Armillaria luteobubalina (armillaria root rot)
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Hosts/Species Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Plant Trade
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Distribution Maps
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IdentityTop of page
Preferred Scientific Name
- Armillaria luteobubalina Watling & Kile
Preferred Common Name
- armillaria root rot
International Common Names
- English: honey root rot
- Spanish: hongo miel; pudricion blanca de las raices
- French: armillaire; pourridie-agaric
- Russian: opienok oseniy
- Chinese: mi huan jun
Local Common Names
- Denmark: honningsvampe
- Germany: hallimasch; wurzelfäule
- Italy: marciume bianco radicale
- Poland: opienka miodowa
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Fungi
- Phylum: Basidiomycota
- Subphylum: Agaricomycotina
- Class: Agaricomycetes
- Subclass: Agaricomycetidae
- Order: Agaricales
- Family: Marasmiaceae
- Genus: Armillaria
- Species: Armillaria luteobubalina
Notes on Taxonomy and NomenclatureTop of page Comprehensive reviews of the taxonomy and nomenclature of this group of fungi have recently been written by Watling et al. (1982, 1991). These authors, after many others, consider that the correct generic name of the fungus is Armillaria, and the names in Armillariella and Clitocybe should be considered synonyms.
Until the 1980s, the annulate armillarias of the northern temperate hemisphere were considered to belong to a single, polymorphic species, Armillaria mellea (Kummer, 1871; Quélet, 1872) or Armillariella mellea (Karsten, 1881) or Clitocybe mellea (Ricken, 1915). However, Romagnesi (1970, 1973) had, on a morphological basis, proposed dividing the European 'mellea complex' into four different species. After Hintikka (1973) had solved the problem of the sexual pattern of the group, Korhonen (1978) demonstrated that the European 'mellea complex' consists of five intersterile groups (which were first named A, B, C, D and E). Subsequent studies by European mycologists and phytopathologists (for example, Guillaumin and Berthelay, 1981; Rishbeth, 1982; Intini and Gabucci, 1987) showed that these groups differ in their geographical and ecological distribution, pathogenicity, host range and cultural characteristics, and can be considered as true species. The groups C, D and E were equated to three of the species proposed by Romagnesi (1970, 1973); they were named Armillaria ostoyae, A. mellea (sensu stricto) and A. gallica, respectively. The name A. lutea proposed by Termorshuizen and Arnolds (1987, 1997) instead of A. gallica is rejected by the majority of authors. The groups A and B received new names: Armillaria borealis Marxm. & Korhonen, and A. cepistipes Velen., respectively (Marxmüller, 1982, 1987; Romagnesi and Marxmüller, 1983).
For very many years the two exannulate European species of Armillaria had been regarded as being distinct from the 'mellea group' and were named Agaricus tabescens Scop. and Agaricus ectypa Fries. They are now known as Armillaria tabescens (Scop.) Dennis, P.D. Orton & Hora, and A. ectypa (Fr.) Lamoure, respectively.
In North America, research proceeded according to the same scheme: nine annulate North American Biological Species (NABS) were defined: I, II, III, V, VI, VII, IX, X (Anderson and Ullrich, 1979; Anderson, 1986) and XI (Morrison et al., 1985). Four of these groups (NABS I, VI, VII and XI) were shown to be synonymous (and frequently interfertile) with, respectively, the European species A. ostoyae, A. mellea, A. gallica Marxm. & Romagn. and A.cepistipes Velen. (Anderson et al., 1980; Guillaumin, 1986, Morrison et al., 1985; Banik et al., 1996; Banik and Budsall 1998). Four of these groups (NABS I, VI, VII and XI) were shown to be synonymous (and frequently interfertile) with, respectively, the European species A. ostoyae, A. mellea, A. gallica Marxm. & Romagn. and A. cepistipes Velen. (Anderson et al., 1980; Guillaumin, 1986; Morrison et al., 1985; Banik et al., 1996; Banik and Budsall, 1998). NABS II, III, V , IX and X have no European counterparts and the first four received new Latin names: Armillaria gemina Bérubé & Dessur. for group II, A. calvescens Bérubé & Dessur. for group III, A. sinapina Bérubé & Dessur. for group V and A. nabsnona T.J. Volk & Burds. for group IX (Berube and Dessureault, 1988, 1989; Volk et al., 1996). At present NABS X remains without a Latin name. However, a low rate of interfertility also exists between A. cepistipes, A. sinapina and NABS X (Bérubé et al., 1994; Banik and Budsall, 1998).
The exannulate American species had long been been recognized as different from the mellea group and was named Clitocybe monadelpha Morgan (1883). Bresadola (1900) then claimed synonymy of this species with the European A. tabescens. However, the North American exannulate Armillaria has only low rates of sexual compatibility with A. tabescens (JJ Guillaumin, INRA, Clermont-Ferrand, France, and C Mohammed, University of Tasmania, Hobart, Tasmania, Australia, unpublished results), which could justify a name in Armillaria (Kile et al., 1993).
Ten biological species of Armillaria were shown to exist in Japan (Nagasawa, 1991; Cha et al., 1992; Mohammed et al., 1994a; Ota et al., 1998a). Four of these species are the same as the holarctic species A. ostoyae, A. gallica, A. cepistipes and A. mellea (Cha et al., 1992; Mohammed et al., 1994a; Ota et al., 1998a). However, the Japanese populations of A. mellea are homothallic (Cha and Igarashi, 1995a; Ota et al., 1998b) and the molecular studies showed that they are fairly different from the heterothallic European and American populations of the same species (Ota et al., 2000). These Japanese forms of A. mellea are regrouped in the subspecies Armillaria mellea (Vahl: Fr.) Kummer subsp. nipponica J.Y. Cha & Igarashi 1995. Two other Japanese groups correspond to the American species A. sinapina (Cha et al., 1994) and A. nabsnona (Ota et al., 1998a). Three species are intersterile with European, American and Australasian testers and thus belong to new species, specific to the Far East. Two of these species were described by Cha et al. (1994), who named them Armillaria jezoensis J.Y. Cha & Igarashi and A. singula J.Y. Cha & Igarashi. The third specific species (Nagasawa's group E) remains without a Latine name. The exannulate Armillaria which is also frequent in Japan (Terashita and Chuman, 1987), is completely interfertile with the European isolates of A. tabescens and certainly belongs to this species (JJ Guillaumin, INRA, Clermont-Ferrand, France, and C Mohammed, University of Tasmania, Hobart, Tasmania, Australia, unpublished results).
