Armillaria luteobubalina

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Armillaria luteobubalina
Armillaria luteobubalina 67510.jpg
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Basidiomycota
Class: Agaricomycetes
Order: Agaricales
Family: Physalacriaceae
Genus: Armillaria
Species:
A. luteobubalina
Binomial name
Armillaria luteobubalina
Watling & Kile (1978)
Armillaria luteobubalina
Information icon.svg
Gills icon.png Gills on hymenium
Convex cap icon.svgFlat cap icon.svg Cap is convex or flat
Sinuate gills icon2.svg Hymenium is sinuate
Ring stipe icon.svg Stipe has a ring
Transparent spore print icon.svg
 Spore print is white
Parasitic fungus.svgEcology is parasitic
Mycomorphbox Edible.pngEdibility is edible

Armillaria luteobubalina, commonly known as the Australian honey fungus, is a species of mushroom in the family Physalacriaceae. Widely distributed in southern Australia, the fungus is responsible for a disease known as Armillaria root rot, a primary cause of Eucalyptus tree death and forest dieback. It is the most pathogenic and widespread of the six Armillaria species found in Australia. The fungus has also been collected in Argentina and Chile. Fruit bodies have cream- to tan-coloured caps that grow up to 10 cm (4 in) in diameter and stems that measure up to 20 cm (8 in) long by 1.5 cm (1 in) thick. The fruit bodies, which appear at the base of infected trees and other woody plants in autumn (March–April), are edible, but require cooking to remove the bitter taste. The fungus is dispersed through spores produced on gills on the underside of the caps, and also by growing vegetatively through the root systems of host trees. The ability of the fungus to spread vegetatively is facilitated by an aerating system that allows it to efficiently diffuse oxygen through rhizomorphs—rootlike structures made of dense masses of hyphae.

Armillaria luteobubalina was first described in 1978, after having been discovered several years earlier growing in a Eucalyptus plantation in southeastern Australia. It distinguished itself from other known Australian Armillaria species by its aggressive pathogenicity. It may take years for infected trees to show signs of disease, leading to an underestimation of disease prevalence. Studies show that the spread of disease in eucalypt forests is associated with infected stumps left following logging operations. Although several methods have been suggested to control the spread of disease, they are largely economically or environmentally unfeasible. Phylogenetic analyses have determined that A. luteobubalina is closely related to A. montagnei and that both of these species are in turn closely related to the Brazilian species A. paulensis . The distribution of A. luteobubalina suggests that it is an ancient species that originated before the separation of the precursor supercontinent Gondwana.

History and phylogeny

Armillaria luteobubalina was first described in 1978 by mycologists Roy Watling and Glen Kile, who studied its effects on a fast-growing plantation of Eucalyptus regnans near Traralgon, Victoria. The plantation, established in 1963, consisted largely of trees with a mean height of about 25 m (80 ft). A cluster of dead and dying trees discovered in 1973 suggested attack by a virulent primary pathogen, that is, one capable of infecting a host before invasion by other, secondary pathogens. This finding was inconsistent with the pathogenic behaviour of the known Armillaria species in Australia at the time, A. mellea and A. elegans. Further study over the next few years showed that the fungus spread by the growth of underground mycelia in root systems, expanding outward from the initial infected stump at an average of 2.5 m (8.2 ft) per year. Most Australian records of Armillaria infections referred to A. mellea, based on the presence of black rhizomorphs. [1] For over one hundred years, A. mellea was thought to be a pleiomorphic (occurring in various distinct forms) species with a widespread distribution and host range, and variable pathogenicity. [2] which led to great confusion among taxonomists and plant pathologists alike. [3] In 1973, Veikko Hintikka reported a technique to distinguish between Armillaria species by growing them together as single spore isolates on petri dishes and observing changes in the morphology of the cultures. [4] Using similar techniques, mycologists eventually determined that the Armillaria mellea species complex in Europe and North America in fact consisted of five and ten distinct "biological species", respectively. [5] [6]

