Armillaria luteobubalina
Encyclopedia
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 (0.590551181102362 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 spore
s 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 hypha
e.
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
.
of Eucalyptus regnans
near Traralgon, Victoria
. The plantation, established in 1963, consisted largely of trees with a mean height of about 25 m (82 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. For over a 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. which led to great confusion among taxonomists and plant pathologists alike. In 1973, Veikko Hintikka reported a technique to distinguish between Armillaria species by growing them together as single spore
isolates on petri dish
es and observing changes in the morphology
of the cultures. 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.
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.
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
, a species known from a single specimen collected in São Paulo
, Brazil. 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. Based on analysis of pectic enzymes, A. luteobubalina is closely related to A. limonea
, a species found in New Zealand; this result corroborates phylogenetic analyses reported in 2003 and 2006. 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.
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. 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 (0.590551181102362 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. Although it has a hot-bitter taste, Armillaria luteobubalina is edible
, and cooking removes the bitterness.
is white when fresh, but becomes more cream-coloured when dry. The smooth spore
s 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 connection
s 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.
is restricted to gully
habitats. A. fumosa
is a rarer species found only in poorly drained or seasonally wet locations. 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. The morphology of the vegetative structures of A. limonea
is distinctly different than A. luteobubalina, and can be used to distinguish the two species. 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. A. luteobubalina is the only Armillaria species which occurs in Western Australia. 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.
through eastern New South Wales
and across Victoria
into southeastern South Australia
. It also occurs in Tasmania
and southwestern Western Australia
. Those of the Karri forest
s (consisting largely of the species E. diversicolor) of the southwest have paler and yellower caps than those in the Jarrah forest
s (which contain predominantly Eucalyptus marginata) further north. 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. Abundant in woodlands, it can invade gardens and orchards, where it can attack many woody plants. The honey fungus infected and killed many plants near Tuart trees (Eucalyptus gomphocephala
) which had been cut down near Kings Park
in suburban Perth. Armillaria luteobubalina is commonly found in eucalyptus
forests in Australia, and is thought to be the most pathogenic and most widespread Armillaria species in the major western Australian forest types. The mushroom has also been reported from southern South America, in Argentina and Chile. 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".
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.
on the Dorrigo Plateau
. 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. 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. 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 25–30 year old karri regrowth forests in western Australia showed an average of 40–45% incidence of infection.
that remain after an area has been logged
. Armillaria luteobubalina can persist on these stumps, using them as a source of food for up to 25 or more years. 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. In individual forest stands, fungal infection is usually found in discrete disease patches separated by stands of healthy trees—a discontinuous distribution. Large-scale aerial photography
can be used to identify regions of forest infected by the species. The species also causes damage to trees and bushes in coastal dune
woodlands, shrubland
, and heath
communities. 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
. It has also infected scattered populations of Wandoo (E. wandoo
). The fungus has also been reported to infect Nothofagus
species in Argentina, and Pinus radiata in Chile.
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. 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
. 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 monopodial
ly (where lateral branches grow from a main stem). Although the structure of A. luteobubalina rhizomorphs is specialised for spread in potentially anaerobic conditions, the soil mycelium is adaptive, and able to amplify the absorptive surface of peripheral hyphae in response to the presence of nutrient-rich soil.
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. 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.
Common name
A common name of a taxon or organism is a name in general use within a community; it is often contrasted with the scientific name for the same organism...
known as the Australian honey fungus, is a species of mushroom
Mushroom
A mushroom is the fleshy, spore-bearing fruiting body of a fungus, typically produced above ground on soil or on its food source. The standard for the name "mushroom" is the cultivated white button mushroom, Agaricus bisporus; hence the word "mushroom" is most often applied to those fungi that...
in the family Physalacriaceae
Physalacriaceae
Physalacriaceae are a family of fungi in the order Agaricales. Species in the genus have a widespread distribution, but most are found in the tropics, particularly in South-East Asia and Australasia. Molecular studies suggested that Physalacria, formerly the sole genus in this family, is related to...
. Widely distributed in southern Australia, the fungus is responsible for a disease known as Armillaria root rot, a primary cause of Eucalyptus
Eucalyptus
Eucalyptus is a diverse genus of flowering trees in the myrtle family, Myrtaceae. Members of the genus dominate the tree flora of Australia...
tree death and forest dieback
Forest dieback
Forest dieback is a condition in trees or woody plants in which peripheral parts are killed, either by parasites or due to conditions like acid rain and drought....