The studies are less advanced in China and presently restricted to the North of the country. Five biological species CBS A, B, C, D and E were distinguished by He et al. (1996) and four biological species ChBS I, II, III and IV by Li et al. (1998). CBS B and ChBS IV were identified as A. gallica, CBS E as A. ostoyae and CBS A as A. sinapina (Mohammed et al., 1994a; He et al., 1996; Qin et al., 1996, 1999; Li et al., 1998; Dai et al., 2000).
The far-eastern wild, achlorophyllous orchids Gastrodia elata and Galeola septentrionalis show mycotrophic associations with species of Armillaria. Several different species (A. mellea subsp. nipponica, A. tabescens, A. gallica, A. sinapina, A. jezoenis and A. singula) can be involved in this symbiosis (Terashita and Chuman, 1987; Mohammed et al., 1994a, Cha and Igarashi, 1995b, Ota et al., 1998a).
Six species of Armillaria have been described from Australasia (Australia, New Zealand, New Guinea, Fiji Islands): A. novae-zelandiae (G. Stev.) Herink, A. hinnulea Kile & Watling, A. limonea (G. Stev.) Boesew., A. luteobubalina Watling & Kile, A. fumosa Kile & Watling and A. pallidula Kile & Watling (Stevenson, 1964; Podger et al., 1978; Kile and Watling, 1983, 1988). A seventh species from New Guinea, A. fellea (Hongo) Kile & Watling, is less certain (Hongo, 1976). A. novae-zelandiae and A. limonea had been described in New Zealand by Stevenson as early as 1964 and thus before the clarification of the 'mellea complex' in Europe and North America. However, all six species appear as biological species with a tetrapolar pattern of sexuality (Kile and Watling, 1988; Guillaumin, 1986). The six species are completely intersterile with the Armillaria species of the northern hemisphere (Guillaumin, 1986). The presence of A. limonea and A. novae-zelandiae in South America is controversial (Kile et al., 1994).
In tropical Africa, Pegler (1977) has distinguished two species, named Armillaria mellea and A. heimii Pegler (syn.: Clitocybe elegans Heim). A. heimii was shown to be by far the most common African species (Mohammed and Guillaumin, 1993; Intini, 1996; Abomo-Ndongo and Guillaumin, 1997; Abomo-Ndongo et al., 1997). A. mellea was found only in plantations in Kenya, Uganda and Sao-Tome (Pegler 1977; Mohammed and Guillaumin, 1993). It appears morphologically similar to the European species A. mellea sensu stricto, but it is homothallic. Ota et al. (2000) showed that this taxon, named A. mellea subsp. africana by Kile et al. (1994), is just a genet of A. mellea subsp. nipponica Cha & Igarashi, possibly transported from Asia to Africa in the historical times. In addition to A. heimii and A. mellea, other species probably exist, especially in the highlands of East and South Africa: a SIG Group III was reported from the plateaux of Kenya (Mohammed and Guillaumin, 1993; Abomo-Ndongo and Guillaumin, 1997) two species were described in Zimbabwe in addition to A. heimii (Mwenje and Ride, 1996, 1997, 1998) a taxon in Transvaal seemed also different from A. heimii (Coetzee et al., 1998). The relationships between these four taxa have not yet been studied.
In India (Chandra and Watling, 1982) and in South America (Singer, 1956) several Armillaria species have been described on the sole basis of the morphology of the basidiomes and need to be confirmed by mating tests. Some authors (Pegler, 1986) consider that A. fuscipes Petch described by Petch in Sri Lanka (1909) could be the same species as the African A. heimii.
It is not possible here to deal comprehensively with all the Armillaria species known to be pathogenic. Full descriptions are available for the five species which more often behave as primary pathogens: Armillaria mellea, A. ostoyae and A. tabescens in the northern temperate hemisphere, A. luteobubalina in Australia and A. heimii in tropical Africa.
Other Accepted Armillaria Species
In the northern hemisphere
Armillaria gallica Marxm. & Romagn. (syn.: A. bulbosa (Barla) Kile & Watling, A. lutea Gillet [sic] (Korhonen's group E, NABS VII)
Armillaria cepistipes Velenovsky (A. cepaestipes Velenovsky) (Korhonen's group B, NABS XI)
Armillaria borealis Marxm. & Korhonen (Korhonen's group A)
Armillaria ectypa (Fr.) Lamoure
In North America and East Asia
Armillaria sinapina Bérubé & Dessur. (NABS V)
Armillaria nabsnona Volk & Burds. (NABS IX)
In North America
Armillaria gemina Bérubé & Dessur. (NABS II)
Armillaria calvescens Bérubé & Dessur. (NABS III)
Armillaria jezoensis J.Y. Cha & Igarashi
Armillaria singula J.Y. Cha & Igarashi
In Australia and New Zealand
Armillaria novae-zelandiae (G. Stev.) Herink
Armillaria limonea (G. Stev.) Boesew.
Armillaria hinnulea Kile & Watling
Armillaria fumosa Kile & Watling
Armillaria pallidula Kile & Watling
In Japan and tropical Africa
Armillaria mellea (Vahl: Fr.) subsp. nipponica Cha & Igarashi
In the West Indies
Armillaria puiggarii Speg. (syn.: A. melleorubens (Berk. & M.A. Curtis) Sacc.)
Taxa Needing Confirmation
Biological species without Latin names
NABS Group X (Anderson and Ullrich, 1979)
Japanese Group E (Nagasawa, 1991)
Zimbabwean Group II (Mwenje and Ride, 1996)
Zimbabwean Group III (Mwenje and Ride, 1996)
Species defined on morphological basis, needing to be studied as biological species
In Central America
Armillariella affinis Singer
In South America
Armillaria procera Speg.
Armillaria sparrei (Singer) Herink
Armillariella griseomellea Singer
Armillariella tigrensis (Singer) Raithelh.
Armillaria montagnei (Singer) Herink
Armillaria olivacea Herink [an invalid name]
In Sri Lanka
Armillaria fuscipes Petch
Eight species described by Berkeley 1850 under the genus name Agaricus: A. adelpha, A. apalosclerus (=Armillaria apalosclera (Berk.) A. Chandra & Watling), A. dichupella Berk., A. duplicata Berk., A. horrens Berk., A. multicolor Berk., A. omnituens Berk., Armillaria vara (Berk.) Sacc.
In New Guinea
Armillaria fellea (Hongo) Kile & Watling
DescriptionTop of page A. luteobubalina resembles A. mellea except for the size of the basidioma (smaller), colour of the pileus (dark brown with yellowish hues becoming lemon-yellow, according to Podger et al., 1978), consistency of the ring (moderately thick, floccose) and dimensions of basidiospores (slightly smaller than in A. mellea). Basidia are without clamp connections. Subcortical fans are often perforated. The morphology of the mycelial mats in culture is very close to that of A. mellea.
