Gibberella circinata
(pitch canker)

G. circinata gained its reputation as an invasive pest following its discovery in California, USA, in 1986. Although the disease was well established by that time, it is clear the infestation expanded rapidly over the next 10 years. For example, surveys revealed no evidence of pitch canker in the native forest on the Monterey Peninsula prior to 1992. Thereafter, the incidence and severity of the disease increased dramatically. The rapid development of pitch canker in coastal California can be attributed to the widespread availability of a highly susceptible host (Pinus radiata), a conducive climate and an abundance of pine-associated insects capable of serving as vectors and wounding agents. Since the discovery of pitch canker in California, the disease has also been found in Japan where it appears to be a recent introduction (Wikler and Gordon, 2000). G. circinata has also become established as a pathogen in pine seedling nurseries in South Africa (Viljoen et al., 1994), Spain (Dwinell, 1999b) and Chile (Wingfield et al., 2002). The ability of the pathogen to be moved as infested seed, to survive in soil and to establish latent infections on seedlings greatly facilitate its potential for dispersal and establishment wherever susceptible pines are grown.

In the USA, pitch canker occurs in nine states in the south-east and in coastal, but not inland, areas of California. There is a single report of pitch canker from the state of Indiana on nursery stock of P. strobus. Records for the states of Washington and Massachusetts which were published in the 1998 CABI/EPPO distribution map for G. circinata are incorrect; pitch canker has never been reported from these states (Ridley and Dick, 2000). Records of pitch canker from Italy (Motta, 1986) and Iraq (Khalisy et al., 1981) are questionable. These reports were based on isolation of Fusarium moniliforme var. subglutinans from seed (Italy) or nursery stock exhibiting damping-off (Iraq). Due to the ambiguous taxonomy of the pine pathogen over time (see Notes on Taxonomy and Nomenclature) and the fact that pathogenicity of these isolates to pines was not demonstrated, it is uncertain whether these were the pitch canker pathogen. The absence of any subsequent reports from these areas suggests they were not. No further observations on the occurrence of pitch canker in Haiti have been published since the original report by Hepting in 1953. In Mexico, the disease is known from at least 15 states. In Chile and South Africa the disease is now well established but is known only from nurseries. It is present in Japan but may be more important in Korea (J Kim, University of Seoul, Korea, personal communication).

Pitch canker is a disease of great concern to countries where Pinus radiata is an important timber species. Thus quarantine restrictions are in force in New Zealand and Australia. Contaminated seed probably poses the greatest risk for introduction of the pathogen to new areas.

The distinction drawn in the list of hosts between 'main' and 'other' hosts is somewhat arbitrary, and is based primarily on published reports of economic damage. The most important cultivated hosts are Pinus radiata, P. patula, P. elliotii var. elliotii, P. taeda and P. virginiana. Other hosts are less damaged because they are either: inherently less susceptible to the pathogen; exposed to lower disease pressure due to location, climate or levels of insect vector activity; or found in natural or less intensively managed systems. Further information on relative susceptibility of some of these hosts can be obtained from the literature (Dwinell, 1978; Dwinell et al., 1985; Storer et al., 1997; Guerra-Santos, 1999; Hodge and Dvorak, 2000; Gordon et al., 2001).

In addition to the species listed in the table, which have been observed to be naturally infected, a number of hosts have been discovered through artificial inoculations in the greenhouse or laboratory. These include Pinus contorta var. murryana, P. eldarica [P. brutia var. eldarica], P. jeffreyi, P. lambertiana and P. monophylla (McCain et al., 1987; Storer et al., 1994; Gordon et al., 1996, 1998a).

