Leptographium procerum
(white pine root decline)

Identity

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Preferred Scientific Name

• Leptographium procerum W.B. (Kendr.) M.J. Wingf. 1985

Preferred Common Name

• white pine root decline

Other Scientific Names

• Verticicladiella procera W.B. Kendr. 1962

International Common Names

• English: Leptographium root decline; Procerum root disease; white pine root disease; white pine wilt

EPPO code

• LEPGPR (Leptographium procerum)

Summary of Invasiveness

Top of page It has been suggested, on the basis of circumstantial evidence, that L. procerum was introduced into New Zealand together with Hylurgus spp. (Wingfield and Gibbs, 1991). The same may be true for South Africa where pines are planted as exotic crops.

Taxonomic Tree

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• Domain: Eukaryota
•     Kingdom: Fungi
•         Phylum: Ascomycota
•             Subphylum: Pezizomycotina
•                 Class: Sordariomycetes
•                     Subclass: Sordariomycetidae
•                         Order: Ophiostomatales
•                             Family: Ophiostomataceae
•                                 Genus: Leptographium
•                                     Species: Leptographium procerum

Notes on Taxonomy and Nomenclature

Top of page White pine root decline had been documented as a serious disease on pines for a number of years before the causal agent was first described by Kendrick (1962) as Verticicladiella procera. The genus Verticicladiella belonged to a complex of morphologically similar genera known as the Leptographium-complex (Kendrick, 1962). The genera Leptographium and Phialocephala also formed part of this complex. The three genera in the complex were distinguished on the basis of their respective modes of conidiogenesis. Species in Leptographium were characterized by annellidic conidium development, whereas species in Verticicladiella and Phialocephala were characterized by sympodial and phialidic conidium development, respectively.

Wingfield (1985) reduced Verticicladiella to synonymy with Leptographium. This synonymy was based on the fact that species in the two genera were indistinguishable under the light microscope. These findings were confirmed by Van Wyk and Wingfield (1987) and Van Wyk et al. (1988) who showed that delayed secession of the conidia that develop percurrently can lead to a false impression of sympodial development when viewed under the light microscope. Verticicladiella procera was transferred to Leptographium and renamed as Leptographium procerum (Wingfield, 1985).

Disease symptoms caused by L. procerum have been described under several different names. The first of these was white pine root decline, which occurs on Pinus strobus (Leaphart, 1960) and in Christmas tree plantations where it can reach epidemic proportions (Lackner and Alexander, 1982). This disease was also known as Leptographium root decline (Dochinger, 1967), white pine wilt and white pine root disease (Lackner and Alexander, 1982) before it was suggested that the name Procerum root disease should be used (Alexander et al., 1988). Red pine decline disease on Pinus resinosa has also been attributed to L. procerum infection (Klepzig et al., 1995).

Description

Top of page L. procerum can be characterized as a typical species of Leptographium (Jacobs and Wingfield, 2001). The conidiophores can occur singly or in groups of up to three, directly from the mycelium and are (150-) 245-570 (-760) µm long with rhizoid-like structures present at the base. As in the case with other species of Leptographium, the stipes are olivaceous, cylindrical, 3-10-septate and (125-) 206-496 (-690) µm long. The conidiogenous apparatus consists of two to five series of cylindrical branches that are (25-) 39-75 (-90) µm long, excluding the conidial mass. The conidiogenous apparatus terminates in conidiogenous cells that are cylindrical, tapering slightly at the apex, (11-) 15-18 (-22) µm long and 1-2 µm wide. The conidia are hyaline, aseptate, obovoid to broadly ellipsoid with truncate bases and rounded apices, and 3-5 x 1-3 µm (Kendrick, 1962; Jacobs and Wingfield, 2001). Strains of L. procerum were found to grow and sporulate equally well on PDA and MEA, although the pathogen grows slightly faster on PDA (Kendrick, 1962).

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.