Distribution TableTop of page
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.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Australia||Present||Present based on regional distribution.|
|-New South Wales||Widespread||Kile and Watling, 1988|
|-Queensland||Present||Kile and Watling, 1988|
|-South Australia||Present||Kile and Watling, 1988|
|-Tasmania||Widespread||Kile and Watling, 1981|
|-Western Australia||Widespread||Kile et al., 1983|
Risk of IntroductionTop of page The different Armillaria species are not officially quarantine pests. However, because no species presently has a worldwide distribution, it seems advisable to avoid introduction of a particular species into new continents. It is possible, for instance, that A. mellea and A. ostoyae could adapt to the climatic conditions of Australia and New Zealand, and A. luteobubalina could adapt to Mediterranean Europe and the southern USA.
Hosts/Species AffectedTop of page Plant species indicated as primary and secondary host crops in the list of hosts are those of which Armillaria species are major and minor parasites, respectively; the terms primary and secondary do not carry their usual phytopathological meanings here.
A. luteobubalina, an exclusively Australian species, was described by Kile and Watling (1981) after the division of the 'mellea group'. The host list originates from the compilation of papers by Kile (1981), Kile and Watling (1981), Smith and Kile (1981), Kile et al. (1983, 1991), Shearer and Tippett (1988), Falk and Parberry (1995), Shearer et al. (1997, 1998).
Growth StagesTop of page Flowering stage, Fruiting stage, Vegetative growing stage
SymptomsTop of page Symptoms on Foliage
Armillaria 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 Stem
In 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 Roots
The 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 Symptoms
Armillaria 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).
List of Symptoms/SignsTop of page
|Growing point / dead heart|
|Leaves / abnormal colours|
|Leaves / abnormal forms|
|Leaves / abnormal leaf fall|
|Leaves / wilting|
|Roots / fungal growth on surface|
|Roots / rot of wood|
|Roots / soft rot of cortex|
|Stems / canker on woody stem|
|Stems / dead heart|
|Stems / dieback|
|Stems / gummosis or resinosis|
|Stems / internal red necrosis|
|Whole plant / dwarfing|
|Whole plant / plant dead; dieback|
Biology and EcologyTop of page Ontogeny
The different organs initiated by the fungus in nature are described below. Species of Armillaria have no known asexual spores, but are able to differentiate a variety of vegetative structures, both in nature and in vitro.
Like Garrett (1956) many authors distinguish the rhizomorphs from the mycelial cords and reserve the name rhizomorph for highly differentiated organs with apical growth. The subterranean rhizomorphs of many species of Armillaria (the 'rhizomorpha subterranea' of Persoon, 1801) fall into this category. These organs show "the most highly differentiated vegetative tissues of fungi" (Garraway et al., 1991), with a peripheral cortex, a living medulla, a central canal containing gas and an apical meristem (Motta, 1969; Garraway et al., 1991). This organ plays an important role in infection, dissemination, search for and colonization of woody substrates in soil (see Epidemiology).
The subterranean rhizomorph takes up and transports nutrients, water and oxygen (Smith and Griffin, 1971). The transport of nutrients has been studied by different experiments with radiolabelled elements (Anderson and Ullrich, 1982b and others); it appears to be bidirectional, but is mostly acropetal, which allows the woody food-base from which the rhizomorph originates to feed the growing apex. It is also likely that, at least in A. gallica and A. cepistipes, the rhizomorphic system can grow without any food-base, by internal reallocation of metabolites (Mohammed, 1987).
The different species have a very different capacity for rhizomorph growth
and development: the saprophytic species of the 'gallica group' (A. gallica,
A. sinapina, A. cepistipes) produce strong, fast-growing, long-living
rhizomorphs.The rhizomorphs of A. ostoyae, A. mellea, A. luteobubalina grow
more slowly. In addition, the rhizomorphs of A. mellea are short-living and
often difficult to detect in field, though they play a major role in infection. A. tabescens does not produce rhizomorphs in nature but it does in pure culture. The African species A. heimii produces rhizomorphs only in cool environments at high altitudes. Differences for this trait were also reported within a species; they account for a part of variability in the pathogenicity of individual genotypes.
Mycelial fans and cords
In conditions of abundant nutrition, especially in the living plant, the fungus initiates flat, white, poorly differentiated, aggregated organs, which have received different names: subcortical rhizomorphs (the 'rhizomorpha subcorticalis' of Persoon, 1801), mycelial cords and mycelial fans. Their general shape can be more or less linear (cords) or isodiametric (fans) according to the host and the localization. Essentially these organs assume a function of nutrition from the living host or the dead wood.
In vitro studies have shown that the rhizomorphs and the fans have the same origin: within certain genetic limits, it is possible to transform fans into differentiated rhizomorphs or vice versa by manipulating the composition of the culture medium.
Many wood-destroying fungi, including Armillaria species, form dark lines in dead wood. These lines (zone lines or pseudosclerotia) are actually dark surfaces which divide the colonized wood into different, more or less independent, volumes. These surfaces are made of dead, melanized, contiguous isodiametric cells. The phenomenon has nothing to do with 'compartmentalization', a resistance process of trees analysed by Shigo and Tippett (1981).
The physiological conditions of zone-line formation in Armillaria species have been studied by several authors (Campbell, 1934; Lopez-Real and Swift, 1975). These organs are mainly found in the heart wood; they are linked to a saprophytic phase of substrate exploitation which begins several weeks after infection.
In A. tabescens (Rhoads, 1956) and A. heimii (Pichel, 1956), the cankers and cracks at the surface of the roots or the collar are often occupied by fungal dark crusts which probably originate from melanization of cambial mycelial fans. These organs are less evident in the other three species which are studied here.
Basidiomata in species of Armillaria usually appear late in the infection process, most often on dead trees or on stumps. However, it is not uncommon to observe fruit bodies of A. mellea or A. ostoyae in the autumn at the bases of infected trees which are still alive.
Different species of Armillaria have very different propensities to fruit in the field. A. tabescens and A. ostoyae fruit rather commonly in nature (Rhoads, 1956), whereas the appearance of fruit bodies is a rare event for the African A. heimii (Pichel, 1956), although this species fruits easily in the laboratory.
Sexual Systems and the Karyological Cycle
The sexual and karyological problems in species of Armillaria have been summarized by Guillaumin et al. (1991a) but new outstanding results have been obtained since this date. The Armillaria group is unique amongst Basidiomycetes in that the secondary mycelium (formed after mating of two compatible haploid mycelia) is diploid and not dikaryotic. This characteristic seems to be common to all the species of the genus which have been studied to date. The existence of a double genetic recombination in the cycle of at least certain Armillaria species could be another characteristic of the genus.