Watling and Kile compared the macroscopic and microscopic characters of the pathogenic Armillaria with A. polymyces (now known as A. obscura ), A. mellea, A. limonea and A. novae-zelandiae and found sufficient differences between them to warrant designating the species as new. Its specific epithet is derived from the Latin lutea "yellow", and was chosen to highlight an important distinguishing characteristic: the strong yellow colour of the cap and lack of reddish or brown tones in the stem typical of other resident Armillaria. [1]

A phylogenetic study of South American Armillaria species concluded that A. luteobubalina is in a lineage that includes A. montagnei , and these are sister to a lineage containing A. paulensis , [7] a species known from a single specimen collected in São Paulo, Brazil. [8] Although they are very similar, specimens of A. luteobubalina have smaller spores than Argentinian specimens of A. montagnei, and their distinctness is well-supported with phylogenetic analysis. [9] Based on analysis of pectic enzymes, A. luteobubalina is closely related to A. limonea , a species found in New Zealand; [10] this result corroborates phylogenetic analyses reported in 2003 [11] and 2006. [12] Molecular analysis of 27 collections of A. luteobubalina from southwest Western Australia and one from Traralgon revealed four distinct polymorphic groups. The genetic variety suggests it is native to Australia. [13]

Description

Mushroom caps are covered with tiny scales and have an umbo. Armillaria luteobubalina 67511.jpg
Mushroom caps are covered with tiny scales and have an umbo.

Up to 10 cm (4 in) in diameter, the cap is convex to flattened in shape with a central umbo (a rounded elevation) and is various shades of cream, yellow and tan. The cap surface is covered with darker scales and feels rough to the touch. The cap edge, or margin, is rolled inward in young specimens. The crowded gills are sinuate and white to cream in colour initially, brownish-cream or pinkish brown in maturity, and sometimes with yellow or rust-coloured marks close to the margins. [14] The stem is central (that is, it joins the cap in the centre) and is up to 20 cm (8 in) long by 1.5 cm (1 in) thick. It is slightly thicker at its base than its apex, sometimes almost bulb-like. The stem surface is streaked with fibrils that run up and down its length. It has a floppy yellow wool-like ring which may develop irregular, jagged edges with time. The flesh is white, and in the stem has a woolly or stringy consistency. [1] Although it has a hot-bitter taste, Armillaria luteobubalina is edible, and cooking removes the bitterness. [15]

Microscopic characteristics

The spore print is white when fresh, but becomes more cream-coloured when dry. The smooth spores are oval to ellipsoid, hyaline (translucent), non-amyloid (meaning they do not absorb iodine from Melzer's reagent), and typically measure 6.5–7.5 by 4.5–5.5  μm. The basidia (spore-bearing cells) are thin-walled, hyaline, and lack clamp connections at their bases. They are usually four-spored but occasionally two-spored, with sterigmata (projections that attach to the spores) up to 4 μm long. The cheilocystidia (cystidia that occur on the edge of a gill) are mostly club-shaped, thin-walled, hyaline, and measure 15–30 by 6–10 μm. [1]

Similar species

Five other Armillaria species are found in Australia. [16] Within the range of A. luteobubalina, A. hinnulea is restricted to gully habitats. A. fumosa is a rarer species found only in poorly drained or seasonally wet locations. [17] A. luteobubalina and A. montagnei share cap features and a similar unpleasant flavour, but the latter species has an olive-tinged cap, larger spores (9.5–11 by 5.5–7 μm compared to 6.5–7.5 by 4.5–5.5 μm) and a more conspicuous annulus than those found in A. luteobubalina. [9] The morphology of the vegetative structures of A. limonea is distinctly different than A. luteobubalina, and can be used to distinguish the two species. [18] A. novae-zelandiae has a sticky more flattened cap and stem below the ring and is found in wet forests, and A. pallidula is a species with cream gills maturing to pale pink found in tropical Australia arising from dead tree stumps or the roots of dead or living trees. [19] A. luteobubalina is the only Armillaria species which occurs in Western Australia. [15] Distinguishing Australian species is economically important, because A. luteobubalina is more pathogenic than the other members of the genus. A molecular diagnostic test, developed in 2002, can accurately identify each species using DNA extracted from its mycelia. Before this, species identification was limited to times when fruit bodies were in season. This technology also revealed a variation in the molecular material of A. luteobubalina that suggested sexual reproduction. [20]

Habitat and distribution

A. luteobubalina grows in Karri forests, like this one in Pemberton, Western Australia. Karri forest.jpg
A. luteobubalina grows in Karri forests, like this one in Pemberton, Western Australia.