Risk of Introduction

Top of page Some studies have indicated that L. procerum is only a weak pathogen (Towers, 1977; Livingston and Wingfield, 1982; Wingfield, 1982, 1986; Wingfield et al., 1988; Harrington and Cobb, 1993). This is illustrated by the fact that in some cases only the symptoms of the disease have been reported, without any trace of a vector or Leptographium sp. The cause of these symptoms has therefore been attributed to factors such as high soil moisture and not to the fungus (Prey, 1975). Houston (1969) found that L. procerum does not kill as many trees as other pathogens. Sinclair and Hudler (1980) indicated that L. procerum is frequently associated with mortality of red pine on poorly drained soils, although there is no evidence to suggest that it is directly responsible for the mortality. Harrington and Cobb (1983) indicated that L. procerum is not virulent and is unable to kill wounded or unwounded Douglas fir (Pseudotsuga menziesii). Wingfield (1983, 1986), who considered L. procerum to be a weak pathogen, confirmed this. In another study, lesions produced by L. procerum on Pinus taeda were not found to be significantly longer than those on controls (Nevill et al., 1995).

L. procerum has also been isolated from severely diseased trees (Leaphart, 1960). Lackner and Alexander (1982) viewed the fungus as the cause of severe losses in Christmas tree plantations. In contrast to the results of Harrington and Cobb (1983) and Wingfield (1983, 1986), pathogenicity tests carried out by Halambek (1976, 1981) and Alexander et al. (1988) using isolates of L. procerum confirmed its ability to kill seedlings. Nevill and Alexander (1992a) postulated that the lack of foliar symptoms observed by Wingfield (1986) might be as a result of a long latent period of this fungus.

The debate surrounding the role of L. procerum as a conifer pathogen has not been fully resolved. The fungus is substantially less virulent than L. wageneri and a general consensus seems to be that it cannot kill trees independently. It is commonly associated with root and root collar insects (Wingfield, 1983). Symptoms associated with insects such as pine root collar weevil (Hylobius radicis) on young trees are similar to those reported for white pine root decline and this may have led to confusion relating to the role of L. procerum as a pathogen (Wingfield, 1986). It is therefore difficult to predict the impact L. procerum will have if introduced to a new area.

Habitat

Top of page L. procerum can be isolated from discoloured roots of symptomatic trees (Livingston and Wingfield, 1982) or from soil in close proximity to diseased roots (Wingfield, 1983). It has also been isolated from various insects, especially bark beetles that infest conifers (Klepzig et al., 1995).

Hosts/Species Affected

Top of page L. procerum occurs exclusively on coniferous hosts, mainly on eastern white pine (Pinus strobus). L. procerum can also infect other species of pine, but the symptoms and disease development differ from those observed in P. strobus (Horner and Alexander, 1983a, b). L. procerum has also been isolated from dying red pine (Pinus resinosa) and Scots pine (P. sylvestris) (Sinclair and Hudler, 1980).

Hosts trees of L. procerum include: Abies fraseri (Alexander et al., 1988), A. grandis (Lane and Goheen, 1979), Picea abies (Hallaksela, 1977; Alexander et al., 1988), Pinus banksiana (Kendrick, 1962; Wingfield, 1982, 1983; Alexander et al., 1988), P. clausa (Barnard et al., 1985; Alexander et al., 1988), P. contorta (Alexander et al., 1988; Bertagnole et al., 1983), P. echinata (Horner and Alexander, 1983a; Alexander et al., 1988), P. elliotii (Horner and Alexander, 1983a; Alexander et al., 1988; Barnard et al., 1991), P. monticola (Hubert, 1953; Alexander et al., 1988), P. nigra (Lackner and Alexander, 1982; Livingston and Wingfield, 1982; Wingfield, 1982; Alexander et al., 1988), P. palustris (Otrosina et al., 1999, 2002), P. pinaster (Morelet, 1986), P. ponderosa (Wingfield, 1982; Alexander et al., 1988), P. radiata (Mackenzie and Dick, 1984; Farrell et al., 1997a, b), P. resinosa (Kendrick, 1962; Towers, 1977; Sinclair and Hudler, 1980; Halambek, 1981; Livingston and Wingfield, 1982; Wingfield, 1982; Harrington, 1988; Alexander et al., 1988), P. strobus (Kendrick, 1962; Dochinger, 1967; Halambek, 1976; Houston, 1969; Towers, 1977; Shaw and Dick, 1979; Sinclair and Hudler, 1980; Lackner and Alexander, 1982, 1984; Livingston and Wingfield, 1982; Wingfield, 1982; Horner and Alexander, 1983a, b; Mackenzie and Dick, 1984; Alexander et al., 1988; Smith, 1991), P. sylvestris (Wingfield and Gibbs, 1991; Lackner and Alexander, 1982, 1984; Wingfield, 1982; Horner and Alexander, 1983b; Rane and Tattar, 1987; Alexander et al., 1988; Harrington, 1988); P. taeda (Horner and Alexander, 1983a; Alexander et al., 1988; Nevill et al., 1995), P. thunbergii (Rane and Tattar, 1987), P. virginiana (Horner and Alexander, 1983a; Alexander et al., 1988) and Pseudotsuga menziesii (Alexander et al., 1988; Morrison and Hunt, 1988).