. 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
Basidiocarp
In fungi, a basidiocarp, basidiome or basidioma , is the sporocarp of a basidiomycete, the multicellular structure on which the spore-producing hymenium is borne. Basidiocarps are characteristic of the hymenomycetes; rusts and smuts do not produce such structures...
have cream- to tan-coloured caps
Pileus (mycology)
The pileus is the technical name for the cap, or cap-like part, of a basidiocarp or ascocarp that supports a spore-bearing surface, the hymenium. The hymenium may consist of lamellae, tubes, or teeth, on the underside of the pileus...
that grow up to 10 cm (4 in) in diameter and stems
Stipe (mycology)
thumb|150px|right|Diagram of a [[basidiomycete]] stipe with an [[annulus |annulus]] and [[volva |volva]]In mycology a stipe refers to the stem or stalk-like feature supporting the cap of a mushroom. Like all tissues of the mushroom other than the hymenium, the stipe is composed of sterile hyphal...
that measure up to 20 cm (8 in) long by 1.5 cm (0.590551181102362 in) thick. The fruit bodies, which appear at the base of infected trees and other woody plants in autumn (March–April), are edible
Edible mushroom
Edible mushrooms are the fleshy and edible fruiting bodies of several species of fungi. Mushrooms belong to the macrofungi, because their fruiting structures are large enough to be seen with the naked eye. They can appear either below ground or above ground where they may be picked by hand...
, but require cooking to remove the bitter taste. The fungus is dispersed through spore
Spore
In biology, a spore is a reproductive structure that is adapted for dispersal and surviving for extended periods of time in unfavorable conditions. Spores form part of the life cycles of many bacteria, plants, algae, fungi and some protozoa. According to scientist Dr...
s produced on gills on the underside of the caps, and also by growing vegetatively
Vegetative reproduction
Vegetative reproduction is a form of asexual reproduction in plants. It is a process by which new individuals arise without production of seeds or spores...
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
Oxygen
Oxygen is the element with atomic number 8 and represented by the symbol O. Its name derives from the Greek roots ὀξύς and -γενής , because at the time of naming, it was mistakenly thought that all acids required oxygen in their composition...
through rhizomorphs—rootlike structures made of dense masses of hypha
Hypha
A hypha is a long, branching filamentous structure of a fungus, and also of unrelated Actinobacteria. In most fungi, hyphae are the main mode of vegetative growth, and are collectively called a mycelium; yeasts are unicellular fungi that do not grow as hyphae.-Structure:A hypha consists of one or...
e.
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
Logging
Logging is the cutting, skidding, on-site processing, and loading of trees or logs onto trucks.In forestry, the term logging is sometimes used in a narrow sense concerning the logistics of moving wood from the stump to somewhere outside the forest, usually a sawmill or a lumber yard...
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
Armillaria montagnei
Armillaria montagnei is a species of mushroom in the Physalacriaceae family. This species is found in Australia, Europe, New Zealand, and South America....
and that both of these species are in turn closely related to the Brazilian species A. paulensis
Armillaria paulensis
Armillaria paulensis is a species of mushroom in the Physalacriaceae family. This species is found in South America....
. The distribution of A. luteobubalina suggests that it is an ancient species that originated before the separation of the precursor supercontinent Gondwana
Gondwana
In paleogeography, Gondwana , originally Gondwanaland, was the southernmost of two supercontinents that later became parts of the Pangaea supercontinent. It existed from approximately 510 to 180 million years ago . Gondwana is believed to have sutured between ca. 570 and 510 Mya,...
.
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 plantationPlantation
A plantation is a long artificially established forest, farm or estate, where crops are grown for sale, often in distant markets rather than for local on-site consumption...
of Eucalyptus regnans
Eucalyptus regnans
Eucalyptus regnans, known variously by the common names Mountain Ash, Victorian Ash, Swamp Gum, Tasmanian Oak or Stringy Gum, is a species of Eucalyptus native to southeastern Australia, in Tasmania and Victoria...
near Traralgon, Victoria
Traralgon, Victoria
Traralgon is a regional city located in the Latrobe Valley in the Gippsland region of Victoria, Australia. Traralgon is a city within the City of Latrobe....