The karyological cycle in species of Armillaria remained a mystery until 1973. Early researchers (Kniep, 1911; Kühner, 1946) had observed that hyphal cells are monokaryotic, irrespective of their origin (a single basidiospore, basidioma tissue or vegetative material). Hintikka (1973) was the first to observe a macromorphological difference between the haploid monospore isolates (of fluffy appearence) and the diploid cultures from basidioma tissue (flat and crustose); he established that the species he was studying (probably A. borealis) had a bifactorial (or tetrapolar) sexual incompatibility system. Korhonen (1978), Ullrich and Anderson (1978), Anderson (1982), Guillaumin et al. (1983), Kile (1983), Guillaumin (1986) and Kile and Watling (1988) showed that this is also the case for all the Armillaria species of the temperate areas (Europe, North America and Australasia), the only exception being A. ectypa, a rare species of European peat bogs (Guillaumin, 1973; Zolciak et al., 1997).
By contrast, the tropical species of Armillaria which have been studied to date do not appear to be tetrapolar: A. puiggarii from the West Indies is homothallic whereas the common African species A. heimii includes both homothallic and bipolar (unifactorial) heterothallic isolates (Mohammed and Guillaumin, 1993; Guillaumin et al., 1994). The subspecies A.mellea ssp. nipponica which has been reported from Japan and from tropical Africa is homothallic in both areas (Cha and Igarashi, 1995b, Abomo-Ndongo et al., 1997; Ota et al., 1998b). Another homothallic Armillaria taxon has been reported from southern China (K Korhonen, personal communication).
Compatible matings in heterothallic species result in the appearance of a crusty mycelium, the diploidy of which has been demonstrated by various methods (Korhonen and Hintikka, 1974; Anderson and Ullrich, 1982a; Peabody and Peabody, 1985). The karyological evolution of the tissues of the basidiome is complex and remains questionable; it is likely that in many cases, a somatic haploidization occurs in the sterile parts of the basidiome (Peabody and Peabody, 1985); this haploidization results in a genetic recombination in the young basidiome mimiking a meiosis (Peabody and Peabody, 2000; Grillo et al., 2000). Nevertheless, the normal meiosis also exists in the basidium; thus, a double recombination process is likely to take place in the cycle of certain heterothallic Armillaria species. These species (A. tabescens, A. gallica, A. ostoyae and most of the North American species) have dikaryotic, clamped cells in the subhymenium and at the base of the basidia, while others (A. mellea, A. luteobubalina and the other Australasian species) have not.
The karyological cycle of the homothallic species is another open problem. The vegetative mycelium is probably also diploid in these species (Mohammed et al., 1994b). In this case, the mycelium originating from the germination of a single spore could be directly infectious. In the case of the subspecies A. mellea ssp. nipponica, according to Ota et al. (1998b), homothallism results from a fusion of the postmeiotic nuclei in the basidium, followed by migration to the basidiospores of the diploid nuclei resulting from this fusion.
Diploid-haploid matings (the Buller phenomenon) take place both in tetrapolar species (Korhonen, 1978) and in the bipolar isolates of A. heimii (Mohammed et al., 1994b). This phenomenon is the basis of the most common method used for identification of the European and North American Armillaria species and is sometimes referred to as Korhonen's method (see Diagnostic Methods).
Basis of Pathogenicity
Destruction of bark, sap wood and heart wood is caused mainly by enzymatic activities: pectinases, cellulases, hemicellulases, peroxidases and laccase (Wahlström et al., 1991; Robene-Soustrade, 1993; Robene-Soustrade et al., 1998). Some of these enzymatic activities (especially laccase and polygalacturonase) are mainly detected in just-infected or just dying roots and seem particularly involved in the infection process, while other activities (CM-cellulase, b-glucosidase and b-xylosidase) are linked to the saprophytic decay of wood caused by saprophytic species and by parasitic species in the late stages of the disease (Robene-Soustrade et al., 1998).
Although the Armillaria species are known to synthesize several toxins belonging to the sesquiterpene group (Donnelly et al., 1990; Peipp and Sonnenbichler, 1992), most authors consider that these toxins (in contrast to the case of Rosellinia necatrix) do not play a major role in the disease.
The infection process has been reviewed by Rykowski (1975, 1980) and by Morrison et al. (1991). All authors agree that the basidiospores play no direct role in the parasitic phase of the cycle. Infection concerns only the large or middle roots, which are lignified and suberized. It can proceed according to two different mechanisms: by contact between a sound root and a subterranean rhizomorph, or by contact between a sound root and an infected root or piece of dead wood colonized by the fungus.
Infection through the subterranean rhizomorph has been described by Day (1927), Thomas (1934) and Guillaumin and Rykowski (1980). The general scheme is the same for conifers and hardwoods: in their growth through the soil, the subterranean rhizomorphs come into contact with roots to which they attach themselves by means of mucilage and produce short branches, the 'infection cones', which directly enter the root bark. After penetration has occurred, the infection cone separates into individual hyphae which colonize the bark. A second aggregation phase then occurs in the cambium, giving rise to the mycelial fans and flat subcortical rhizomorphs. No wound is required for such a penetration: in an experiment of Guillaumin and Pierson (1976) the rate of success of artificial infections on Prunus mahaleb was decreased when the host was wounded.
This 'classical' mode of infection is very common for A. mellea and A. ostoyae; it is probably more rare for A. luteobubalina and A. heimii and cannot exist with A. tabescens where subterranean rhizomorphs are not observed in nature.
Infection by direct contact between a diseased root (or a colonized wood fragment) and a living root probably concerns all five species: it was first described by Zeller (1926). The process is less precisely understood, but could involve preliminary degradation of the outer layers of the root by enzymatic and/or toxic activities. According to Morrison et al. (1991), in conifers, the first step of infection could consist of external proliferation of the fungus between the outer scales of the root.
Whatever the mode of infection, as soon as the fungus has reached the cambium, it begins to grow rapidly in both directions (to the root end and to the collar) by means of mycelial fans and subcortical white rhizomorphs.
Two kinds of dissemination occur: short-range dissemination through vegetative structures and long-range dissemination by basidiospores.
In short-range dissemination, the fungus spreads partly through the growth of the subterranean rhizomorphs in soil (Redfern, 1973) and partly by mycelium, mycelial fans and subcortical rhizomorphs growing in the living roots or in the dead wood.
Dissemination by subterranean rhizomorphs is particularly efficient for species of the 'gallica subgroup' (A. gallica, A. cepistipes, A. sinapina, etc.) which behave as saprophytes or opportunists. The long, thick, perennial rhizomorphs of these species are well adapted for finding and invading stumps and buried wood. As shown by Mohammed (1987), the subterranean rhizomorphs of the aggressive species (for instance A. mellea) are more fragile and short lived; their main role is in infection, not in dissemination.
