Gremmeniella abietina
(Brunchorstia disease)

A distribution map has been published by CMI (1989, No. 423).

The monitoring of 110 plantations of P. contorta in northern Sweden during 1987-1991, shows that this introduction was not problem-free (Karlman et al., 1994). In harsh areas (low temperature sum), an extensive epidemic of G. abietina caused severe damage and mortality in young plantations of P. contorta during the late 1980s. The damage was worst in topographic depressions within the regeneration areas and on sites where Picea abies was estimated to have a higher wood yield than Pinus sylvestris.

See also CABI/EPPO (1998, No. 203).

G. abietina has not been classified as a quarantine pest by EPPO, but is of quarantine significance for NAPPO, and potentially in other regions. In Europe, it has generally been regarded as widespread and to have reached the limits of its natural distribution. Its absence from certain areas has been attributed to the fact that they lie outside the natural range of the fungus. There is certainly no strong suggestion that G. abietina has the potential to cause direct damage in such areas. However, its presence, even at relatively insignificant levels, could have indirect consequences for the export trade.

Phytosanitary Measures

Planting material of tree species included in the host range of G. abietina should be chemically treated with the fungicide chlorothalonil prior to movement. Before export to countries free from the disease, Christmas trees should be inspected for canker and for shoot blight symptoms during the summer before trading. Immersion of diseased seedlings in warm water (55°C) and immersion or spraying with dilute sodium hypochlorite eradicated the pathogen with no apparent loss in needle colour or retention (Hudler and Neal, 1990). Regulatory action by the USA and Canada now prohibits the movement of Christmas trees and nursery stock from areas where the European strain of the pathogen is present.

In affected plantations, the optimum time to carry out sanitation fellings is the first winter after symptoms of the disease have appeared.

In Scandinavia there is a risk of secondary damage by the pine shoot beetle (Tomicus piniperda) which transfers blue stain fungi (Leptographium wingfieldii and Ophiostoma minus [Ceratocystis minor]) to already weakened Pinus sylvestris trees (Solheim et al., 2001). It has recently been shown that Pinus sylvestris defoliated by other insects by up to 90% may still manage to produce enough resin to avoid attack by Tomicus piniperda (Langström et al., 2001). This limit is, however, not applicable when the tree is defoliated by Gremmeniella. After the heavy Gremmeniella outbreak in Sweden, preliminary results indicate that Scots pines with less than 30% living crown in 2001 were dead in 2002 (M Vikholm and J Witzell, Swedish University of Agricultural Sciences, Umea, Sweden, personal communication, 2003).

The five-needled pines seem to be more resistant than the two- and three-needled group (Skilling and O'Brien, 1979). For more information see Phillips and Burdekin (1985).

During the late 1970s and 1980s the North American species Pinus contorta was extensively introduced into northern Sweden, in order to increase forest yield. To date, P. contorta has been planted on more than 550,000 ha in Sweden. This pine species has a westerly distribution in North America, and therefore has not been exposed to G. abietina naturally. In harsh areas (low temperature sum), an extensive epidemic of G. abietina caused severe damage and mortality in young plantations of P. contorta during the late 1980s (Karlman et al., 1994). Populations attacking P. sylvestris and P. contorta in northern Sweden are probably identical genetically, suggesting that the fungus is not host-specific with regard to these two conifers. In view of the fact that the exotic P. contorta was severely infected during the late 1980s, the risk of spread from severely infected P. contorta plantations to adjacent plantations of indigenous P. sylvestris should be considered high (Hansson et al., 1996).

Recently, an even more severe outbreak of G. abietina has occurred in Sweden. The Forestry Board reported approximately 300,000 ha of at least moderately damaged Scots pine forests in 2001. The typical forest was a monoculture on sites formerly supporting Picea abies and the age was ca 50 years. The most effective sanitation action has been clear-cutting; sanitation thinning did not usually control the disease. About a third of the diseased forest area has been clear-cut.

Life Cycle

The fungus enters the apical buds and developing shoots by germinating conidia or ascospores, especially during cool and wet conditions (see section on Symptoms). The presence of free water has been found to be necessary to induce the discharge of both conidia and ascospores (Skilling, 1969). In addition, the ambient temperature at this time influences both the number of ascospores that are discharged per apothecium and how soon dispersal commences. Maximum spore discharge takes place at about 17°C. If free water is available in the form of rain for 4-8 h at about 17°C, major spore release will take place (Skilling, 1972). Experiments in Finland show that relative humidity is more important for conidial dispersal earlier in the season, and rainfall later in the season (Petäistö et al., 2000).

