Armillaria mellea (armillaria root rot)

Symptoms on FoliageArmillaria species cause root and collar rot of trees. Infection of a root system does not immediately result in the appearance of symptoms on the aerial part. These only begin to show when the collar is attacked or when several large roots are destroyed. Depending on the age and susceptibility of the host, Armillaria species and isolate, and the environmental conditions, the rate of development of the disease may be progressive (decline) or the tree may die suddenly (apoplexy) (Guillaumin, 1977; Guillaumin et al., 1982; Morrison et al., 1991).In the case of slow decline, the main symptoms are a reduction of shoot growth, changes in foliage characteristics (foliage becomes stunted, chlorotic and sparse). The leaves can wilt (on fruit trees), fall prematurely or show abnormal colorations (especially on grapevines) in autumn. Then all foliage can turn yellow or sometimes brown (in conifers), or droop. In eucalypts attacked by A. luteobubalina, disease development results in a dead top of mature trees (Pearce et al., 1986). On fruit trees and grapevines 'en gobelet', asymmetric infection of the root system frequently results in death of only one main branch.Disease development can be more rapid (apoplexy): the trees or shrubs can wilt suddenly, sometimes without having shown any previous symptoms. This death often occurs in a period of water stress, or at the first onset of fruiting. The trees often respond to infection by an abnormally heavy blooming or fruit production (Rhoads, 1956).In most cases, the disease extends in patches, the dead or dying plants being grouped in foci, surrounded by declining trees.Symptoms on the Basal StemIn the final stages of fungal infection, the mycelial fans of the fungus colonizing the roots reach the level of the collar and can grow up in the trunk for some decimetres or more. Sometimes spectacular, these fans are easily detected by stripping the bark of the base of the tree. In some cases, the fungus can destroy the bark and the mycelial fans are visible outside.Trees attacked by species of Armillaria frequently exhibit cracks or cankers, or produce exudates at the base of the trunk (Morrison et al., 1991). The longitudinal cracks are particularly frequent on tropical trees (cocoa, coffee, etc.). Armillaria disease of cocoa, described by Dade as early as 1927, was named 'collar crack' by this author. The cracks are probably due to the mechanical pressure exerted on bark by the fungal fans colonizing the cambium; these fans are particularly thick for the African species A. heimii.The presence of basal cankers, which are generally triangular, means that progression of the fungus has been stopped locally: callusing occurs around the margin of the lesion. This symptom has been occasionally reported from hardwood trees (birch, beech, cork oak) infected by A. mellea (Guillaumin, 1986).The production of resin at the collar is a common response of Abietaceae, especially pines, attacked by A. ostoyae or A. heimii (Gibson, 1960; Hintikka, 1974; Rykowski; 1975). Production of gums is sometimes observed at the base of citrus (Rhoads, 1948) and is common on stone-fruits attacked by A. mellea (Guillaumin et al., 1982). Latex exudes from rubber trees when the collar is reached by A. heimii (Petit-Renaud, 1991) and 'kino' from eucalypts attacked by A. luteobubalina (Edgar et al., 1976).Symptoms on RootsThe bark of the roots is brown, softish and often fissured. With A. mellea, reddish tufts of mycelium sometimes appear through the cracks.The main symptom is the presence at the level of the cambium of white, thick, mycelial fans, sometimes constituting a continuous mycelial tube. This muff is somewhat less developed and continuous in the case of A. tabescens (Rhoads, 1945). The fans are frequently perforated in A. luteobubalina (Kile and Old, 1982) and A. tabescens (Rhoads, 1945).Depending on the Armillaria species involved, the roots are sometimes surrounded by subterranean rhizomorphs 1-2 mm in diameter and varying in colour from black to mahogany: these external rhizomorphs are very frequent when the species involved belongs to the 'gallica group' (A. gallica, A. sinapina, etc.). However, these species are generally weak pathogens and their pathogenicity is limited. External rhizomorphs are fairly common with A. ostoyae; they are rather rare with A. mellea, A. heimii and A. luteobubalina; they are never observed with A. tabescens (Rhoads, 1945).Armillaria Infection without SymptomsArmillaria can be an agent of heartwood decay (heart rot). Heart rot of trees is often due to weakly aggressive Armillaria species, for instance A. borealis or A. cepistipes on conifers in northern Europe (Roll-Hansen, 1985). However, even the aggressive species can behave as heart-rot agents on tolerant tree species, as is sometimes the case with A. mellea on beech or poplars (Guillaumin, 1986). This localization of the fungus does not provoke symptoms, except an enhanced susceptibility to windthrow.Infection without symptoms can also occur in the case of latent infections on the roots of young, healthy trees. Armillaria infections are often stopped by the host reactions. The fungus remains alive and constitutes a 'latent infection' limited in area and showing no evolution. However, these latent infections (the number of which increases with time) can resume their evolution and colonize the root system if the tree is weakened by age or environment (Delatour and Guillaumin, 1995).Infestation by an unidentified species of Armillaria was reported in Germany on fir logs during long-term storage under water sprinklers (Gross et al., 1996).