The teleomorph is readily formed under laboratory conditions and may occur in nature, but the anamorphic stage (Fusarium circinatum) predominates. Two asexual propagules, macroconidia and microconidia, are presumed to be the primary form in which the pathogen is disseminated, either by wind or by insects to which spores can adhere. Bark-feeding insects commonly breed in pitch canker-killed branches and a large percentage of the emergent brood carry the pathogen. These insects (including numerous species in the genera: Pityophthorus, Ips and Conophthorus) cannot only transport the pathogen to a new host but may also provide a wound suitable for infection and thus serve as vectors of pitch canker (Storer et al., 1997). These and other insects may also serve as wounding agents for fungal propagules already present on host surfaces.

The suitability of a wound for infection may depend on how rapidly it dries out. Thus, superficial wounds may require ambient moisture for an infection to occur, which could impose environmental constraints on the above-ground activity of the pathogen. Indeed, where the foliar phase of pitch canker is a problem, infections appear to be associated with locations/seasons where atmospheric moisture is readily available and temperatures are relatively warm, such as in the south-eastern USA during summer thunderstorms (Dwinell et al., 1985). In California, the disease is most severe in close proximity to the coast. The distribution of the disease also suggests that cooler temperatures are restrictive (Gordon et al., 2001). At moderate temperatures the pathogen survives for 1 year or more in infected wood. Spores can survive in soil for from several months to a year or more, depending on conditions. The climatic limitations on pitch canker are less likely to apply to the seedling phase of the disease, because conditions that are conducive to root growth in soil would generally also be suitable for infection by G. circinata.

Incidence

G. circinata can infest seed internally or be present as a superficial contaminant (Barrows-Broaddus and Dwinell, 1985; Storer et al., 1998). The mechanisms by which G. circinata infests seed are unknown. Superficial contamination might occur when airborne propagules enter the cone during periods when the cone is open. For cones on infected branches, fungal hyphae might grow from the lesion on the branch, through the cone stalk and into the seed. In Pinus radiata in California, the pathogen was isolated from up to 83% of seeds collected from cones on recently infected branches and from 21% of seeds from cones on symptomless branches (Storer et al., 1998). Seeds from symptomless branches were superficially contaminated, while up to 64% of seeds from recently infected branches were internally infested. The pathogen has similarly been isolated from seed of P. elliotii var. elliotii (Miller and Bramlett, 1979), P. taeda (Miller et al., 1984), P. palustris (Runion and Bruck, 1988), and P. echinata (Dwinell, 1999a).

Effect on Seed Quality

Internal infestations have been associated with deterioration of seed. Radiographs of infected seeds have shown the gametophyte shrunken from the seed coat and a slight deterioration of the embryo, while microscopy revealed hyphal growth and a lack of cellular organization of the seed tissues (Barrows-Broaddus and Dwinell, 1985). In a study of P. radiata, emergence from infested seed was reduced to 9%, down from 67% emergence from comparable uninfested seed (Storer et al., 1998). Similar levels of emergence have been observed for infested seed lots of P. palustris (Runion and Bruck, 1988).

Pathogen Transmission

Infection or contamination of seed may result in pre- or post-emergence damping-off or late season mortality of older, woody seedlings (Barnard and Blakeslee, 1980; Blakeslee et al., 1981; Storer et al., 1998).

Seed Treatments

For seeds that are only externally contaminated, the pathogen can be eliminated by soaking in 1% sodium hypochlorite for 2 minutes (Storer et al., 1998); 30% hydrogen peroxide has also been used for this purpose (Dwinell, 1999a). For seed that is infected internally, systemic fungicides have been used to increase emergence and reduce damping-off. Effective fungicides include thiabendazole-dimethyl sulfoxide (Runion and Bruck, 1988) and a formulated mixture of thiabendazole with carboxin and thiram (TR Gordon, University of California-Davis, USA, personal communication).