G. abietina infects through stomata on bracts subtending the short shoots. Germ tubes penetrate between the guard cells and the bract tissue is sparsely colonized by late summer or autumn. Only after mid January-early February of the following year does the fungus extend from the bract and begin to colonize the short shoot and surrounding cortical tissue, producing a resinous, brown, necrotic area of cortical parenchyma and phloem beneath the bract as the first visible symptom of infection (Skilling, 1972; Patton et al., 1990). The death of vascular tissue inside the shoots occurs during winter and when the temperature is between +5 and -6°C (Marosy et al., 1989; Petäistö, 1993). After entry, the fungus kills the bud and proceeds downwards into the stem and needle fascicles. Shoots start dying in the following spring from the tips. Needle bases turn orange to brown while the tip may still be green, and finally fall off. Small, black pycnidia (vegetative fruiting bodies) appear at the base of dead needles or on dead shoot tips throughout the year but more commonly in spring and early autumn. The sexual fruiting bodies, apothecia, occur in the same place as pycnidia but 1 year after the shoots die (and 2 years after initial infection). The entire crown may be infected, which causes significant loss of foliage, further weakening of the trees due to secondary attack by other fungi and insects, and finally death. In Sweden, during the heavy epidemics of 2001, tens of thousands of hectares of middle-aged Scots pine stands were rapidly killed within some mild winter months and without having any chance to produce adventitious shoots.

The fungus overwinters as mycelium in the conifer host or as immature fruiting bodies. It is capable of infecting the host while it is actively growing, but rapid development of disease symptoms can take place while the host plant is dormant. Mortality incurred during the development of an epidemic depends on the size of the host plant at the time of infection. Very small trees, such as nursery seedlings, are susceptible and die soon after infection, usually in the first year. Most larger trees take several years to succumb, usually dying one branch at a time.

Experiments indicate that Gremmeniella abietina has the ability to degrade celloluse and pectin within cell walls (Ylimartimo et al., 1997).

Causes of Epidemics

Climatic conditions such as wet spring and cool summer months, high precipitation, high humidity and fog are reported to favour serious outbreaks of the disease (Butin and Hackelberg, 1978; Karlman, 1986; Uotila, 1988; Karlman et al., 1994). In Japan, the epidemic of 1970 is thought to have been favoured by unusually low (freezing) air temperatures from late September to early October 1969 and a subsequent long period of deep snow (Yokota, 1975). In Sweden the most severe epidemic ever (300,000 ha of Scots pine) was presumably predisposed by the very wet summer and autumn of 2000 and the following very mild winter.

Plantations in topographic depressions, on north-facing slopes and fertile, moist sites (in Scandinavia known as 'spruce sites') often suffer from an increased risk of disease (Dorworth, 1973; Uotila, 1988; Witzell and Karlman, 2000). Heavy snow loads, especially if combined with bad root development (instability), are extremely dangerous since the pathogen has perfect conditions under the snow (Karlman et al., 1994; Hansson and Karlman, 1997).

At stand level, dense stands seem to be more affected (Read, 1967; Nevalainen, 1999). The origin of plant material is also important; there is less infection on northerly provenances (Karlman, 1986; Dietrichsson and Solheim, 1987; Hansson, 1998). In Sweden, during the epidemics of 2001, provenances of Pinus sylvestris transferred two degrees or more to the north were significantly more affected than local or more northern provenances (M Wikström and P Hansson, Swedish University of Agricultural Sciences, Umea, Sweden, personal communication, 2003).

Under field conditions G. abietina is easiest to detect when the shoot blight symptom is fresh, during the first summer after initial infection. At this stage the diseased stands are bright reddish-brown. Affected stands might be recorded from aerial inspection (helicopter or small aircraft), and also from satellites (Olsson, 1990). This inspection is harder to perform if the disease is concentrated in the lower part of the crown. With satellite remote sensing there is a risk of confusion with the colour patterns of recently thinned stands which have wilting logging slash on the ground.

Using PCR techniques it is possible to detect latent infection and differentiate the North American and European races (Hamelin et al., 2000; Zeng et al., 2005). This could be useful in nurseries.

Detection based on symptoms on host plants and identification based on the morphology of the isolate are detailed in OEPP/EPPO (2009).

The ascoma of G. abietina are similar to those of Cenangium ferruginosum, which, at least in Scandinavia, is saprobic. On recently killed plant material there is usually no difficulty in identifying G. abietina, since no saprobic fungi have yet invaded. The ascoma of G. abietina are somewhat smaller, less aggregated (clustered) and, most important, not so obviously concentrated on the needle-scars on the twigs as those of Cenangium.

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.

The disease may be controlled in the nursery using the fungicide chlorothalonil applied about seven times from May to mid-August (Skilling and Waddell, 1970, 1974). In Swedish nurseries the fungicides propiconazole and azoxystrobin are used. On the forest scale, however, once G. abietina is established in a plantation it is almost impossible to control. The use of chemicals is not practical in plantation crops where careful selection of disease-free planting material, as well as selection of planting sites at some distance from infected plantations, are important considerations.

Systematic pruning of the lower four whorls in diseased red pine (Pinus resinosa) plantations in Quebec, Canada, reduced the incidence rate of the disease from 67% to 22% (Laflamme, 1999). To avoid many successive interventions, pruning the lower half of the crown whorls and even two-thirds, if necessary, is recommended in infected plantations less than 20 years old.