. The plantation, established in 1963, consisted largely of trees with a mean height of about 25 m (82 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
Armillaria mellea
Armillaria mellea is a plant pathogen and a species of Honey fungus. It causes Armillaria root rot in many plant species. The mushrooms are edible but some people may be intolerant to them. The fungus produces mushrooms around the base of trees it has infected...
and A. elegans. Further study over the next few years showed that the fungus spread by the growth of underground mycelia
Mycelium
thumb|right|Fungal myceliaMycelium is the vegetative part of a fungus, consisting of a mass of branching, thread-like hyphae. The mass of hyphae is sometimes called shiro, especially within the fairy ring fungi. Fungal colonies composed of mycelia are found in soil and on or within many other...
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. For over a 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. which led to great confusion among taxonomists and plant pathologists alike. In 1973, Veikko Hintikka reported a technique to distinguish between Armillaria species by growing them together as single spore
Spore
In biology, a spore is a reproductive structure that is adapted for dispersal and surviving for extended periods of time in unfavorable conditions. Spores form part of the life cycles of many bacteria, plants, algae, fungi and some protozoa. According to scientist Dr...
isolates on petri dish
Petri dish
A Petri dish is a shallow glass or plastic cylindrical lidded dish that biologists use to culture cells or small moss plants. It was named after German bacteriologist Julius Richard Petri, who invented it when working as an assistant to Robert Koch...
es and observing changes in the morphology
Morphology (biology)
In biology, morphology is a branch of bioscience dealing with the study of the form and structure of organisms and their specific structural features....
of the cultures. Using similar techniques, mycologists eventually determined that the Armillaria mellea species complex
Species complex
A species complex is a group of closely related species, where the exact demarcation between species is often unclear or cryptic owing to their recent and usually still incomplete reproductive isolation. Ring species, superspecies and cryptic species complex are example of species complex...
in Europe and North America in fact consisted of five and ten distinct "biological species", respectively.
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
Armillaria limonea
Armillaria limonea is a species of mushroom in the Physalacriaceae family. This plant pathogenic species is one of three Armillaria that have been identified in New Zealand ....
and A. novae-zelandiae
Armillaria novae-zelandiae
Armillaria novae-zelandiae is a species of mushroom in the Physalacriaceae family. This plant pathogen species is one of three Armillaria species that have been identified in New Zealand ....
and found sufficient differences between them to warrant designating the species as new. Its specific epithet is derived from the Latin
Latin
Latin is an Italic language originally spoken in Latium and Ancient Rome. It, along with most European languages, is a descendant of the ancient Proto-Indo-European language. Although it is considered a dead language, a number of scholars and members of the Christian clergy speak it fluently, and...
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.
A phylogenetic study of South American Armillaria species concluded that A. luteobubalina is in a lineage that includes A. montagnei
Armillaria montagnei
Armillaria montagnei is a species of mushroom in the Physalacriaceae family. This species is found in Australia, Europe, New Zealand, and South America....
, and these are sister
Cladistics
Cladistics is a method of classifying species of organisms into groups called clades, which consist of an ancestor organism and all its descendants . For example, birds, dinosaurs, crocodiles, and all descendants of their most recent common ancestor form a clade...
to a lineage containing A. paulensis
Armillaria paulensis
Armillaria paulensis is a species of mushroom in the Physalacriaceae family. This species is found in South America....
, a species known from a single specimen collected in São Paulo
São Paulo
São Paulo is the largest city in Brazil, the largest city in the southern hemisphere and South America, and the world's seventh largest city by population. The metropolis is anchor to the São Paulo metropolitan area, ranked as the second-most populous metropolitan area in the Americas and among...
, Brazil. 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. Based on analysis of pectic enzymes, A. luteobubalina is closely related to A. limonea
Armillaria limonea
Armillaria limonea is a species of mushroom in the Physalacriaceae family. This plant pathogenic species is one of three Armillaria that have been identified in New Zealand ....
, a species found in New Zealand; this result corroborates phylogenetic analyses reported in 2003 and 2006. 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.