Growth Stages

Top of page Vegetative growing stage

Symptoms

Top of page White pine root decline was first reported in eastern USA and L. procerum was later found to be consistently isolated from diseased trees (Kendrick, 1962; Dochinger, 1967). However, the role of the fungus in causing this disease has been a matter of considerable debate (Lackner and Alexander, 1982; Harrington and Cobb, 1983; Wingfield, 1983, 1986). The disease is commonly referred to as a root decline but in most cases manifests itself as a wilt (Lackner and Alexander, 1982). The symptoms of the disease are similar to those caused by infestation by the root-collar weevil (Hylobius radicis) (Wingfield, 1983), for which it can be easily mistaken.

In inoculation studies using Leptographium isolated from western white pine (Pinus monticola), symptoms appeared about 25-35 days after inoculation and tree death occurred 35-40 days after inoculation (Hubert, 1953). One of the first symptoms to appear, in both inoculation studies and natural infections, is a reduction in height growth, followed by crown discoloration. A dark stain can be observed in the roots of the diseased trees, which rapidly progresses upwards in the tree (Leaphart, 1960; Alexander et al., 1988). In severe infections, marked resin exudation is observed (Alexander et al., 1988). Symptoms associated with white pine root decline include extended periods of bud break, retardation of shoot elongation, crooking of growing shoots, loss of turgour in older needles, wilting of younger needles (Hubert, 1953; Dochinger, 1967; Halambek, 1976; Pest Alert, 1977; Smith, 1991), retention of needles, needle wilt, browning of needles, and resin-soaked, black-streaked wood at the base of stems and basal cankers (Houston, 1969; Pest Alert, 1977; Towers, 1977; Anderson and Alexander, 1979; Mackenzie and Dick, 1984; Alexander et al., 1988; Smith, 1991; Otrosina et al., 1997). The basal cankers are at first circular to irregular, reddish, sunken areas, which in some cases enlarge and coalesce to form larger flattened cankers (Houston, 1969). Colonized roots are resin-soaked and cross-sections of the stems reveal prominent wedges of blue-stained wood. Discoloration of the sapwood is consistent with the patterns and physiology of blue-stain fungi (Alexander et al., 1988). In some cases the roots show diffuse black streaking (Livingston and Wingfield, 1982).

L. procerum acts in a similar way to wilt pathogens. It occurs in the vascular system, where it erodes the cell walls and travels from cell to cell through the pits (Kilbertus et al., 1980). White pine infected with L. procerum showed greater vascular occlusion, lower moisture content and reduced hydraulic conductivity than non-infected trees (Butnor et al., 2000). The water in the stem is reduced, leading to desiccation of the sapwood and foliage and ultimately premature death (Butnor et al., 2000).

Reduced water potential in symptomatic trees supports the notion that this root disease is associated with xylem dysfunction (Horner et al., 1987). Tree death occurs when the xylem is blocked by resin (Alexander et al., 1988). Symptoms were found to vary between Pinus strobus and P. sylvestris; it takes longer for symptoms to appear on P. sylvestris (Horner and Alexander, 1983b).

Red pine decline disease is characterized by circular regions of dead and dying trees that expand gradually. The root systems of these trees show high levels of mortality and several fungi (L. terebrantis, L. procerum and Ophiostoma ips) can be isolated from stained areas (Klepzig et al., 1995; Erbilgin and Raffa, 2002).

List of Symptoms/Signs

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Biology and Ecology

Top of page Genetics

Jacobs et al. (2001) found that L. procerum was phylogenetically most closely related to Leptographium terebrantis. Although they share a common habitat, these species are morphologically distinct.