Armillaria luteobubalina has been recorded in southeastern Australia, from the southeastern corner of Queensland through eastern New South Wales and across Victoria into southeastern South Australia. It also occurs in Tasmania and southwestern Western Australia. [14] Those of the karri forests (consisting largely of the species E. diversicolor ) of the southwest have paler and yellower caps than those in the jarrah forests (which contain predominantly Eucalyptus marginata ) further north. [15] The fruit bodies arise on wood, especially on stumps or around the base of trees, and often in huge numbers. They usually appear between April and July, although most production occurs in the second half of May. [21] Abundant in woodlands, it can invade gardens and orchards, where it can attack many woody plants. [19] [22] The honey fungus infected and killed many plants near tuart trees ( Eucalyptus gomphocephala ) which had been cut down near Kings Park in suburban Perth. [15] Armillaria luteobubalina is commonly found in eucalyptus forests in Australia, [1] [21] and is thought to be the most pathogenic and most widespread Armillaria species in the major western Australian forest types. [23] [24] The mushroom has also been reported from southern South America, in Argentina and Chile. [7] A 2003 study of the molecular phylogenetics and pattern of its distribution in South America and Australia indicate that A. luteobubalina is an ancient species, originating before the separation of the precursor supercontinent Gondwana. Genetic differences between isolates in the South American and Australian populations indicate a long period of geographical separation, and the authors suggest that they "later might be regarded as independent taxa". [11]

Root rot

Young fruit body found in Wielangta forest in southeastern Tasmania, Australia Wielangta Unidentified Fungus 5164.jpg
Young fruit body found in Wielangta forest in southeastern Tasmania, Australia

Appearance of infected trees

Trees that are infected by A. luteobubalina show characteristic symptoms both above and below ground. Above the ground, the base of the tree develops inverted V-shaped lesions, and the infected wood undergoes white rot, a fungal wood decay process where the cellulose and lignin of the sapwood are both broken down, leaving the wood stringy. The bark of the stem dies and becomes discoloured up to 3 m (10 ft) above the ground. Clusters of fruit bodies appear at the base of the tree in autumn. Crowns may show gradual deterioration, or tree death may occur suddenly. Below the ground, characteristic symptoms of infections include rotting the ends of tree roots, white-rotted sapwood, and the presence of fan-shaped areas of white mycelium below dead or infected bark. [16]

Occurrence

In selectively logged eucalypt forests in the central highlands of Victoria, it has been estimated that about 3–5% of the forest area is "moderately to severely affected" by Armillaria root rot caused by A. luteobubalina. [25] A review of eucalypt plantations planted in New South Wales from 1994 to 2005 found that infection by A. luteobubalina was rare, and only accounted for 1% of mortality in total. In this instance, the cases had been restricted to Eucalyptus nitens on the Dorrigo Plateau. [26] Unlike other Armillaria species found in Australia's native forests, which require a host tree to become weakened by prior infection by a different species, A. luteobubalina is a primary pathogen, and can infect healthy trees. [25] [27] Tree roots may be infected for years before showing above-ground symptoms, making it difficult to accurately assess the true extent of disease in a forest stand. [28] Surveys are usually conducted in autumn, to coincide with the appearance of fruit bodies; infection is assessed by the presence of basal scars on the trees, and the appearance of fruit bodies. Several factors, however—such as cost, variable on-site conditions, and non-symptomatic diseased trees—make it difficult for such surveys to reliably detect all infections. One study showed that above-ground examinations detected only 50% of the trees actually infected, leading to underestimation of the incidence of true infection by 20–40%. The study used more intensive surveying methods to determine that 25- to 30-year-old karri regrowth forests in western Australia showed an average of 40–45% incidence of infection. [16]

Disease spread

A dense cluster of fruit bodies growing on a rotting stump Armillaria luteobubalina 151150.jpg
A dense cluster of fruit bodies growing on a rotting stump