Description
Up to 10 cm (4 in) in diameter, the capPileus (mycology)
The pileus is the technical name for the cap, or cap-like part, of a basidiocarp or ascocarp that supports a spore-bearing surface, the hymenium. The hymenium may consist of lamellae, tubes, or teeth, on the underside of the pileus...
is convex to flattened in shape with a central umbo
Umbo (mycology)
thumb|right|[[Cantharellula umbonata]] has an umbo.thumb|right|The cap of [[Psilocybe makarorae]] is acutely papillate.An umbo is a raised area in the center of a mushroom cap. Caps that possess this feature are called umbonate. Umbos that are sharply pointed are called acute, while those that are...
(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. The stem
Stipe (mycology)
thumb|150px|right|Diagram of a [[basidiomycete]] stipe with an [[annulus |annulus]] and [[volva |volva]]In mycology a stipe refers to the stem or stalk-like feature supporting the cap of a mushroom. Like all tissues of the mushroom other than the hymenium, the stipe is composed of sterile hyphal...
is central (that is, it joins the cap in the centre) and is up to 20 cm (8 in) long by 1.5 cm (0.590551181102362 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
Annulus (mycology)
An annulus is the ring like structure sometimes found on the stipe of some species of mushrooms. The annulus represents the remaining part of the partial veil, after it has ruptured to expose the gills or other spore-producing surface. An annulus may be thick and membranous, or it may be cobweb-like...
which may develop irregular, jagged edges with time. The flesh
Trama (mycology)
In mycology trama is a term for the inner, fleshy portion of a mushroom's basidiocarp, or fruit body. It is distinct from the outer layer of tissue, known as the pileipellis or cuticle, and from the spore-bearing tissue layer known as the hymenium....
is white, and in the stem has a woolly or stringy consistency. Although it has a hot-bitter taste, Armillaria luteobubalina is edible
Edible mushroom
Edible mushrooms are the fleshy and edible fruiting bodies of several species of fungi. Mushrooms belong to the macrofungi, because their fruiting structures are large enough to be seen with the naked eye. They can appear either below ground or above ground where they may be picked by hand...
, and cooking removes the bitterness.
Microscopic characteristics
The spore printSpore print
thumb|300px|right|Making a spore print of the mushroom Volvariella volvacea shown in composite: mushroom cap laid on white and dark paper; cap removed after 24 hours showing pinkish-tan spore print...
is white when fresh, but becomes more cream-coloured when dry. The smooth spore
Spore
In biology, a spore is a reproductive structure that is adapted for dispersal and surviving for extended periods of time in unfavorable conditions. Spores form part of the life cycles of many bacteria, plants, algae, fungi and some protozoa. According to scientist Dr...
s are oval to ellipsoid, hyaline
Hyaline
The term hyaline denotes a substance with a glass-like appearance.-Histopathology:In histopathological medical usage, a hyaline substance appears glassy and pink after being stained with haematoxylin and eosin — usually it is an acellular, proteinaceous material...
(translucent), non-amyloid
Amyloid
Amyloids are insoluble fibrous protein aggregates sharing specific structural traits. Abnormal accumulation of amyloid in organs may lead to amyloidosis, and may play a role in various neurodegenerative diseases.-Definition:...
(meaning they do not absorb iodine
Iodine
Iodine is a chemical element with the symbol I and atomic number 53. The name is pronounced , , or . The name is from the , meaning violet or purple, due to the color of elemental iodine vapor....
from Melzer's reagent
Melzer's Reagent
Melzer's reagent is a chemical reagent used by mycologists to assist with the identification of fungi.-Composition:...
), and typically measure 6.5–7.5 by 4.5–5.5 μm
Micrometre
A micrometer , is by definition 1×10-6 of a meter .In plain English, it means one-millionth of a meter . Its unit symbol in the International System of Units is μm...
. The basidia (spore-bearing cells) are thin-walled, hyaline, and lack clamp connection
Clamp connection
A clamp connection is a structure formed by growing hyphal cells of certain fungi. It is created to ensure each septum, or segment of hypha separated by crossed walls, receives a set of differing nuclei, which are obtained through mating of hyphae of differing sexual types...
s 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.