Introduction

Control of Armillaria root rot is extremely difficult, because the inoculum is found in the soil, in the form of masses of mycelium enclosed in important volumes of wood and often protected by the 'zone lines' within this wood.

In forestry, the value of individual trees is often too low (except in particular cases, such as seed orchards) to support expensive control methods such as biological or chemical treatments. Therefore, the control aims to avoid and reduce the losses due to Armillaria root disease and is based mainly upon forest management and cultural methods. These methods have been reviewed by Shaw and Roth (1978), Hagle and Shaw (1991) and Lung-Escarmant et al. (1995).

By contrast, the value of the plants in orchards, vineyards, floriculture and urban forestry justifies higher treatment costs, and methods such as chemical control (mostly by soil fumigation), biological methods, or the use of tolerant rootstocks may be considered. At the moment the last method seems to be the most reliable in fruit arboriculture, at least for stone fruits.

Choice of the Site for Planting

Sites can be hazardous either because they can predispose the host in some way, or because the inoculum potential of pathogenic Armillaria species is likely to be important. The sites of recent deforestation are particularly risky, depending also on the composition of the natural vegetation (see Biology and Ecology). In southern France, it has long been known that sites with Quercus species (especially Q. pubescens and Q. ilex) are particularly unfavourable for planting vineyards.

Forest Management

Armillaria is a normal component of natural forest ecosystems, which in many situations may be present without causing major damage (this assertion is not true for orchards, where the fungus generally behaves as a primary pathogen). Therefore, the mere presence of the fungus in a forest is not sufficient cause for treatment; significant damage is observed only if the stands are weakened by diverse causes and/or if inoculum potential (i.e. the volume of dead wood in the soil) is increased beyond a certain threshold. Correct forest management will try to avoid these two possibilities (Hagle and Shaw, 1991; Lung-Escarmant et al., 1995): it is possible to manage the length of rotations (stands are cut before the age at which they are expected to become highly susceptible to the fungus), the diversity of the tree species (where A. ostoyae is concerned, it is often desirable to maintain a percentage of hardwoods in a conifer stand) and the density of the stocks. All the events which greatly increase the volume of dead wood should be avoided in risky sites: for instance, partial commercial harvest and undergrowth clearance with herbicides.

The characteristics of thinning (intensity, date and rhythm) play an important role. A major aim is to avoid thinning during periods of stress (drought, defoliation by insects, etc.) (Hagle and Shaw, 1991; Lung-Escarmant et al., 1995). The regeneration mode is also important, natural regeneration often leading to less damage by Armillaria than plantation (Onsando et al., 1997). The mode of plantation (angle notch planting versus pit planting) and the type of plant (bare roots versus plants in paper pots) also affects the rate of killing by the fungus (Tomiczek, 1997; Wiensczyk et al., 1997).

In the western USA (Rocky Mountains), a model was designed to predict the spread and impact of the main root rots of conifers (A. ostoyae and Phellinus weirii) (Shaw et al., 1985, 1991; Stage et al., 1990). The model operates in conjunction with a model for stand development. It requires evaluation of the initial inoculum potential on the stand and can simulate the results of different sylvicultural strategies, for instance concerning thinning and harvesting.