Physiology and Phenology

L. procerum is characterized by the presence of cellulose in its cell walls, a characteristic shared with other species of Ophiostoma (Horner et al., 1986).

Hubert (1953) showed that extracts from L. procerum could induce wilt and death in tomato seedlings, indicating that a toxin could be involved.

Environmental Requirements

White pine root decline appears to be linked to stress conditions (Alexander et al., 1988). The disease was found to be prevalent in areas with heavy soil moisture or drought conditions (Prey, 1975). It was also noticed in trees planted in poorly-drained sites and those infested by other pathogens (Towers, 1977). L. procerum, together with L. terebrantis, was isolated from symptomatic and asymptomatic trees that were stressed as a result of prescribed burning practices (Otrosina et al., 2002). The presence of L. procerum in Pinus palustris could also be seen as an indicator of stress (Otrosina et al., 1999). Trees exposed to air pollution are also more prone to infection by L. procerum and insects (Lackner and Alexander, 1983).

Red pine decline, which is also associated with the presence of L. procerum, mainly occurs on sandy soils. Stressed conditions can play a role in this disease as they create favourable conditions for attack by the insects that vector the fungus (Klepzig et al., 1991).

Associations

L. procerum has been isolated from the roots of trees infested with black stain root disease (Bertagnole et al., 1983). This disease is caused by a species in the same genus, Leptographium wageneri. Both white pine root decline and red pine decline appear to be caused by a complex of organisms, involving a number of insects and beetles, rather than by a single organism (Otrosina et al., 1999; Erbilgin and Raffa, 2002). Although L. procerum has been associated with the symptoms of white pine root decline, it does not seem to be the primary cause of the disease (Hubert, 1953).

The disease is not prevalent on healthy, unstressed trees, but readily occurs on trees that are stressed (Livingston and Wingfield, 1982). L. procerum appears to be of minor importance in tree mortality and occurs in weevil-damaged trees (Wingfield, 1982; Nevill and Alexander, 1992a). In most cases, L. procerum is isolated, together with L. terebrantis, from trees showing symptoms of insect damage (Livingston et al., 1983; Wingfield, 1983; Rane and Tattar, 1987). L. terebrantis appears to be more virulent than L. procerum (Rane and Tattar, 1987; Klepzig et al., 1996). Barnard et al. (1985) reported that in half of the cases of sand pine root disease, L. procerum was isolated together with a known root pathogen. Houston (1969) found that cankers on Pinus strobus caused by L. procerum infection were almost always associated with damage by snow, ice and the activities of ants.

Means of Movement and Dispersal

Top of page Natural Dispersal (non-biotic)

L. procerum can spread over short distances through soil or root contact. Propagules of L. procerum can survive in the soil around infected hosts for a short period of time (Lackner and Alexander, 1984; Alexander et al., 1988). These propagules are sparsely, and not uniformly, distributed throughout the soil and are therefore unlikely to be the major source of infection (Lewis and Alexander, 1985; Lewis et al., 1987; Alexander et al., 1988). L. procerum can also be spread through root contact between infected and uninfected trees (Lackner and Alexander, 1984).

Vector Transmission

L. procerum is known to be associated with insects, especially weevils (Wingfield, 1985; Lewis and Alexander, 1986; Nevill and Alexander, 1992a, c; Lévieux et al., 1994). These insects usually feed on the roots and root collar. Wingfield et al. (1988) proposed that the association of L. procerum with these insects explains the occurrence of the fungus in trees other than those dying from white pine root decline.

Trees infected with L. procerum are usually also infested with insects that may act as vectors for the fungus (Alexander et al., 1988). Weevils are the main vectors, with bark beetles less commonly associated with the fungus (Wingfield, 1983; Lewis and Alexander, 1986; Horner et al., 1987; Alexander et al., 1988). Volatiles such as ethanol and terpenes are often released from trees infected with L. procerum and may play an important role in the association of the insects with the trees (Nevill and Alexander, 1992a).