Similar species
Five other Armillaria species are found in Australia. Within the range of A. luteobubalina, A. hinnuleaArmillaria hinnulea
Armillaria hinnulea is a species of mushroom in the Physalacriaceae family. 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...
is restricted to gully
Gully
A gully is a landform created by running water, eroding sharply into soil, typically on a hillside. Gullies resemble large ditches or small valleys, but are metres to tens of metres in depth and width...
habitats. A. fumosa
Armillaria fumosa
Armillaria fumosa is a species of mushroom in the Physalacriaceae family. This species is found in Australia....
is a rarer species found only in poorly drained or seasonally wet locations. 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. The morphology of the vegetative structures of A. limonea
Armillaria limonea
Armillaria limonea is a species of mushroom in the Physalacriaceae family. This plant pathogenic species is one of three Armillaria that have been identified in New Zealand ....
is distinctly different than A. luteobubalina, and can be used to distinguish the two species. 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. A. luteobubalina is the only Armillaria species which occurs in Western Australia. 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
DNA
Deoxyribonucleic acid is a nucleic acid that contains the genetic instructions used in the development and functioning of all known living organisms . The DNA segments that carry this genetic information are called genes, but other DNA sequences have structural purposes, or are involved in...
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.
Habitat and distribution
Armillaria luteobubalina has been recorded in southeastern Australia, from the southeastern corner of QueenslandQueensland
Queensland is a state of Australia, occupying the north-eastern section of the mainland continent. It is bordered by the Northern Territory, South Australia and New South Wales to the west, south-west and south respectively. To the east, Queensland is bordered by the Coral Sea and Pacific Ocean...
through eastern New South Wales
New South Wales
New South Wales is a state of :Australia, located in the east of the country. It is bordered by Queensland, Victoria and South Australia to the north, south and west respectively. To the east, the state is bordered by the Tasman Sea, which forms part of the Pacific Ocean. New South Wales...
and across Victoria
Victoria (Australia)
Victoria is the second most populous state in Australia. Geographically the smallest mainland state, Victoria is bordered by New South Wales, South Australia, and Tasmania on Boundary Islet to the north, west and south respectively....
into southeastern South Australia
South Australia
South Australia is a state of Australia in the southern central part of the country. It covers some of the most arid parts of the continent; with a total land area of , it is the fourth largest of Australia's six states and two territories.South Australia shares borders with all of the mainland...
. It also occurs in Tasmania
Tasmania
Tasmania is an Australian island and state. It is south of the continent, separated by Bass Strait. The state includes the island of Tasmania—the 26th largest island in the world—and the surrounding islands. The state has a population of 507,626 , of whom almost half reside in the greater Hobart...
and southwestern Western Australia
Western Australia
Western Australia is a state of Australia, occupying the entire western third of the Australian continent. It is bounded by the Indian Ocean to the north and west, the Great Australian Bight and Indian Ocean to the south, the Northern Territory to the north-east and South Australia to the south-east...
. Those of the Karri forest
Karri forest
Karri forest is tall open forest of Eucalyptus diversicolor , one of the tallest hardwoods in the world.It occurs only in the south-west corner of the Southwest Botanical Province of Western Australia, in the Warren biogeographic region...
s (consisting largely of the species E. diversicolor) of the southwest have paler and yellower caps than those in the Jarrah forest
Jarrah forest
Jarrah forest is tall open forest in which the dominant overstory tree is Eucalyptus marginata . The ecosystem occurs only in the Southwest Botanical Province of Western Australia...
s (which contain predominantly Eucalyptus marginata) further north. 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. Abundant in woodlands, it can invade gardens and orchards, where it can attack many woody plants. The honey fungus infected and killed many plants near Tuart trees (Eucalyptus gomphocephala
Eucalyptus gomphocephala
Eucalyptus gomphocephala is a species of tree, also known as Tuart, in the genus Eucalyptus. Native to the southwest of Western Australia the tree grows to over 35m tall. As a durable hardwood the timber is sought after for scantlings, structural timber, the construction of railway carriages, and...
) which had been cut down near Kings Park
Kings Park, Western Australia
Kings Park is a park located on the western edge of Perth, Western Australia central business district. The park is a mixture of grassed parkland, botanical gardens and natural bushland on Mount Eliza with two thirds of the grounds conserved as native bushland. With panoramic views of the Swan...
in suburban Perth. Armillaria luteobubalina is commonly found in eucalyptus
Eucalyptus
Eucalyptus is a diverse genus of flowering trees in the myrtle family, Myrtaceae. Members of the genus dominate the tree flora of Australia...
forests in Australia, and is thought to be the most pathogenic and most widespread Armillaria species in the major western Australian forest types. The mushroom has also been reported from southern South America, in Argentina and Chile. 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
Gondwana
In paleogeography, Gondwana , originally Gondwanaland, was the southernmost of two supercontinents that later became parts of the Pangaea supercontinent. It existed from approximately 510 to 180 million years ago . Gondwana is believed to have sutured between ca. 570 and 510 Mya,...