Whatever the process, the vegetative dissemination in Armillaria species is very efficient; it results in the formation of large homogeneous genotypes (also named 'clones' or 'genets'). A genet of A. gallica described in Michigan occupied a minimum of 15 ha and was aged 1500 years (Smith et al., 1992). More recently, an even larger genet of A. ostoyae was found in eastern Oregon (T Dreisbach, USDA Forest Service, Pacific Northwest Research Station, personal communication, 2000). It covered 800 ha and its calculated age was at least 2400 years. This genet can be regarded as the biggest living individual ever detected in the world. Hodnett and Anderson (2000) have shown that, despite their age, these large clones are genetically completely homogeneous.
In long-range dissemination, the basidiospores of Armillaria are transported by wind and probably also by other agents. In contrast to vegetative dissemination, dissemination by basidiospores creates new genotypes. Germination of a basidiospore gives rise to a haploid mycelium which is probably short-lived unless it is diploidized by another compatible haploid mycelium, or by a diploid mycelium (the Buller phenomenon).
It is probable that new foci established on first-rotation forests originate from basidiospores (Rishbeth, 1988, 1991). However, the site of germination of basidiospores and the establishment of new diploid genotypes is not clearly known. By analogy with Heterobasidion annosum, it was thought to be the surface of cut stumps. However, Rishbeth (1964) failed to obtain regular germination of the basidiospores on stumps. Legrand et al. (1996) showed that stump removal does not prevent the appearence of numerous new genotypes on a stand submitted to clear felling.
Whatever the exact site of formation of the new diploids, it is of importance for the epidemiologist to appreciate the respective role of vegetative and sexual dissemination for a given Armillaria species and and in a given environment. More than 25 papers since the pioneering work of Korhonen (1978) on studies using the tools of population genetics: various methods including Somatic Incompatibility (SI) and the molecular or non-molecular markers have been used in order to map the teritories of the genets. The results obtained were diverse, even within the same Armillaria species: the genet of A. ostoyae of 800 ha found is eastern Oregon probably represents an extreme situation when sexual reproduction is completely inhibited. The opposite situation has been described for the same Armillaria species by Legrand et al. (1996) who found 38 genets on a stand ot 4 ha (average area of one genet: <500 m²).
The fungus is essentially preserved as mycelial masses in the dead wood buried in the soil; heart wood is colonized after sap wood and is slowly decomposed. Heart wood is often compartmentalized by zone lines which protect the mycelium against drying and antagonistic organisms. The period of conservation of the fungus depends mainly on the size of the wood fragments. On entire stumps, fungal survival can be estimated at several decades: for example, 40 years on English oak stumps according to Rishbeth (1972), 20 years on east African hardwoods according to Swift (1972). The fungus can also survive as mycelium in latent cortical necroses on living roots of symptomless trees (Whitney et al., 1989; Delatour and Guillaumin, 1995).
The mycelium preserved in stumps or in latent necroses can initiate new subterranean rhizomorphs or infect living roots directly by contact.
The large subterranean rhizomorphs of 'gallica subgroup' species can probably survive for several years and so play a role in inoculum conservation. However, the species of this subgroup are only weak pathogens.
The prevailing role of woody inoculum
The characteristics of woody inoculum (volume, age, nature and distribution of dead wood in soil) are the main epidemiological factors and are largely responsible for the evolution of the disease following planting. Three situations are especially risky.
The first is when planting follows recent deforestation or shrub clearance. Even if no symptoms of Armillaria root rot have been detected on the trees constituting the natural vegetation, their roots can carry latent necroses from which the fungus can colonize the entire root system after cutting of the tree (Delatour and Guillaumin, 1995). However, the type of tree removed is of importance; hardwoods, especially Quercus species, appear to be particularly hazardous even when they are followed by conifers (Rishbeth, 1972; Rykowski, 1985). A. ostoyae as a parasite is mostly aggressive to conifers, but as a saprophyte it can also colonize hardwood stumps and the mycelial survival and rhizomorph production are generally higher from hardwoods. In tropical arboriculture, the risk for woody plantations depends on the volume of wood left in the soil after deforestation and the small indigenous plantations which cannot use important means to uproot the stumps are often more hazardous (Onsando et al., 1997).
The second situation is when a new plantation succeeds a previous plantation, especially if the two woody species involved are susceptible to the same Armillaria species.
The third is if the plantation is sited on the banks of a river subject to flooding (wood carried in the current is deposited and buried together with alluvions).
In forest management, thinning and cutting often play an essential role: the first damage by Armillaria can be triggered by precommercial thinning or by the first commercial cuttings (Morrison and Mallett, 1996).
Weak or equilibrium parasitism and predisposition
Species of Armillaria are a natural component of the mycoflora of forests worldwide. In most cases, they do not cause important damage in these natural forests. They behave as wood decomposers (particularly the species belonging to the 'gallica subgroup') and weak necrotrophic pathogens, infecting and killing trees which are suppressed or stressed by diverse factors (Kile et al., 1991).
Delatour and Guillaumin (1985) distinguished three ecological categories among the agents of the root rots of trees: (i) the primary parasites which can be lethal in the absence of any predisposing factor; (ii) the equilibrium parasites (saprophytes which can become parasites and pathogenic if the host is enfeebled by certain factors) and (iii) the heart-rot agents. The parasites belonging to the last two categories have inferior pathogenic capacities. These three categories can be found among the Armillaria species. For instance, A. gallica generally belongs to type (ii), whilst A. borealis and A. cepistipes often belong to type (iii) on conifers.
The five species described here in detail (A. ostoyae, A. mellea, A. luteobubalina, A. tabescens and A. heimii) are those which commonly act as primary pathogens. However, in the presence of fairly resistant hosts, they can also behave as equilibrium parasites or heart-rot agents. For instance, A. mellea is currently a primary pathogen on orchard trees and grapevines, an equilibrium pathogen on adult Quercus species and a heart-rot agent on poplars.
Wargo and Harrington (1991) have reviewed the numerous factors which can act as stresses and thus induce equilibrium parasitism by Armillaria species. These factors can be abiotic (drought, excess of water responsible for anaerobic soil conditions, nutrient deficiencies, air pollution) or biotic (defoliators, sap-sucking insects, bark-infesting beetles, dwarf mistletoe (Byler, 1978), fungal diseases of foliage). An excessive density of stock can also favour the disease by increasing the competition between the trees: thus, insufficient thinning can be favourable to the disease for physiological reasons while excess of thinning can have the same result for epidemiological reasons (by increasing the inoculum potential). The equilibrium point can be very variable function of the host and environment: for example, Rosso and Hansen (1998) showed that on Douglas fir in the Cascade Mountains in Oregon, the impact of A. ostoyae was linked to epidemiological factors, but not to tree vigour. The results could be very different in other ecosystems.