Insects associated with L. procerum are: Dendroctonus frontalis (Otrosina et al., 1997), Dendroctonus valens (Wingfield, 1983; Rane and Tattar, 1987; Harrington, 1988; Klepzig et al., 1991), Dendroctonus terebrans (Harrington, 1988; Perry, 1991), Hylastes sp. (Lewis and Alexander, 1986; Alexander et al., 1988), Hylastes ater (Mackenzie and Dick, 1984), Hylastes opacus (Wingfield and Gibbs, 1991), Hylastes abietis (Lévieux et al., 1994), Hylastes pales (Lackner and Alexander, 1982; Wingfield, 1983; Lewis and Alexander, 1986; Alexander et al., 1988; Klepzig et al., 1991; Nevill and Alexander, 1992a, b, c, d), Hylobius radicis (Wingfield, 1982, 1983; Alexander et al., 1988; Klepzig et al., 1991), Hylobius rhizophagus [H. assimilis] (Wingfield, 1982, 1983; Alexander et al., 1988), Hylobius porculus (Klepzig et al., 1991), Hylurgus ligniperda (Mackenzie and Dick, 1984), Hylurgops palliatus (Wingfield and Gibbs, 1991), Hylurgops porosus (Wagner, 1977), Ips typographus (Harrington, 1988), Orthotomicus spp. (Lewis and Alexander, 1986; Alexander et al., 1988), Pachylobius picivorus (Wingfield, 1983; Alexander et al., 1988; Klepzig et al., 1991), Pissodes spp. (Lewis and Alexander, 1986), Pissodes nemorensis (Lackner and Alexander, 1982; Alexander et al., 1988; Nevill and Alexander, 1992a, b, c, d), Pissodes pini (Kendrick, 1962; Livingston and Wingfield, 1982), Pityokteines sp. (Lackner and Alexander, 1984; Alexander et al., 1988), Pityogenes sp. (Lackner and Alexander, 1984; Lewis and Alexander, 1986; Harrington, 1988; Alexander et al., 1988), Pityophthorus sp. (Lackner and Alexander, 1984; Alexander et al., 1988), Tomicus piniperda (Gibbs and Inman, 1991) and Xyleborus sp. (Lewis and Alexander, 1986; Alexander et al., 1988).

Three root-feeding weevils, Hylobius radicis, H. pales and Pachylobium picivorus, are implicated in the cause of red pine decline (Klepzig et al., 1991).

Silvicultural Practices

Cultural practices that can cause wounds on the roots of Pinus trees should be seen as a risk factor for increasing white pine root decline (Horner and Alexander, 1983a), as damaged roots allow entry of the fungus. This disease is prevalent in areas where roads have been cleared or trees thinned out (Shaw and Dick, 1979). L. procerum could pose a threat to the regeneration of seedlings as it can easily spread through root grafts (Otrosina et al., 1999).

Plant Trade

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Plant parts not known to carry the pest in trade/transport
Leaves

Impact Summary

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Impact

Top of page White pine root decline is now known to occur in various parts of the world in a number of ecosystems, and is not restricted to forest trees (Livingston and Wingfield, 1982; Morelet, 1986; Alexander et al., 1988; Morrison and Hunt, 1988; Smith, 1991). The extent of damage associated with the disease has not been fully assessed (Towers, 1977; Meyer et al., 1983).

Environmental Impact

Top of page L. procerum is indigenous to North America and its impact appears to be greater in planted areas such as plantations than in natural forest. It does not cause disease symptoms in healthy, unstressed trees, and should have a low impact in healthy forests.

Diagnosis

Top of page Several selective media have been described for the isolation of L. procerum. McCall and Merrill (1980) suggested the use of acidic malt agar with 500 mg/l cycloheximide; the growth of most other fungi is inhibited at this concentration (McCall and Merrill, 1980). Swai and Hindal (1981) proposed the use of Verticicladiella procera isolation media (VPIM) for the selective recovery of L. procerum. The medium consisted of 2 g glucose, 0.2 mg iron, 0.2 mg zinc, 0.1 mg manganese, 50 mg chlorotetracycline hydrocholoride, 50 mg cycloheximide and 50 mg streptomycin in 1 litre of distilled water with 15 g agar (Swai and Hindal, 1981).

Detection and Inspection

Top of page The greatest recovery of L. procerum can be made from discoloured areas in the roots and root collars of infected trees (Horner et al., 1987). Insect activity at the base of trees may be an indication that the tree is under stress and therefore likely to be infested with L. procerum. Other indications of white pine root decline are a black crust and resin soaking at the base of the tree. Uniform discoloration of the foliage may also indicate the presence of L. procerum (Alexander et al., 1988).