Seed Health Tests

The standard method by which G. circinata is detected on seed is by plating the seed on a Fusarium-selective medium (Correll et al., 1991). To discriminate between internal and external infections, half of the seed can be treated with sodium hypochlorite to eliminate external infections. After incubation of the plates for 5 days at approximately 20°C under a 12:12h fluorescent light regime, colonies are identified on the basis of colony morphology and size and shape of the microconidia and their disposition on the conidiophores (see section 'Morphology'). A different technique developed by Anderson (1986) utilizes blotter paper in conjunction with a nutrient medium semiselective for Fusarium. The broth contains 15 g peptone, 5 g MgSO4, 1 g KH2PO4, 0.75 g PCNB, 1 g streptomycin sulphate and 0.12 g neomycin sulphate in 1 L of distilled water. In this technique, the broth is sprayed onto steel-blue blotter paper until saturated. Twenty-five unsterilized seeds are evenly spaced on the blotter paper in a sterile, transparent, plastic box and crushed with a Plexiglas plate. The boxes are incubated at about 20°C until the colonies are about 2 cm in diameter (about 14 days) at which time the colonies are examined under the microscope. For seed lots judged to be pathogen-free by either of the above methods, confirmation should be obtained by conducting a seedling grow-out test. In this way, dormant seed infections not detected by culturing seed might be revealed.

Although the amber-coloured, resin-soaked appearance of tissue beneath the bark is a distinctive characteristic of pitch canker, isolation of the pathogen is strongly recommended to confirm a diagnosis. To make an isolation, pieces of wood are soaked in 70% ethanol for 30 sec and then in 1% sodium hypochlorite for 1 min. The pieces are blotted dry and placed on a Fusarium-selective (FS) medium (Correll et al., 1991) and incubated at room temperature. The composition of FS medium can be modified from the published recipe by eliminating the chlorneb, triadimefon, and rifampicin, and by reducing the pentachloronitrobenzene concentration from 750 ppm down to 200 ppm, without any apparent loss of selectivity. For species identification, candidate Fusarium colonies are transferred from FS medium to carnation leaf agar amended with 6.0 g/L of KCl (Fisher et al., 1983). In some areas, the occurrence of morphologically similar species can make definitive identification of the pathogen challenging (refer to the sections on 'Morphology' and 'Similarities to Other Species').

For the utmost confidence in a diagnosis, the isolate in question should be tested for pathogenicity to pine by mechanical inoculation (Gordon et al., 1998b). Additionally, differences in the sequence of the histone H3 gene can separate G. circinata from morphologically similar fungi (Steenkamp et al., 1999).

The detection and identification, via morphological and molecular methods, of the pathogen are described in OEPP/EPPO (2009).

On living plants, pitch canker can be recognized as described in the Symptoms section. On raw logs, resinous cankers may be visible. Removal of the bark should reveal resin-soaked and discoloured wood. The pathogen can survive in chipped wood and would probably be difficult to detect from a visual inspection. The pathogen can also be transported as infested seed and in soil, and its presence in these materials would require laboratory tests to detect (see Diagnostic Methods section). Infected seedlings can be symptomless.

Pre- and post-emergence damping-off caused by G. circinata is not readily distinguishable from death due to other seedling pathogens such as Pythium. Death of older seedlings (1-3 years of age), caused by G. circinata could be mistaken for Phytophthora root rot. Branch tip dieback caused by pitch canker is somewhat distinctive in the relatively rapid abscission of needles and the accumulation of resin at the junction of living and dead tissue (the infection site). The resulting naked tips, however, could be confused with symptoms caused by numerous other branch-infecting pathogens, such as Sphaeropsis sapinea and Peridermium harknessii [Endocronartium harknessii].

In the laboratory, it could be difficult to distinguish G. circinata from any of several species of F. subglutinans sensu lato; this includes F. guttiforme, F. pseudocircinatum, F. sacchari, F. subglutinans sensu stricto, and as yet undescribed species of Fusarium associated with mango and maize. All these taxa are similar in bearing microconidia in false heads but differ in a number of subtler characteristics that can be used to differentiate them from F. circinatum in most cases: whether condiophores originate directly from the substrate or from hyphae growing above the surface of the substrate; the number of conidiogenous openings per phialide; and the number of septa in the macroconidia.

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.