Weak or equilibrium parasitism in Armillaria was studied by Wargo in the north-eastern USA, where colonization of hardwood trees (Acer saccharum and Quercus species) by Armillaria species is generally triggered by insect defoliation (Wargo, 1980, 1981). One effect of the stress is to enfeeble the host root defences against the fungus. The latent necroses, which are frequent on the root systems of many adult trees, probably play an important role in this restart of fungal growth in the roots; the mycelium confined in the necrosis is still alive and can then break the wound periderms (Delatour and Guillaumin, 1995).
Wargo (1972, 1975, 1980, 1984) has tried to analyse the biochemical ways through which the different stresses enhance the susceptibility of the hosts to Armillaria species. According to this author, several mechanisms can be involved, including hydrolysis of the starch of roots which provides the fungus with soluble sugars, disturbance of phenolic synthesis by the host, and decrease in the efficiency of the host enzymes which decay the wall of the fungal cells.
Of course, most of the weakening factors which trigger equilibrium parasitism can also play a role in cases of primary parasitism by modifying the balance between fungal pathogenicity and the host's responses.
Ecological requirements of Armillaria species
The European Armillaria species have different temperature requirements (Mohammed, 1987) which can explain their different distributions concerning latitude and altitude (Guillaumin et al., 1993). For instance, A. ostoyae is less thermophilic than A. mellea (their optimal temperatures for growth are 21 and 23°C, respectively) and can be found in Europe at higher latitudes and altitudes than A. mellea. However, A. mellea is less thermophilic than A. tabescens.
The same ecological differences between the three species can be observed in North America (Rhoads, 1945).
Armillaria root rot is found in all soil types. Contrary to some presumptions, it is not restricted to heavy or damp soils, or to those with a particular pH. However, differences exist between the species concerning the optimal pH range for growth of subterranean rhizomorphs: it is generally accepted (Morrison, 1974; Guillaumin and Lung-Escarmant, 1985) that the growth of the rhizomorphs of A. ostoyae is higher in acidic soils whereas A. mellea and A. gallica have a preference for neutral pH.
Contrary to some presumptions, converging results indicate that Armillaria rot rot is generally more severe on sandy soils than on clayey soils (Wiensczyk et al., 1997; Mallett and Maynard, 1998) however, the incidence of soil texture could be indirect, through an effect on host resistance.
The importance of the microbiological environment on growth and pathogenicity of Armillaria species is just beginning to be suspected. It is well known that certain microfungi of the rhizosphere of large roots (for example, Trichoderma species) are antagonistic to Armillarias. Kwasna (1996, 1997) has shown that other fungi, especially members of the Zygomycetes, behave as synergists for Armillaria species: the composition of the rhizosphere and its evolution could play an important role in the development of the rhizomorphs outside the root and their penetration into it.
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Bark||hyphae||Yes||Pest or symptoms usually invisible|
|Bulbs/Tubers/Corms/Rhizomes||hyphae||Yes||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Roots||hyphae||Yes||Yes||Pest or symptoms usually invisible|
|Stems (above ground)/Shoots/Trunks/Branches||fruiting bodies; hyphae||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Wood||hyphae||Yes||Pest or symptoms usually invisible|
|Plant parts not known to carry the pest in trade/transport|
|Fruits (inc. pods)|
|True seeds (inc. grain)|
ImpactTop of page Although A. luteobubalina can attack many orchard or amenity trees which are either indigenous or have been introduced into Australia (Smith and Kile, 1981; Kile et al., 1983; Falk and Parberry, 1995), the most significant damage concerns native eucalypt forest where the fungus behaves as a primary pathogen. Forests of the highlands of western central Victoria are those most severely damaged, the main species of the area being Eucalyptus obliqua, E. radiata and E. viminalis (Kile, 1983). Edgar et al. (1976) estimated that 3% of the forests of this zone are moderately to severely affected. Important damage has also been reported from Tasmania, mainly on E. obliqua and E. regnans (Kile, 1980) and from south-western Australia on E. diversicolor (Pearce et al., 1986), E. marginata (Shearer and Tippett, 1988) and E. wandoo (Shearer et al., 1997).
DiagnosisTop of page
Isolation of the fungus must be carried out on a medium containing benomyl or thiabendazole (Guillaumin, 1977). Most of the time, the isolates obtained are diploid, their macroscopical aspect on malt agar or potato dextrose agar (presence of rhizomorphs, crusts and zone lines) is typical of a species of Armillaria and no confusion is possible with another fungal genus.
The distinction between the different species of Armillaria is more difficult. However, it is often of importance to know if the species present is one which is highly pathogenic (for instance A. mellea or A. ostoyae) or saprophytic and weakly pathogenic (A. gallica, A. cepistipes, etc.).
Different methods have been proposed for the identification of the European species. Some of these methods can also be used for the North American species.
Interfertility testing has become a common method for routine identification of unknown cultures (Korhonen, 1978; Anderson and Ullrich, 1979; Guillaumin and Berthelay, 1981; Guillaumin et al., 1991a). The test consists of pairing the unknown culture with haploid tester strains that represent each species to which the isolate possibly belongs. The pairings are carried out on malt agar, in Petri dishes. When the new culture and the tester strain are conspecific, the tester is diploidized (its morphology turns to crusty). When the new culture and tester strain belong to different species, the tester is not modified and a pigmented line appears in the agar medium between the two thalli. The method works with both haploid and diploid isolates (in the latter case, thanks to the Buller phenomenon).
The morphological characteristics of diploid mycelial mats in standardized pure cultures (i.e. on 2% malt agar in Petri dishes) characterize the seven European species sufficiently to assist identification. (Guillaumin and Berthelay, 1981; Rishbeth, 1986; Intini and Gabucci, 1987; Mohammed, 1987; Marxmüller, 1994). However, the method cannot distinguish A. gallica from A. cepistipes.
Other differences between the species can be used as tools to assist identification, such as the morphology of the basidiomata in nature (Gonthier, 2010); morphology of the subterranean rhizomorphs in nature (Morrison, 1982) or in a mist case (Mohammed, 1987); capacity to fruit in vitro (A. tabescens and A. ostoyae fruit more easily in vitro than the other species); and response to temperature (Mohammed, 1987).