Similarities to Other Species/Conditions

Top of page White pine root decline refers to a symptom. The consistent association of L. procerum with diseased trees does not imply that the fungus causes the disease. However, the association of the fungus with opportunistic insects that feed in the roots and root collars of stressed trees means that L. procerum is commonly found in those parts of trees displaying symptoms of white pine root decline (Wingfield, 1983; Wingfield et al., 1988).

Kendrick (1962) considered L. procerum to be similar to L. abietinum. These species could be distinguished on the basis of the broader, uncurved conidia, longer sporogenous apparatus and primary branches of L. procerum. L. procerum is also similar to L. alethinum, L. pityophilum and L. euphyes. All three species were initially misidentified as L. procerum, but can be separated from it on the basis of clear morphological differences. The most prominent distinguishing character is probably the characteristic concentric rings formed by mycelium of L. procerum in culture (Jacobs and Wingfield, 2001; Jacobs et al. 2001).

Leptographium albopini shares a habitat with L. procerum and has been isolated from the roots of Pinus strobus and P. edulis. However, it is easily distinguished from L. procerum by the conidiophores, which occur singly in L. albopini, not arranged in groups as in L. procerum (Wingfield et al., 1994). The conidia of L. albopini are also slightly larger than those of L. procerum (Wingfield et al., 1994).

Wingfield and Marasas (1980) isolated a species of Leptographium from the roots of Pinus pinaster in South Africa and described it as Verticicladiella alacris. This species differed from L. procerum in that the conidiophores were not arranged in groups as in L. procerum (Wingfield and Marasas, 1980). L. alacris was later synonymized with L. serpens, and is characterized by serpentine hyphal growth (Wingfield and Marasas, 1981).

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.

Procerum root disease can be controlled by planting trees on sites suitable for the species, controlling weevils and bark beetles, removing slash in and around the plantation, and controlling weeds (Alexander et al., 1988). It is advisable to allow sites to lie fallow for 1 year or to consider planting non-susceptible trees (Lewis, 1985). Salmon et al. (1996) found that some natural compounds (e.g. R (-) carvone, S (-) carvone and limonin) could inhibit the germination of L. procerum conidia. However, these compounds only suppressed germination of the conidia and did not affect the growth of the fungus (Salmon et al., 1996).

References

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Alexander SA; Horner WE; Lewis KJ, 1988. Leptographium procerum as a pathogen of pines. In: Harrington TC, Cobb FW Jr, eds. Leptographium Root Diseases on Conifers. St Paul, Minnesota, USA: American Phytopathological Society Press, 97-112.

Anderson RL; Alexander SA, 1979. How to identify and control white pine root decline. Forestry Bulletin, SA-FR/P6.

Barnard EL; Blakeslee GM; English JT; Oak SW; Anderson RL, 1985. Pathogenic fungi associated with sand pine root disease in Florida. Plant Disease, 69(3):196-199

Barnard EL; Gilly SP; Dixon WN, 1991. Incidence of Heterobasidion annosum and other root-infecting fungi in residual stumps and roots in thinned slash pine plantations in Florida. Plant Disease, 75(8):823-828

Bertagnole CL; Woo JY; Partridge AD, 1983. Pathogenicity of five Verticicladiella species to lodgepole pine. Canadian Journal of Botany, 61(7):1861-1867

Butnor JR; Seiler JR; Gray JA, 2000. Influence of procerum root disease on the water relations of eastern white pine (Pinus strobus L.). Journal of Sustainable Forestry, 10(1/2):95-105; 14 ref.

Dochinger LS, 1967. Leptographium root decline of eastern white pine. Phytopathology, 57:809.

Erbilgin N; Raffa KF, 2002. Association of declining red pine stands with reduced populations of bark beetle predators, seasonal increases in root colonizing insects, and incidence of root pathogens. Forest Ecology and Management, 164(1/3):221-236; many ref.

Farrell RL; Duncan SM; Ram AP; Kay SJ; Hadar E; Hadar Y; Blanchette RA; Harrington TC; McNew D, 1997. Causes of sapstain in New Zealand. FRI Bulletin, No. 204:25-29; 13 ref.