Phytosanitary Measures

Although the chemical seed treatments described in the section on 'Seedborne Aspects' may be effective in eliminating internal infections, such measures should not, by themselves, be considered sufficient to prevent transport of the pathogen. A more prudent policy would be to avoid movement of any pine seed from an infested region to areas where the disease does not occur. Likewise, movement of other pine material (logs, pine litter, wood chips, etc.) into uninfested areas should be avoided. These restrictions, if enforced, would significantly limit opportunities for introduction of the pathogen. For areas in the southern hemisphere where pines are not native, restrictions on the import of pine material would also aid in the exclusion of pine-associated insects which may not yet be present in an area. A host-free buffer zone around points of entry might be a useful measure, particularly in island nations such as New Zealand. A certification programme would be appropriate for seed orchards and pine nurseries. Such a programme might include visual inspection for symptoms and isolation from random samples. More importantly, nursery managers should be enlisted in a programme of continuous monitoring of seedling mortality, with representative samples sent to an appropriate diagnostic laboratory for testing.

Cultural Control and Sanitary Methods

Pruning to remove infected tips will usually not eliminate the disease, as pre-symptomatic infections will remain and new infections will continue to occur. However, if a lightly infected tree is relatively isolated from other diseased trees, removal of infected tips may slow the development of a new disease centre. Also, if elimination of infected branches can restore the aesthetic value of a tree and thereby allow it to be retained in the landscape, the cost of pruning may be repaid by a delay in removal and replacement of the diseased tree. Sterilization of pruning tools with Lysol or household bleach should be performed before and after pruning operations. Infected or uninfected cut branches and infected trees may contain or become infested with insects that carry the pathogen. Chipping this material will significantly reduce insect populations (McNee et al., 2002). If the chips are to be moved to an uninfested area, they should be further treated with moist heat (for example through composting or solarization) to eliminate the pathogen. It is not recommended that logs and firewood cut in infested areas be moved from the region of origin. If such logs must be moved, debarking is desirable because it will eliminate most of the habitat occupied by insects that can carry the pathogen and transmit the disease to healthy trees.

For Pinus radiata in California, USA, it is recommended that trees generally should not be removed solely due to pitch canker infection. Some trees, despite numerous infections, will remain relatively healthy due to genetic resistance. Others will become severely affected, but may later go into remission, a phenomenon which has been documented to occur at numerous locations (Gordon et al., 2001). A more aggressive approach to tree removal might be justified where an infected tree occurs in an area that is otherwise free of the disease.

In southeastern USA seed orchards and plantations, recommendations for cultural control consist of careful selection of a geographic location and planting site that are suitable for a particular species. When possible, it is suggested to use local seed sources which may be better adapted (Dwinell et al., 1985). In seed orchards, wounding incurred during harvest should be minimized. Over-fertilization should be avoided, as nitrogen fertilization in seed orchards may aggravate pitch canker problems (Fraedrich and Witcher, 1982). Maintaining clean seed orchards and seed production areas will reduce the potential for infected or contaminated seed.

In nurseries and Christmas tree farms, the use of clean seed is of paramount importance. When diseased seedlings or trees are found, they should be uprooted and either burned or placed in a sealed plastic bag for disposal. As much of the root system as possible should be removed. Because the fungus can be associated with soil, care should be taken not to distribute soil from the removal site to other locations on the farm. One should avoid the use of equipment that has recently been moved from an infested site. Because the pathogen may be present in areas where it has not yet been identified, using a high-pressure wash to remove soil before allowing any equipment on-site is a good precaution.

Host-Plant Resistance

In a large-scale inoculation study of Central American and Mexican pine species and Pinus radiata, 23 species, varieties, and geographic races were screened for resistance in a greenhouse (Hodge and Dvorak, 2000). In this study, P. radiata and its close relatives (Section Serotinae, sub-section Patula) were very susceptible (less than 10% surviving), while 4 out of 5 taxa in sub-section Oocarpa were extremely resistant. These resistant closed-cone species might be useful as alternate or secondary plantation species or as part of a hybrid breeding programme to improve resistance of P. radiata (Hodge and Dvorak, 2000).