. 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".
Root rot
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 celluloseCellulose
Cellulose is an organic compound with the formula , a polysaccharide consisting of a linear chain of several hundred to over ten thousand β linked D-glucose units....
and lignin
Lignin
Lignin or lignen is a complex chemical compound most commonly derived from wood, and an integral part of the secondary cell walls of plants and some algae. The term was introduced in 1819 by de Candolle and is derived from the Latin word lignum, meaning wood...
of the sapwood are both broken down, leaving the wood stringy. The bark
Bark
Bark is the outermost layers of stems and roots of woody plants. Plants with bark include trees, woody vines and shrubs. Bark refers to all the tissues outside of the vascular cambium and is a nontechnical term. It overlays the wood and consists of the inner bark and the outer bark. The inner...
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
Crown (botany)
The crown of a plant refers to the totality of the plant's aboveground parts, including stems, leaves, and reproductive structures. A plant canopy consists of one or more plant crowns growing in a given area....
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.
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. 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 nitensEucalyptus nitens
Eucalyptus nitens, commonly known as Shining Gum, is a Eucalypt species native to Victoria and eastern New South Wales, Australia. It grows in wet forests and rainforest margins on fertile soils in cool high-rainfall areas.-Description:...
on the Dorrigo Plateau
Dorrigo Plateau
Dorrigo Plateau is a plateau in northern New South Wales, which forms part of the Great Dividing Range. The plateau is sometimes referred to as the Dorrigo & Guy Fawkes Plateau....
. 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. 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. 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 25–30 year old karri regrowth forests in western Australia showed an average of 40–45% incidence of infection.
Disease spread
Several studies have shown that the spread of Armillaria root rot in eucalypt forests is associated with infected stumpsTree stump
After a tree has been cut and felled, the stump or tree stump is usually a small remaining portion of the trunk with the roots still in the ground. Stumps may show the age-defining rings of a tree. The study of these rings is known as dendrochronology....
that remain after an area has been logged
Logging
Logging is the cutting, skidding, on-site processing, and loading of trees or logs onto trucks.In forestry, the term logging is sometimes used in a narrow sense concerning the logistics of moving wood from the stump to somewhere outside the forest, usually a sawmill or a lumber yard...
. Armillaria luteobubalina can persist on these stumps, using them as a source of food for up to 25 or more years. In one case reported in Ovens, Victoria
Ovens, Victoria
Ovens is a small town in north east Victoria, Australia located at the junction of the Ovens River and Happy Valley Creek. At the 2006 census, Ovens and the surrounding area had a population of 130. It is south east of Myrtleford heading towards Bright and is the home of the Happy Valley Hotel...
, the disease was spread to blueberry
Blueberry
Blueberries are flowering plants of the genus Vaccinium with dark-blue berries and are perennial...
plants (Vaccinium species) via buried fragments of infected Eucalyptus that remained following preparation of the previously forested site for planting. In individual forest stands, fungal infection is usually found in discrete disease patches separated by stands of healthy trees—a discontinuous distribution. Large-scale aerial photography
Aerial photography
Aerial photography is the taking of photographs of the ground from an elevated position. The term usually refers to images in which the camera is not supported by a ground-based structure. Cameras may be hand held or mounted, and photographs may be taken by a photographer, triggered remotely or...
can be used to identify regions of forest infected by the species. The species also causes damage to trees and bushes in coastal dune
Dune
In physical geography, a dune is a hill of sand built by wind. Dunes occur in different forms and sizes, formed by interaction with the wind. Most kinds of dunes are longer on the windward side where the sand is pushed up the dune and have a shorter "slip face" in the lee of the wind...
woodlands, shrubland
Shrubland
Shrubland, scrubland, scrub or brush is a plant community characterized by vegetation dominated by shrubs, often also including grasses, herbs, and geophytes. Shrubland may either occur naturally or be the result of human activity...