Several studies have shown that the spread of Armillaria root rot in eucalypt forests is associated with infected stumps that remain after an area has been logged. [28] [29] [30] Armillaria luteobubalina can persist on these stumps, using them as a source of food for up to 25 or more years. [27] In one case reported in Ovens, Victoria, the disease was spread to blueberry plants (Vaccinium species) via buried fragments of infected Eucalyptus that remained following preparation of the previously forested site for planting. [31] In individual forest stands, [32] fungal infection is usually found in discrete disease patches separated by stands of healthy trees—a discontinuous distribution. [27] Large-scale aerial photography can be used to identify regions of forest infected by the species. [33] The species also causes damage to trees and bushes in coastal dune woodlands, shrubland, and heath communities. [34] It can be found on a wide range of hosts, but is most commonly associated with (in order of decreasing frequency) jarrah ( Eucalyptus marginata ), bull banksia ( Banksia grandis ), marri ( E. calophylla ), Lasiopetalum floribundum , and Acacia saligna . [35] It has also infected scattered populations of wandoo ( E. wandoo ). [36] The fungus has also been reported to infect Nothofagus species in Argentina, and Pinus radiata in Chile. [7] Armillaria luteobubalina uses "an elaborate, sophisticated aeration system" that enables it to efficiently deliver oxygen into the rhizomorphs, helping it thrive in low-oxygen environments. [37] [38] When grown in culture, the mycelium develops into a continuous region of tissue with a perforated crust. This tissue is hydrophobic and resistant to becoming waterlogged. Rhizomorphs develop beneath clusters of so-called "air-pores" near the perforations. These gas spaces connect the atmosphere with the central canal of the rhizomorph, to facilitate diffusion of oxygen and satiate the organism's high oxygen requirement during growth. This aeration system is thought to be an important factor in the organism's pathogenicity, allowing it to grow on wet or waterlogged root surfaces and send hyphae or rhizomorphs into live roots or cut stumps, where conditions may be hypoxic. [38] The rhizomorphs have a dichotomous branching pattern, so that they split or bifurcate at various intervals. Experiments and field observations have shown that this allows the fungus to be a more aggressive and virulent pathogen than Armillaria species whose rhizomorphs branch monopodially (where lateral branches grow from a main stem). [39] Although the structure of A. luteobubalina rhizomorphs is specialised for spread in potentially anaerobic conditions, the soil mycelium is adaptive and can amplify the absorptive surface of peripheral hyphae in response to the presence of nutrient-rich soil. [40]

Control

Methods for controlling the spread of Armillaria root rot include physical removal of infected trees, stumps and large roots; [41] fumigation of soil around infected hosts; and injection of fumigants directly into infected hosts. [42] These methods are often not practical due to high cost, introduction of toxic chemicals that affect other organisms, or health and safety issues for the operator. [42] [43] Biological control is another method that has been investigated to control root rot caused by A. luteobubalina. In one study, thinning stumps of Eucalyptus diversicolor were simultaneously inoculated with A. luteobubalina and one of the saprobic wood decay fungi Coriolus versicolor , Stereum hirsutum and Xylaria hypoxylon ; all three fungi significantly reduced infection by A. luteobubalinea. [44] These results were echoed in another study of stumps in karri regrowth forests, where it was shown that the presence of other wood decay fungi suppressed the growth of A. luteobubalina on the stump base. [24]

See also

Related Research Articles

<i>Armillaria</i> Genus of fungi

Armillaria is a genus of fungi that includes the A. mellea species known as honey fungi that live on trees and woody shrubs. It includes about 10 species formerly categorized summarily as A. mellea. Armillarias are long-lived and form the largest living fungi in the world. The largest known organism covers more than 3.4 square miles (8.8 km2) in Oregon's Malheur National Forest and is estimated to be 2,500 years old. Some species of Armillaria display bioluminescence, resulting in foxfire.

<i>Armillaria mellea</i> Species of fungus

Armillaria mellea, commonly known as honey fungus, is an edible basidiomycete fungus in the genus Armillaria. It is a plant pathogen and part of a cryptic species complex of closely related and morphologically similar species. It causes Armillaria root rot in many plant species and produces mushrooms around the base of trees it has infected. The symptoms of infection appear in the crowns of infected trees as discoloured foliage, reduced growth, dieback of the branches and death. The mushrooms are edible but some people may be intolerant to them. This species is capable of producing light via bioluminescence in its mycelium.