Direct Reduction of Inoculum

The most drastic method of reducing inoculum potential consists of the total removal of the stumps. This method was used on a large scale in New Zealand: according to Van der Pass (1981), and Van der Pass and Hood (1984), the mortality rate of planted pines after 4 years was 2% on the stands where the stumps had been removed and 23% on the controls. Similar results were obtained in the USA (Thies and Russell, 1984) and Canada (Morrison et al., 1988). However, if the beneficial effect of the treatment in the long term is not considered, stump removal can temporarily increase the damage by increasing the quantity of small roots in soil. Moreover, the economic balance of such a heavy operation is difficult to establish; it depends on the expected losses in the absence of treatment and also the possibility of exploiting the uprooted stumps.

Stump and root removal is commonly practised in preparing sites for plantation of fruit orchards and vineyards. Several rippings at different depths (possibly including subsoiling) are followed by hand removal of the remaining roots.

These methods can be combined with a few years of fallow before plantation. The efficacy of fallowing depends on the size of the colonized roots which remain in the soil.

Other methods have also been advocated for reduction of inoculum: artificial depletion of food bases was found to be particularly satisfactory in Africa for plantation of industrial crops after clearing the tropical forest (Leach, 1937; Dadant, 1963). Two systems have been used: (i) ring incisions of the trunk 6-12 months before felling, which deplete the roots of their reserve carbohydrates, and (ii) poisoning of the trees with herbicides a few months before felling. These methods were also tried under temperate climates, but with less success (Redfern, 1968; Lanier, 1971).

Prescribed burning of vegetation has also been attempted (Hood and Sandberg 1989; Filip and Yang-Erve, 1997). The direct effect of destroying the inoculum by heat is limited to a few centimetres, however, heating also has indirect effects in altering the microbiological balance in the soil (Filip and Yang-Erve, 1997).

Direct killing of the fungus in stumps and dead trunks was also achieved by injection of fumigants into the stumps (Filip and Roth, 1977). The fumigants were the same as those which are used for soil fumigation. The method could be interesting in situations where stump removal is not possible.