Since the 1980s, biochemical, immunological and molecular methods of diagnosis have been developed. The biochemical methods include electrophoresis of the denaturated total proteins (SDS PAGE) (Lung-Escarmant et al., 1985c) and isoenzyme analysis (e.g. Morrison et al., 1985b; Lin et al., 1989; Agustian et al., 1994; Bragaloni et al., 1997). Although these methods often gave satisfying results, isoenzyme analysis did not become a routine method for Armillaria species identification.
Immunological tests included the use of polyclonal antibodies (Lung-Escarmant and Dunez, 1980) and monoclonal antibodies (Priestley et al., 1994). These methods have also remained experimental.
A molecular approach has been developed for the Armillaria group, mainly by J. Anderson's team at Toronto, Canada, since 1987. This approach was recently reviewed by Schulze and Bahnweg (1998). The first methods prior to the emergence of PCR methods used restriction of mitochondrial DNA (mt-DNA) or the non-transcribed parts of ribosomal DNA (Anderson et al., 1989; Smith and Anderson, 1989). These methods revealed an interspecies variability much higher than intraspecies variability and they contributed largely to the distinction between the Armillaria species. However, this approach was laborious and time consuming and involved the development of probes and the use of Southern blotting and so did not generate routine identification methods.
The PCR approach was easier to use. The first method used was RAPD, which uses arbitrary decameric primers. RAPD was well adapted to the analysis of intraspecific variability (Guillaumin et al., 1996) but was too sensitive for species identification.
The method which appeared most suitable for diagnosis was PCR amplification of the non-transcribed parts of ribosomal DNA, ITS (Internal Transcribed Spacer) and IGS (Intergenic Spacer region) followed by RFLP with one or a few restriction enzymes RFLP-PCR (Aguín-Casal et al., 2004). Using the sequence data of the IGS obtained by Anderson and Stasovski (1992), Harrington and Wingfield (1995) proposed a method involving amplification of the first part of the IGS (IGS1) followed by cutting the amplicon with the enzyme Alu I. The method was improved by other teams in the USA, Europe and Japan (Banik et al., 1996; Terashima et al., 1998; White et al., 1998; Perez-Sierra et al., 1999). This method is well on the way to becoming the new routine method for Armillaria species identification. In France it is now used concurrently with the traditional method based on mating tests. The main advantage of the method is that it does not require isolation of the fungus. Sometimes it does not even require extraction of DNA. IGS can be amplified directly from decayed wood or mycelial fans.
Chillali et al. (1998) used the ITS. Digestion using a set of restriction enzymes (Cfo I, Alu I and Hinf I) allowed the distinction of all European Armillaria species. Bragança et al. (2004) found the ITS1 region to be a reliable molecular marker for A. mellea, particularly when HinfI restriction analysis was applied, since two fragments with 245 bp and 125 bp have been obtained for this most aggressive species.
The main drawback of such methods is that nobody can be sure that all the possible patterns for a species have been detected, especially for species that are highly variable and/or have a wide geographical range. It is recommended that molecular tests are used in parallel with traditional identification methods based on mating type reactions and the morphology of mycelial mats in culture.
New molecular methods such as Sequencing with Arbitrary Primer Pairs (SWAPP) and the use of Microsatellites are currently being developed, especially for phylogenetic analyses (Piercey-Normore et al., 1998). However, it is unlikely that these methods will be used for routine diagnosis.
Detection and InspectionTop of page Observe the symptoms on the aerial parts of affected plants and the disposition of the dead or declining plants in the plot (are they distributed in patches?).
Observe the base of the trunk and the collar for the presence of cracks, basal cankers, resin, gums, etc.
Cut tangentially the bark of the collar and the large roots with a knife or an axe. Search for thick, white, continuous, mycelial fans at the level of the cambium.
The presence of cylindrical subterranean rhizomorphs and/or fruit bodies can sometimes help to conclude a diagnosis.
See also Similarities to Other Species for a discussion on possible confusion with other diseases.
The presence of Armillaria in the soils of forest plots has been investigated using trapping methods, mostly wood logs (Wiensczyk et al., 1996). The problem with this trapping method is that it detects mainly species of Armillaria, which form rhizomorphs in soil (for example, A. gallica, A. cepistipes and A. sinapina) and are generally less pathogenic.
Correlation of the amount of damage on the roots with the intensity of the above-ground symptoms gave few results (Whitney, 1997; Morrison and Pellow, 1998) and was dependent on environmental conditions and the age of the stands (Morrison and Pellow, 1998).
Aerial photography has been used in France (Guyon et al., 1985), North America (Williams and Leaphart, 1978) and Australia (Shearer and Tippett, 1988). It generally detects gaps in forests or plantations and must be completed by ground inspection which allows distinction of Armillaria root rot from other root rots (e.g. Heterobasidion or Rosellinia), other diseases (e.g. Phytophthora), insect attacks (bark beetles foci) or abiotic problems (localised anoxy).
Similarities to Other Species/ConditionsTop of page On orchard trees, grapevines and certain amenity trees, species of Armillaria can sometimes be confused with Rosellinia necatrix, the agent of white root rot, a fungus belonging to the Ascomycota. However, the host list of the two diseases is not exactly the same: in western Europe, R. necatrix is more frequent on pome fruits and fig trees, whereas species of Armillaria (mainly A. mellea) are more frequent on stone fruits, walnuts and grapevines. However, cherries and citrus are attacked by both parasites with comparable frequencies.
R. necatrix is generally easily distinguished from species of Armillaria by the presence of mycelium and mycelial strands outside the root and by the small, thin, finger-like fans inside the bark (the fans in species of Armillaria are larger, more continuous and mostly localized at the level of the cambium).
In addition, R. necatrix does not rot the wood: the sapwood becomes dry and the presence of the fungus is marked by black halos, which are very different from the distinct zone lines characteristic of Armillaria.
In tropical countries, several other Basidiomycetes can cause root rots of trees, particularly Rigidoporus lignosus, Phellinus noxius and species of Ganoderma. These can sometimes infect the same hosts as A. heimii, for instance rubber (Pichel, 1956; Nandris et al., 1987). It is not possible here to describe the symptoms of these different diseases in detail. Like R. necatrix, R. lignosus is easily distinguished from species of Armillaria by the presence of mycelial cords and webs on the surface of the root. These organs are white, cream or yellowish. Where species of Ganoderma are concerned, external cords are also observed, but their colour is red to purple; the rotten wood is wet and reddish. P. noxius, the agent of brown rot disease, characteristically causes roots to be surrounded by a dark crust in which earth and sand particles are aggregated, with brown or black hyphae sometimes constituting sclerotia or stromas.
The presence of large, thick mycelial fans at the level of the cambium, together with the cylindrical rhizomorphs (when they are present) allows, in most cases, Armillaria species to be distinguished from these various polypores.