<span class="mw-page-title-main">Mycelial cord</span> Structure produced by fungi

Mycelial cords are linear aggregations of parallel-oriented hyphae. The mature cords are composed of wide, empty vessel hyphae surrounded by narrower sheathing hyphae. Cords may look similar to plant roots, and also frequently have similar functions; hence they are also called rhizomorphs. As well as growing underground or on the surface of trees and other plants, some fungi make mycelial cords which hang in the air from vegetation.

<i>Armillaria tabescens</i> Species of fungus

Armillaria tabescens is a species of fungus in the family Physalacriaceae. It is a plant pathogen. The mycelium of the fungus is bioluminescent.

<i>Rhizomorpha subcorticalis</i> Species of fungi

Rhizomorpha subcorticalis is a species name that has been used to characterize certain fungal plant pathogen observations where the pathogen is evident only through mycelial cords ("rhizomorphs"). The species in question very likely also produces reproductive structures which would allow it to be situated in the normal taxonomic tree, especially if DNA analysis is available. A name like R. subcorticalis should only be used where such identification is impossible.

<i>Armillaria fuscipes</i> Species of fungus

Armillaria fuscipes is a plant pathogen that causes Armillaria root rot on Pinus, coffee plants, tea and various hardwood trees. It is common in South Africa. The mycelium of the fungus is bioluminescent.

<i>Armillaria novae-zelandiae</i> Species of fungus

Armillaria novae-zelandiae is a species of mushroom-forming fungus in the family Physalacriaceae. This plant pathogen species is one of three Armillaria species that have been identified in New Zealand.

<i>Armillaria hinnulea</i> Species of fungus

Armillaria hinnulea is a species of mushroom in the family Physalacriaceae. This rare species is found only in Australia and New Zealand; in Australia, it is a secondary pathogen of wet sclerophyll forests, and causes a woody root rot. A 2008 phylogenetic study of Australian and New Zealand populations of A. hinnulea suggests that the species was introduced to New Zealand from Australia on two occasions, once relatively recently and another time much longer ago.

<i>Armillaria gallica</i> Species of fungus in the family Physalacriaceae

Armillaria gallica is a species of honey mushroom in the family Physalacriaceae of the order Agaricales. The species is a common and ecologically important wood-decay fungus that can live as a saprobe, or as an opportunistic parasite in weakened tree hosts to cause root or butt rot. It is found in temperate regions of Asia, North America, and Europe. The species forms fruit bodies singly or in groups in soil or rotting wood. The fungus has been inadvertently introduced to South Africa. Armillaria gallica has had a confusing taxonomy, due in part to historical difficulties encountered in distinguishing between similar Armillaria species. The fungus received international attention in the early 1990s when an individual colony living in a Michigan forest was reported to cover an area of 15 hectares, weigh at least 9.5 tonnes, and be 1,500 years old. This individual is popularly known as the "humongous fungus", and is a tourist attraction and inspiration for an annual mushroom-themed festival in Crystal Falls. Recent studies have revised the fungus's age to 2,500 years and its size to about 400 tonnes, four times the original estimate.

Armillaria fellea is a species of mushroom in the family Physalacriaceae. This species is found in Australia.

Armillaria fumosa is a species of mushroom in the family Physalacriaceae. This species is found in Australia.

Armillaria griseomellea is a species of mushroom in the family Physalacriaceae. This species is found in South America.

Armillaria montagnei is a species of agaric fungus in the family Physalacriaceae. This species is found in Australia, Europe, New Zealand, and South America.

Armillaria pallidula is a species of mushroom in the family Physalacriaceae. This species is found in Australia.

<i>Armillaria</i> root rot Fungal tree disease

Armillaria root rot is a fungal root rot caused by several different members of the genus Armillaria. The symptoms are variable depending on the host infected, ranging from stunted leaves to chlorotic needles and dieback of twigs and branches. However, all infected hosts display symptoms characteristic of being infected by a white rotting fungus. The most effective ways of management focus on limiting the spread of the fungus, planting resistant species, and removing infected material. This disease poses a threat to the lumber industry as well as affecting recreational areas.