Farrell RL; Hadar E; Kay; SJ; Blanchette RA; Harrington TC, 1997. Survey of sapstain organisms in New Zealand and albino anti-sapstain fungi. Proceedings: Biology and Prevention of Sapstain. British Columbia, Canada: Whistler.

Gibbs JN; Inman A, 1991. The pine shoot beetle Tomicus piniperda as a vector of blue stain fungi to windblown pine. Forestry (Oxford), 64(3):239-249

Halambek M, 1976. Dieback of eastern white pine (Pinus strobus L.) in cultures. Agriculturae Conspectus Scientificus, 39:495-498.

Halambek M, 1981. Verticicladiella procera Kendrick, the pathogen of wilt of Eastern white pine in conifers. Zastita Bilja, 32(3):313-323

Hallaksela A-M, 1977. Microbial flora isolated from Norway spruce stumps. Acta Forestalia Fennica, 158:50 pp.

Harrington TC, 1988. Leptographium species, their distributions, hosts and insect vectors. In: Harrington TC, Cobb FW Jr, eds. Leptographium Root Diseases on Conifers. St Paul, Minnesota, USA: American Phytopathological Society Press, 1-39.

Harrington TC; Cobb FW Jr, 1983. Pathogenicity of Leptographium and Verticicladiella spp. isolated from roots of western North American conifers. Phytopathology, 73(4):596-599

Horner WE; Alexander SA; Julian MM, 1986. Qualitative determination of cellulose in the cell walls of Verticicladiella procera. Mycologia, 78(2):300-303

Horner WE; Alexander SA; Lewis KJ, 1987. Colonization patterns of Verticicladiella procera in Scots and eastern white pine and associated resin-soaking, reduced sapwood moisture content, and reduced needle water potential. Phytopathology, 77(4):557-560

Houston DR, 1969. Basal canker of white pine. Forest Science, 15:66-83.

Hubert EE, 1953. Studies of Leptographium isolated from western white pine. Phytopathology, 43:637-641.

Jacobs K; Wingfield MJ, 2001. Leptographium Species. Tree pathogens, insect associates and agent of bluestain. St Paul, MN, USA: APS Press.

Jacobs K; Wingfield MJ; Uzunovic A; Frisullo S, 2001. Three new species of Leptographium from pine. Mycological Research, 105(4):490-499; 26 ref.

Jacobs K; Wingfield MJ; Wingfield BD, 2001. Phylogenetic relationships in Leptographium based on morphological and molecular characters. Canadian Journal of Botany, 79(6):719-732; 65 ref.

Kendrick WB, 1962. The Leptographium complex. Verticicladiella S.Hughes. Canadian Journal of Botany, 40:771-797.

Kilbertus G; Mangenot F; Radtke D, 1980. Deterioration of beech (Fagus silvatica L.) timber by Fusarium solani (Mart.) Sacc. and Verticicladiella procera Kendrick. Cryptogamie Mycologie, 1(2):97-104

Klepzig KD; Raffa KF; Smalley EB, 1991. Association of an insect-fungal complex with red pine decline in Wisconsin. Forest Science, 37(4):1119-1139

Klepzig KD; Raffa KF; Smalley EB, 1995. Dendroctonus valens and Hylastes porculus (Coleoptera: Scolytidae): vectors of pathogenic fungi (Ophiostomatales) associated with red pine decline disease. The Great Lakes Entomologist, 28:81-87.

Klepzig KD; Raffa KF; Smalley EB, 1996. Interactions of ecologically similar saprogenic fungi with healthy and abiotically stressed conifers. Forest Ecology and Management, 86:163-169.

Lackner AL; Alexander SA, 1982. Occurrence and pathogenicity of Verticicladiella procera in Christmas tree plantations in Virginia. Plant Disease, 66(3):211-212

Lackner AL; Alexander SA, 1983. Root disease and insect infestations on air-pollution-sensitive Pinus strobus and studies of pathogenicity of Verticicladiella procera. Plant Disease, 67(6):679-681

Lackner AL; Alexander SA, 1984. Incidence and development of Verticicladiella procera in Virginia Christmas tree plantations. Plant Disease, 68(3):210-212

Lane BB; Goheen DJ, 1979. Incidence of root disease in bark beetle-infested eastern Oregon and Washington true firs. Plant Disease Reporter, 63(4):262-266

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