See Morphology for a discussion of the differences between Armillaria species A. heimii, A. luteobubalina, A. mellea, A. ostoyae and A. tabescens.
Prevention and ControlTop of page
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.
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.
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.
The fumigants which were most often used in the past for destroying Armillaria inoculum in soil included carbon disulphide (Bliss, 1951; Darley and Wilbur, 1954), the role of which was thoroughly investigated in California by Munnecke's team at the end of the 1960s (Kolbezen et al., 1969; Munnecke et al., 1969, 1970; Ohr et al. 1973). However, other fumigants such as methylisothiocyanate, metam-sodium, nabam, dazomet and tetrathiocarbonate also show some efficacy. Many experiments conducted in France in the 1970s and 1980s led to a treatment with metam-sodium, which is now routinely used in the Bordeaux vineyards (Dubos et al., 1998). In California, USA, the recommended fumigant is tetrathiocarbamate (Elkins et al., 1998; Adaskaveg et al., 1999). In general, the treatment lessens the inoculum potential of the soil, but does not eradicate the parasite and other measures such as deep ripping and root removal must be used for complete control.
Whichever fumigant is used, three factors play a major role in the success of the treatment: (i) the number, size and depth of the root fragments colonized by the fungus; (ii) the temperature during and after the treatment; and (iii) the nature of the soil (light, sandy soils are more favourable than clayey soils). The presence of a hardened or compacted layer of soil near the surface is very unfavourable to the success of the treatment.
Chemical Treatment of Living Plants
Among the drugs used as soil fumigants, only one (tetrathiocarbonate) can also be used, at lower concentrations, on living plants. Certain growth regulators such as paclobutrazol (Jacobs and Berg, 2000) or herbicides such as glyphosate (Zolciak, 1998) also show an inhibitory effect on Armillaria in vitro and in situ. Mixtures of phenolics originating from coal distillation have also been tested, generally with poor results.
Systemic fungicides have been studied by some authors. The localization of the parasite in roots makes it difficult to reach with systemic fungicides, which are essentially transported in xylem. In Australia, Heaton and Dullahide (1990) obtained some success with phosphorous acid on peach trees attacked by A. luteobubalina; however, it does not seem that the method has developed in practice. G Lercari, F Brunatti and F Calceoni, Istituto Regionale per la Floricoltura, San-Remo, Italy (unpublished results, 1994) found, in experimental conditions, some efficacy of molecules belonging to the morpholine and tridemorph groups (fenpropimorph, cyproconazole). The efficacy of propiconazole was reported by Adaskaveg et al. (1999).
The most thoroughly studied antagonists of Armillaria species have been different species of the Adelomycete genus Trichoderma, (and also the related genus Gliocladium). In vitro or in semi-natural conditions, the antagonistic effect of Trichoderma on Armillaria is often spectacular (Aytoun, 1953; Dubos et al., 1978). However, attempts to control Armillaria by artificial introduction of a Trichoderma inoculum on various substrates were generally unsuccessful, because populations of the Adelomycete in the soil tend to decrease with time. Even when significant amounts of organic matter were brought with the antagonistic fungus, the application of Trichoderma in the field generally led to disappointing results (Otieno, 1998).
However, it was shown that Trichoderma species are fairly resistant to soil fumigation, which suggested associating the action of the indigenous Trichoderma inoculum with sublethal doses of carbon disulphide: in fumigated soils, Armillaria can be killed partly by direct fumigant toxicity and partly by subsequent action of Trichoderma species (Munnecke et al., 1973; Ohr et al., 1973).
A different strategy consists of using direct competition for the colonization of woody substrates: in this case, control is achieved in the saprophytic phase. This approach was suggested by Leach as long ago as 1937. Several species of common wood-decaying basidiomycetes (Hypholoma fasciculare, Coriolus versicolor, Megacollybia platyphylla, Stereum hirsutum, Gymnopilus spectabilis), have been advocated for this purpose by the different teams working on the subject (Pearce and Malaczuk, 1990; Gallet et al., 1994; Nicolotti et al., 1993). However, to date, this method remains experimental. Recent studies (Burrill et al., 1999) tried to include the role of wood decaying competitors in the management of stand thining and cutting.
Use of Tolerant Host Species or Rootstocks
In situ host resistance to Armillaria root rot is a complex phenomenon, depending not only on the genotype of the host, but also on the genotype of the pathogen and environmental influences. Lists of tolerant and susceptible species have been established by several authors. Concerning conifers, differences between species in their susceptibility to Armillaria species were noted, for instance, by Morrison (1981) in British Columbia (towards A. ostoyae) and by Gibson (1960) in Kenya (towards A. heimii). However, some species with high tolerance to infection in one location can be quite susceptible in other locations: Douglas fir (Pseudotsuga menziesii) is considered to be very susceptible to A. ostoyae within its natural range in north-western America (Morrison, 1981), while in western Europe, the same species is one of the more tolerant among conifer species and is recommended for planting in areas where a risk exists with A. ostoyae (Greig and Strouts, 1983; Delatour and Guillaumin, 1985).
Concerning fruit cultures in more homogeneous environmental conditions, the behaviour of the species is generally more stable. The use of tolerant rootstocks is often the best method of controlling the disease in fruit culture. Tolerant rootstocks exist for walnuts (Jugans nigra and J. hindsii, Desray et al., 1998), pears (quince is susceptible, but the rootstock 'pear' is tolerant - Thomas et al., 1948), citrus (sour orange is highly resistant, Rhoads, 1948b; Tuset et al., 1999), cherry (the rootstocks belonging to the species Prunus avium are more tolerant than those belonging to P. mahaleb and P. cerasus - Proffer and Jones, 1988). Several tolerant rootstocks are available for peaches, almonds and apricots (Thomas et al., 1948; Guillaumin et al., 1993; Beckman et al., 1998): they are found within the plums, for instance Prunus domestica (common plum), P. insititia, P. cerasifera (myrobalan), the American P. angustifolia and P. munsoniana. Certain hybrids between these species and peach have retained the tolerance to Armillaria of the plum parent, associated with satisfying agronomical characteristics (Nicolas and Bonet, 1996).
In certain cases, it is possible to save trees already infected by the parasite if the attack is not too advanced and the tree is worth saving. The collar and upper parts of the main roots should be uncovered, the diseased parts cut out and fungicides applied to the wounds.
It is also advisable to leave the main roots exposed to the air during a whole summer. The combined action of drought and high temperatures may stop progression of the fungus. This method, in association with fungicide application, is used on a large scale in Gabon in Hevea plantations infected by Armillaria heimii (Van-Cahn, CIRAD Hevea, Libreville, Gabon, unpublished results).
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