, and heath
Heath (habitat)
A heath or heathland is a dwarf-shrub habitat found on mainly low quality acidic soils, characterised by open, low growing woody vegetation, often dominated by plants of the Ericaceae. There are some clear differences between heath and moorland...
communities. 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
Banksia grandis
Banksia grandis, commonly known as Bull Banksia, Giant Banksia or Mangite, is a common and distinctive tree in South West Western Australia....
), Marri (E. calophylla), Lasiopetalum floribundum
Lasiopetalum floribundum
Lasiopetalum floribundum, commonly known as the free flowering lasiopetalum, is a species of shrub which is endemic to Western Australia. The plant was first described by George Bentham in 1863....
, and Acacia saligna
Acacia saligna
Acacia saligna, commonly known by various names including coojong, golden wreath wattle, orange wattle, blue-leafed wattle, Western Australian golden wattle, and, in Africa, Port Jackson willow, is a small tree in the family Fabaceae...
. It has also infected scattered populations of Wandoo (E. wandoo
Eucalyptus wandoo
Eucalyptus wandoo is a medium-sized tree widely distributed in southwest Western Australia.-Description:It grows as a small to medium-sized tree up to 25 metres in height. It has smooth bark, often in mottled patches of white, light grey, light brown light yellow and pink...
). The fungus has also been reported to infect Nothofagus
Nothofagus
Nothofagus, also known as the southern beeches, is a genus of 35 species of trees and shrubs native to the temperate oceanic to tropical Southern Hemisphere in southern South America and Australasia...
species in Argentina, and Pinus radiata in Chile.
Microbiological culture
A microbiological culture, or microbial culture, is a method of multiplying microbial organisms by letting them reproduce in predetermined culture media under controlled laboratory conditions. Microbial cultures are used to determine the type of organism, its abundance in the sample being tested,...
, the mycelium
Mycelium
thumb|right|Fungal myceliaMycelium is the vegetative part of a fungus, consisting of a mass of branching, thread-like hyphae. The mass of hyphae is sometimes called shiro, especially within the fairy ring fungi. Fungal colonies composed of mycelia are found in soil and on or within many other...
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
Diffusion
Molecular diffusion, often called simply diffusion, is the thermal motion of all particles at temperatures above absolute zero. The rate of this movement is a function of temperature, viscosity of the fluid and the size of the particles...
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
Hypoxia (environmental)
Hypoxia, or oxygen depletion, is a phenomenon that occurs in aquatic environments as dissolved oxygen becomes reduced in concentration to a point where it becomes detrimental to aquatic organisms living in the system...
. 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 monopodial
Monopodial
Vascular plants with monopodial growth habits grow upward from a single point. They add leaves to the apex each year and the stem grows longer accordingly...
ly (where lateral branches grow from a main stem). Although the structure of A. luteobubalina rhizomorphs is specialised for spread in potentially anaerobic conditions, the soil mycelium is adaptive, and able to amplify the absorptive surface of peripheral hyphae in response to the presence of nutrient-rich soil.
Control
Methods for controlling the spread of Armillaria root rot include: physical removal of infected trees, stumps and large roots; fumigation of soil around infected hosts; and injection of fumigants directly into infected hosts. 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. Biological controlBiological pest control
Biological control of pests in agriculture is a method of controlling pests that relies on predation, parasitism, herbivory, or other natural mechanisms...
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
Wood-decay fungus
A wood-decay fungus is a variety of fungus that digests moist wood, causing it to rot. Some wood-decay fungi attack dead wood, such as brown rot, and some, such as Armillaria , are parasitic and colonize living trees. Fungi that not only grow on wood but actually cause it to decay, are called...
Coriolus versicolor, Stereum hirsutum
Stereum hirsutum
Stereum hirsutum is a plant pathogen. S. hirsutum is in turn parasitised by certain other species such as the fungus Tremella aurantia. Substrates for S. hirsutum include dead limbs and trunks of both hardwoods and conifers.-References:...
and Xylaria hypoxylon
Xylaria hypoxylon
Xylaria hypoxylon is an inedible species of fungus in the genus Xylaria. It is known by a variety of common names, such as the candlestick fungus, the candlesnuff fungus, carbon antlers, or the stag's horn fungus. The fruit bodies, characterized by erect, elongated black branches with whitened...
; all three fungi significantly reduced infection by A. luteobubalinea. 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.