<i>Armillaria ostoyae</i> Species of fungus

Armillaria ostoyae is a species of fungus (mushroom), pathogenic to trees, in the family Physalacriaceae. In the western United States, it is the most common variant of the group of species under the name Armillaria mellea. A. ostoyae is common on both hardwood and conifer wood in forests west of the Cascade Range in Oregon, United States. It has decurrent gills and the stipe has a ring. The mycelium invades the sapwood and is able to disseminate over great distances under the bark or between trees in the form of black rhizomorphs ("shoestrings"). In most areas of North America, Armillaria ostoyae can be separated from other species by its physical features: cream-brown colors, prominent cap scales, and a well-developed stem ring distinguish it from other Armillaria. Like several other Armillaria, the mycelium of Armillaria ostoyae can display bioluminescence, resulting in foxfire.

<i>Mycena cystidiosa</i> Species of fungus

Mycena cystidiosa is a species of mushroom in the family Mycenaceae. Described as new to science in 1964, it is known only from New Zealand and Australia. The fruit bodies have a broadly conical small white cap up to 12 mm (0.5 in) wide, with distantly spaced cream-coloured gills on the underside. The stipe is particularly long, up to 20 cm (8 in), with an abundant covering of white hairs at the base. The species is known for its abundant rhizomorphs—long, root-like extensions of mycelia.

Roy Watling, PhD., DSc, FRSE, F.I.Biol., C.Biol., FLS is a Scottish mycologist who has made significant contributions to the study of fungi both in the identification of new species and correct taxonomic placement, as well as in fungal ecology.

<i>Heterobasidion occidentale</i> Species of fungus

Heterobasidion occidentale is a tree root-rotting pathogenic fungus in the family Bondarzewiaceae. It is endemic in western North America west of the Rocky Mountains from Alaska to southern Mexico. While a natural agent of forest turnover, H. occidentale has become of increased concern due to forest management processes such as pre-commercial thinning, altered site density and species composition, and carbon sequestration. H. occidentale forms part of the genus that includes other species forming the important forest pest Heterobasidion annosumsensu lato that is spread across the Northern Hemisphere. H. occidentale is part of the S-type intersterility group differing from the other North American species, Heterobasidion irregulare.

