: CABI. Map 1027. DOI:10.1079/DMPD/20083091295

EPPO, 2022. EPPO Global database. In: EPPO Global database, Paris, France: EPPO. 1 pp. https://gd.eppo.int/

Harrison K J, Hurley J E, Ostry M E, 1998. First report of butternut canker caused by Sirococcus clavigignenti-juglandacearum in New Brunswick, Canada. Plant Disease. 82 (11), 1282. DOI:10.1094/PDIS.1998.82.11.1282B

NPPO of the Netherlands, 2013. Pest status of harmful organisms in the Netherlands., Wageningen, Netherlands:

Ostry M E, Katovich S, Anderson R L, 1997. First report of Sirococcus clavigignenti-juglandacearum on black walnut. Plant Disease. 81 (7), 830. DOI:10.1094/PDIS.1997.81.7.830D

Ostry M E, Moore M, 2007. Natural and experimental host range of Sirococcus clavigignenti-juglandacearum. Plant Disease. 91 (5), 581-584. DOI:10.1094/PDIS-91-5-0581

Seebens H, Blackburn T M, Dyer E E, Genovesi P, Hulme P E, Jeschke J M, Pagad S, Pyšek P, Winter M, Arianoutsou M, Bacher S, Blasius B, Brundu G, Capinha C, Celesti-Grapow L, Dawson W, Dullinger S, Fuentes N, Jäger H, Kartesz J, Kenis M, Kreft H, Kühn I, Lenzner B, Liebhold A, Mosena A (et al), 2017. No saturation in the accumulation of alien species worldwide. Nature Communications. 8 (2), 14435. http://www.nature.com/articles/ncomms14435

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