A. mellea is distributed in western and southern Europe, the southern USA, southern Japan, probably Maghreb, Caucasus and the near Orient, and inAfrica south of the Sahara, as various subspecies.The host range of the species is larger than that of A. ostoyae. It includes most woody Angiosperms and also Gymnosperms of the family Cupressaceae (for example, Cryptomeria japonica, a species heavily attacked on the Azores Islands (Santos de Azevedo, 1976). Incidentally, it also attacks very young Abietaceae. In some countries with a Mediterranean climate, such as Greece (Tsopelas, 1994) and in California, USA (Jacobs et al., 1994), A. ostoyae is replaced even on adult Abietaceae by the more thermophilic A. mellea as the main agent of conifer root rot.A. mellea has been reported on hardwood forest trees, amenity trees, orchard trees and grapevines. On hardwood forest trees, its impact is usually limited; the fungus often behaves as a weak parasite of Quercus, Fraxinus, Betula, etc. and an agent of heart rot of Fagus and Populus (Guillaumin, 1986). In Italy, A.mellea is a weak parasite of several Mediterranean species of Quercus, its impact is increased by drought (Luisi et al., 1996). The fungus is also generally considered as the main causal agent of 'yellow stain' of cork oak (Quercus suber), a discoloration of the cork plates responsible for 'cork-taint' of wines (Moio et al., 1998). However, recent observations in Portugal have questioned the role of Armillaria in the aetiology of yellow stain (Sousa Santos and Braganþa, INIA, Estaþao Florestal Nacional, Oeiras, Portugal, personal communication).Conversely, the impact of the parasite can be very important in orchards and vineyards, especially in France, Italy and California. In France, it is a major disease of grapevines, especially in the Bordeaux region (Saint Emilion) and in the 'Côtes du Rhône' and 'Costières du Gard'. In southern France and California the damage on stone fruits (peaches, almonds, apricots, cherries) and walnuts can be severe. Unfortunately, few quantitative data are available concerning the overall mortality rates in orchards and vineyards. Guillaumin et al. (1982) reported some extreme examples where the mortality rates exceeded 50% in vineyards, 65% in a peach orchard and 85% in an apricot orchard. In the vineyards of the 'Côtes du Rhône' (south-eastern France), the overall number of plants killed each year is evaluated in the order of one per thousand.On 2-4-year-old seedlings of Picea abies, P. mariana, P. sitchensis and Pinus sylvestris, inoculated with A. mellea and studied for 4 years, disease rating was highest in P. sitchensis with 49.3% infection and 45.3% seedling mortality. P. sitchensis also developed symptoms first (after 7 months). A. mellea entered through the root collar or through roots with a diameter >2 mm. Annual height growth was markedly reduced in infected seedlings (Singh, 1980).In Wisconsin, USA, damage to stands dominated by Populus tremuloides was assessed. Infection by A. mellea occurred by rhizomorph penetration, mycelial growth through roots from parent stumps and by contact with colonized roots. Obvious injuries were associated with ca 10% of infections. The incidence of root rot increased with stand age, with >70% of sampled trees infected in the 15-year-old stands. In these stands, colonization extended to stem bases in >25% of infected root systems and to within 20 cm of the stem base in a further 50%. The results indicated the potential losses that A. mellea may cause as the stands mature (Stanosz and Patton, 1987). Outbreaks of A. mellea infection caused Pinus resinosa losses of 12, 18 and 37% in three widely separated Wisconsin mixed-oak plantations. Trees died within 10 years of planting. The disease was most common where P. resinosa was established on oak sites and where the oak was eliminated by chemical sprays. Pine mortality was positively correlated with the total number of dead oak stems/ha but not with pine height growth (Pronos and Patton, 1977). In Idaho and Montana, root disease losses were estimated on >3 million hectares of commercial forest; A. mellea was one of the two major root pathogens found (James et al., 1984). Annual losses in two Idaho forests due to root diseases were ca 2.2 and 0.4 trees/ha, respectively. A. mellea was one of the most frequently found pathogens (Stewart et al., 1982). Pinus ponderosa forests in Washington were assessed for loss of wood volume due to A. mellea. Loss of wood volume increased from 9 m³/ha in 1957 to 24 m³/ha in 1971. There was little change in the proportion of infected plots over the 14 years, the increased loss being caused by the death of fewer but larger trees (Shaw et al., 1976). In Hawaii, A. mellea was responsible for serious losses in thousands of acres of Metrosideros collina forests (Burgan and Nelson, 1972). In California, damage mainly concerns the stone fruits and walnuts (Thomas et al., 1948).In Newfoundland, Canada, A. mellea is reported as the most important disease of softwood plantations (Singh, 1975). Sample plots in three plantations of Pseudotsuga menziesii on Vancouver Island were examined for damage at 15-17 years and again 3, 6 and 11 years later. The incidence of root rot increased from 1-17% to 2-23% during the study, A. mellea causing most of the rot. However, of the trees infected with A. mellea at the beginning of the study, 25% recovered by the end of the study and 60% showed signs of recovery (Johnson et al., 1972). In Ontario, A high incidence of A. mellea was said to contribute to the reduced numbers and size of suckers in aspen (Populus tremuloides and P. grandidentata) (Stiell and Berry, 1986).In Greece, A. mellea was present in coniferous and broad-leaved forests in most of the areas examined, except the high altitudes (above 1000 m) of the mountains of northern Greece. It caused significant damage in Abies forests as well as in fruit orchards and vineyards (Tsopelas, 1999).In southern Italy, A. mellea attacks mainly citrus (Salerno and Cutuli 1985; Ippolito et al., 1989) and prickly pears (Magnano di San Lio and Tirro, 1983). In the Mediterranean basin, it is found sporadically on olive trees (Sanchez-Hernandez et al., 1996).In California, damage traditionally concerns stone fruits and walnuts (Thomas et al., 1948); recently, the incidence of Armillaria root rot has significantly increased on pears (Elkins et al., 1998).On amenity trees, the species is often important in parks and arboretums, especially when they are ageing, as well as in private gardens and on urban trees. This aspect is particularly important in the UK (Rishbeth, 1983).A. mellea is probably the agent of the decline of Chamaecyparis obtusa (Cupressaceae) in southern Japan.