Within P. radiata, variation in susceptibility has been observed in California populations of both planted and naturally regenerated trees (Storer et al., 1999; Storer et al., 2002). In native stands, management of pitch canker can best be achieved through practices that promote natural regeneration of the forest. Fire results in plentiful regeneration, and would also have the benefit of eliminating inoculum associated with the litter layer and the soil surface. The ability of P. radiata to colonize openings in the forest canopy will ensure regeneration in areas where gaps are created by any of various means, including pitch canker-induced mortality. Under these circumstances, selection in the presence of pitch canker should ultimately increase the frequency of resistant trees in the population. In managed stands, replanting with resistant seed or seedlings should be done as these materials become available.

Within several species of southern USA pines, there is documented variation in susceptibility. Disease severity can vary with the provenance of the host (P. elliotii; Dwinell and Phelps, 1977), between individual clones (P. taeda and P. virginiana; Kelley and Williams, 1982; Kuhlman et al., 1982; Barrows-Broaddus and Dwinell, 1984), or between full-sib or half-sib families (P. virginiana; Barrows-Broaddus and Dwinell, 1984). Among the recommendations to reduce incidence of pitch canker are the use of a local seed source, use of seed from resistant clones in existing orchards and continued selection for resistant material where feasible (Dwinell et al., 1985; Rockwood et al., 1988).

In landscape situations, non-pines or less susceptible pine species should be selected for planting in affected areas. For example, in California, several exotic pine species that are suitable for a Mediterranean climate are less susceptible than the native species (Gordon et al., 1998a).

Biological Control

No practical biological control programme exists for pitch canker. Although strains of a bacterium (Arthrobacter sp.) have been identified which are antagonistic to G. circinata in vitro, they were not found to control pitch canker in the field (Barrows-Broaddus et al., 1983; Barrows-Broaddus et al., 1985). Fusarium moniliforme [Gibberella fujikuroi] was found to be a competitive colonizer of wounds, making it a good candidate to protect wounds from infection. However, it is also a weak pathogen of seedlings (Dwinell et al., 1985).

Chemical Control

As is generally the case with diseases of trees, there are no realistic therapeutic options for dealing with pitch canker. Fungicides with activity against the pathogen are available, so, in principle, trees could be protected from infection. However, maintaining a sufficiently high concentration of the active ingredient on all susceptible surfaces would be problematic, even if cost were not a consideration. Therefore, in forest, landscape, and plantation situations, chemical control of pitch canker is not practised.

Chemical control might be feasible in more intensively managed systems such as nurseries and Christmas tree farms. Under nursery conditions, fungicides might be exploited to prevent infection of seedlings. For example, pre-plant treatment of Pinus palustris seeds with thiabendazole-dimethyl sulfoxide has been demonstrated to increase germination and seedling survival (Runion and Bruck, 1988). In a field trial in North Carolina, USA, treatment of 1-year-old P. taeda seedlings with thiabendazole reduced terminal shoot infections (Runion et al., 1993). Various biocidal treatments can be applied to the soil to eliminate the pathogen. On Christmas tree farms, the sites of diseased, removed trees should be treated to eliminate the pathogen from the soil. Broad-spectrum biocides such as metham sodium [metam] have been used for this purpose. When the treated site is eventually replanted, trees should be closely monitored for the appearance of pitch canker symptoms. If the disease reappears, the same procedure should be repeated.

The use of insecticides such as chlorpyrifos to control insect pests may indirectly reduce pitch canker infections by reducing the number of wounding agents and vectors (Dwinell et al., 1985; Runion et al., 1993). In general, however, chemical control of vectors would be economically unfeasible and not very effective. Furthermore, in some areas insect vectors are native pine associates that contribute to the process of decomposition.