References

  1. 1 2 3 4 5 Podger FD, Kile GA, Watling R, Fryer J (1978). "Spread and effects of Armillaria luteobubalina sp. nov. in an Australian Eucalyptus regnans plantation". Transactions of the British Mycological Society. 71 (1): 77–87. doi:10.1016/S0007-1536(78)80009-6.
  2. ↑ Pegler DN. (2000). "Taxonomy, nomenclature and description of Armillaria". In Fox RTV (ed.). Armillaria Root Rot: Biology and Control of Honey Fungus. Andover: Intercept. pp. 81–93. ISBN   978-1-898298-64-9.
  3. ↑ Watling R, Kile GA, Gregory NM (1982). "The genus Armillaria – nomenclature, typification, the identity of Armillaria mellea and species differentiation". Transactions of the British Mycological Society. 78 (2): 271–85. doi:10.1016/S0007-1536(82)80011-9.
  4. ↑ Hintikka V. (1973). "A note on the polarity of Armillaria mellea". Karstenia. 13: 32–39. doi: 10.29203/ka.1973.80 .
  5. ↑ Korhonen K. (1978). "Interfertility and clonal size in the Armillaria mellea complex". Karstenia. 18 (2): 31–42. doi: 10.29203/ka.1978.135 .
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  12. ↑ Maphosa L, Wingfield BD, Coetzee MP, Mwenje E, Wingfield MJ (2006). "Phylogenetic relationships among Armillaria species inferred from partial elongation factor 1-alpha DNA sequence data". Australasian Plant Pathology. 35 (5): 513–20. doi:10.1071/AP06056. S2CID   25188074.
  13. ↑ Dunne CP, Glen M, Tommerup IC, Shearer L, Jardy GE St J (2002). "Sequence variation in the rDNA ITS of Australian Armillaria species and intra-specific variation in A. luteobubalina". Australasian Plant Pathology. 31 (3): 241–51. doi:10.1071/AP02015. S2CID   36960183.
  14. 1 2 Grey P. (2005). Fungi Down Under: The Fungimap Guide to Australian Fungi. Melbourne: Royal Botanic Gardens. p. 23. ISBN   978-0-646-44674-5.
  15. 1 2 3 4 Bougher NL, Syme K (1998). Fungi of Southern Australia. Nedlands, WA: University of Western Australia Press. pp. 192–93. ISBN   978-1-875560-80-6.
  16. 1 2 3 Robinson RM, Williams MR, Smith RH (2003). "Incidence of Armillaria root disease in Karri regrowth forest is underestimated by surveys of aboveground symptoms". Australian Forestry. 66 (4): 273–78. doi:10.1080/00049158.2003.10674921. S2CID   55363942.
  17. ↑ Kile GA, Watling R (1983). "Armillaria species from south-eastern Australia". Transactions of the British Mycological Society. 81 (1): 129–40. doi:10.1016/S0007-1536(83)80212-5. ISSN   0007-1536.
  18. ↑ Shaw CG, MacKenzie M, Toes EH, Hood IA (1981). "Cultural characteristics and pathogenicity to Pinus radiata of Armillaria novae-zelandiae and A. limonea". New Zealand Journal of Forestry Science. 11: 65–70.
  19. 1 2 Fuhrer B. (2005). A Field Guide to Australian Fungi. Melbourne: Bloomings Books. pp. 29–31. ISBN   978-1-876473-51-8.
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  21. 1 2 Kile GA, Watling R (1981). "An expanded concept of Armillaria luteobubalina". Transactions of the British Mycological Society. 77 (1): 75–83. doi:10.1016/S0007-1536(81)80181-7.
  22. ↑ Smith L, Kile GA (1981). "Distribution and hosts of Armillaria root rot in Melbourne suburban gardens". Australasian Plant Pathology. 10 (3): 41–42. doi:10.1071/APP9810041. ISSN   0815-3191. S2CID   7757884.
  23. ↑ Kile GA, Watling R, Malajczuk N, Shearer BL (1983). "Occurrence of Armillaria luteobubalina Watling and Kile in Western Australia". Australasian Plant Pathology. 12 (2): 18–20. doi:10.1071/APP9830018. S2CID   46318969.
  24. 1 2 Pearce MH, Malanjczuk N (1989). "Stump colonization by Armillaria luteobubalina and other wood decay fungi in an age series of cut-over stumps in Karri (Eucalyptus diversicolor) regrowth forests in south-western Australia". New Phytologist. 115 (1): 129–38. doi: 10.1111/j.1469-8137.1990.tb00930.x . JSTOR   2557060.
  25. 1 2 Kile GA. (1983). "Armillaria root rot in eucalypt forests aggravated endemic disease". Pacific Science. 37 (4): 459–64. ISSN   0030-8870.
  26. ↑ Carnegie AJ. (2007). "Forest health condition in New South Wales, Australia, 1996–2005. II. Fungal damage recorded in eucalypt plantations during forest health surveys and their management". Australasian Plant Pathology. 36 (3): 225–39. doi:10.1071/AP07021. S2CID   23376623.
  27. 1 2 3 Kile GA. (1981). "Armillaria luteobubalina – a primary cause of decline and death of trees in mixed species eucalypt forests in central Victoria". Australian Forest Research. 11 (1): 63–77. ISSN   0004-914X.
  28. 1 2 Edgar JG, Kile GA, Almond CA (1976). "Tree decline and mortality in selectively logged eucalypt forests in central Victoria". Australian Forestry. 39 (4): 288–303. doi:10.1080/00049158.1976.10675656.
  29. ↑ Pearce MH, Malajczuk N, Kile GA (1986). "The occurrence and effects of Armillaria luteobubalina in the karri (Eucalyptus diversicolor F. Muell.) forests of Western Australia". Australian Forest Research. 16 (3): 243–59.
  30. ↑ Kellas JD, Kile GA, Jerrett RG, Morgan BJ (1987). "The occurrence and effects of Armillaria luteobubalina following partial cutting in mixed eucalypt stands in the Wombat Forest, Victoria". Australian Forest Research. 17 (3): 263–76.
  31. ↑ Falk SP, Parbery DG (1995). "Armillaria luteobubalina population-structure in horticultural plantings in Victoria, Australia". Mycological Research. 99 (2): 216–20. doi:10.1016/S0953-7562(09)80888-5.
  32. ↑ A forest stand may be defined as: "A group of trees occupying a given area and sufficiently uniform in species composition, age, structure, site quality, and condition so as to be distinguishable from the forest on adjoining areas." From "Glossary – SFMRP – Division of Forestry: Minnesota DNR". Minnesota Department of Natural Resources. Retrieved 2009-12-23.
  33. ↑ Myers BJ, Kile GA, Runnalls R (1983). "Evaluation of large scale aerial photography for identifying areas of Armillaria root rot in mixed species eucalypt forest". Australian Forestry. 46 (1): 39–42. doi:10.1080/00049158.1983.10674375. ISSN   0004-9158.
  34. ↑ Shearer BL, Crane CE, Fairman RG, Grant MJ (1997). "Occurrence of Armillaria luteobubalina and pathogen-mediated changes in coastal dune vegetation of south-western Australia". Australian Journal of Botany. 45 (5): 905–17. doi:10.1071/BT96084.
  35. ↑ Shearer BL, Tippett JT (1988). "Distribution and impact of Armillaria luteobubalina in the Eucalyptus marginata forest of south-western Australia". Australian Journal of Botany. 36 (4): 433–45. doi:10.1071/BT9880433.
  36. ↑ Shearer BL, Byrne A, Dillon M, Buehrig R (1997). "Occurrence of Armillaria luteobubalina and its impact on community diversity and structure in Eucalyptus wandoo woodland of southern Western Australia". Australian Journal of Botany. 45 (1): 151–65. doi:10.1071/BT95083.
  37. ↑ Kile GA. (1983). "Identification of genotypes and the clonal development of Armillaria luteobubalina Watling and Kile in eucalypt forests". Australian Journal of Botany. 31 (6): 657–71. doi:10.1071/BT9830657.
  38. 1 2 Pareek M, Allaway WG, Ashford AE (2006). "Armillaria luteobubalina mycelium develops air pores that conduct oxygen to rhizomorph clusters". Mycological Research. 110 (1): 38–51. doi:10.1016/j.mycres.2005.09.006. PMID   16376531.
  39. ↑ Morrison DJ. (2004). "Rhizomorph growth habit, saprophytic ability and virulence of 15 Armillaria species". Forest Pathology. 34 (1): 15–26. doi:10.1046/j.1439-0329.2003.00345.x.
  40. ↑ Pareek M, Cole L, Ashford AE (2001). "Variations in structure of aerial and submerged rhizomorphs of Armillaria luteobubalina indicate that they may be organs of absorption". Mycological Research. 105 (11): 1377–87. doi:10.1017/S0953756201004622.
  41. ↑ Robinson RM. (2003). "Short-term impact of thinning and fertilizer application on Armillaria root disease in regrowth karri (Eucalyptus diversicolor F. Muell.) in Western Australia". Forest Ecology and Management. 176 (1–3): 417–26. doi:10.1016/S0378-1127(02)00231-1.
  42. 1 2 Robinson RM, Smith RH (2001). "Fumigation of regrowth karri stumps with metham-sodium to control Armillaria luteobubalina" (PDF). Australian Forestry. 64 (4): 209–15. doi:10.1080/00049158.2001.10676190. S2CID   85224336. Archived from the original (PDF) on April 27, 2013.
  43. ↑ Schütt P. (1985). "Control of root and butt rots: limits and prospects". European Journal of Forest Pathology. 15 (5–6): 357–63. doi:10.1111/j.1439-0329.1985.tb01112.x.
  44. ↑ Pearce MH, Malajczuk N (1990). "Inoculation of Eucalyptus diversicolor thinning stumps with wood decay fungi for control of Armillaria luteobubalina". Mycological Research. 94 (1): 32–37. doi:10.1016/S0953-7562(09)81261-6. ISSN   0953-7562.

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