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First Record of Amanita muscaria in Western Australia

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  • Department of Biodiversity, Conservation and Attractions

Abstract and Figures

Amanita muscaria is a Northern Hemisphere mycorrhizal fungus that has become well established in eastern Australia; associated with amenity plantings of exotic conifers and hardwoods and also pine plantations. In regions of Tasmania and Victoria, A. muscaria has also been recorded in temperate rainforest dominated by Nothofagus cunninghamii. However, A. muscaria has not previously been reported from Western Australia; this paper confirms the first record. Records of its association with eucalypts in eastern Australia and other regions of the world are briefly reviewed and discussed with respect to the possibility of it spreading to eucalypt forests in the south-west.
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© 2010 Australasian Mycological Society Inc.
First Record of Amanita muscaria in Western Australia
Richard Robinson
Science Division, Department of Environment and Conservation, Locked Bag 2, Manjimup, WA 6258. Email richard.robinson@dec.wa.gov.au.
Abstract
Amanita muscaria is a Northern Hemisphere mycorrhizal fungus that has become well established in
eastern Australia; associated with amenity plantings of exotic conifers and hardwoods and also pine
plantations. In regions of Tasmania and Victoria, A. muscaria has also been recorded in temperate
rainforest dominated by Nothofagus cunninghamii. However, A. muscaria has not previously been
reported from Western Australia; this paper conrms the rst record. Records of its association with
eucalypts in eastern Australia and other regions of the world are briey reviewed and discussed with
respect to the possibility of it spreading to eucalypt forests in the south-west.
Key words: Ectomycorrhiza, Amanita muscaria, Western Australia, plant host associations.
Introduction
Amanita muscaria occurs naturally in the Northern
Hemisphere as a mycorrhizal fungus associated with
various conifers and hardwoods including pine, chestnut
and birch. Following the establishment of the Pinus
radiata plantation industry in Australia, A. muscaria
has also become common in pine plantations and
under exotic plantings of both conifer and hardwood
trees in eastern Australia (see Grey & Grey 2005). In
the early 1990s, A. muscaria, along with the northern
hemisphere bolete Chalciporus piperatus, was found to
be invading myrtle (Nothofagus cunninghamii) forest in
northwestern Tasmania (Fuhrer & Robinson 1992). It has
since been collected in temperate rainforest at several
locations in Victoria (B. Fuhrer pers. comm.; T. May pers.
comm.; Dunk 2002), and in mixed wet sclerophyll forest
in southern Tasmania (D. Ratkowsky pers. comm.)
and there is concern that it may become established
and compete with or replace native mycorrhizal fungi
associated with N. cunninghamii trees.
A. muscaria has also become established in New
Zealand. It has a wide distribution within pine and
Douglas-r plantations and under ornamental plantings
of Nothofagus spp., Betula pendula, Fagus silvatica and
Quercus robur trees in both the North and South Islands
(Ridley 1991). In the early 1960s it was reported fruiting
in natural Nothofagus forest in the Nelson district of the
South Island (Stevenson 1962) and more recently it was
shown to have a much broader range within Nothofagus
forests; being reported throughout the northern half of
the South Island and within the central region of the
North Island (Johnson & Buchannan 1998).
Fig. 1 Sporophores of Amanita muscaria from Manjimup Western Australia.
Australasian Mycologist (2010) 29, 4–6
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Conversely, in other regions of the world, including New
Zealand, Spain and Portugal, A. muscaria has been
found associated with exotic plantings of eucalypts
(Ridley 1991: Castro 1998 and others cited in May &
Wood 1997).
Despite being common in eastern Australia A. muscaria
has not previously been recorded in Western Australia
(WA). Trial plantings of Pinus radiata began in the late
1890s in WA and the plantation industry became well
established during the 1950s (Forests Department 1969).
The most common mycorrhizal species associated with
P. radiata trees in WA include Rhizopogon luteus, R,
roseus, Suillus luteus and S. granulosus (Kessell 1927;
Bougher & Syme 1998, Dunstan et al. 1998). In June
2009, six sporophores of A. muscaria were found in a
rural garden in the southwestern town of Manjimup,
under a birch (B. pendula) tree.
Materials and methods
Sporophores were photographed in situ, and a collection
consisting of four specimens was brought back to the
laboratory for formal identication. Morphological details
of the fresh specimens were compared with descriptions
published for both Australian (Grgurinovic 1997) and New
Zealand (Ridley 1991) collections of A. muscaria. The
sporophores were then air dried at 35º C and processed
for lodging at the Western Australian Herbarium (PERTH).
Microscopic examination of dried material was undertaken
using bright eld microscopy.
Results
Macroscopic and microscopic details of the Manjimup
collection of A. muscaria agree with descriptions by
Grgrinovic (1997) for South Australian collections held
in the State Herbarium in Adelaide (AD) and Ridley
(1991) for New Zealand collections held at Auckland
(PDD). The cap is 55–95 mm diameter, orange-red,
fading to yellow at the margin with creamy-white wart-
like universal veil fragments on the surface, the gills
are creamy-white, and the stipe is white with a torn
membranous veil and a bulbous tapering base (Fig.
1). The spores are short ellipsoid, inamyloid, hylaine,
8–10.5 × 7–9.5 μm; basidia are 4-spored, clavate,
46–55 × 10–12 μm and there are occasional clamp
connections (Fig. 2). All macrosopic and microscopic
characters are typical for A. muscaria.
Collection details. Western Australia: Manjimup.
Under Betula pendula, 3 June 2009, B. & J. Markotis
(RR1104WA, PERTH 06672345)
Discussion
A. muscaria is a well known conspicuous fungus.
Although it is a Fungimap target species (Grey & Grey
2005) and WA has an active community-based fungal
studies group this is the rst record of A. muscaria in
WA. Pine plantations in WA were established using
seed and in the 1920s P. radiata seedlings were actively
inoculated with R. luteolus using spores and soil from
established nurseries (Kessell 1927; Kessell & Stoat
1938). It is not clear how R. luteolus became established
in nurseries, but possibly through the introduction of
spores with seed (Kessell 1927). A. muscaria has not
been actively used to inoculate trees in WA, unlike
plantations in eastern Australia (Sawyer 2001).
The garden in which the sporophores were found was
established about 1996 and is isolated within cleared
farm land surrounded by lawn and a gravel driveway.
There are three ornamental trees in the garden; a birch
(B. pendula), a crab apple (Malus sp.) and a golden ash
(Fraxinus excelsior ‘Aurea’). The trees were purchased
in Balingup, a town approximately 60 km northwest of
Manjimup. The birch tree is the most likely host. The
owners of the property rst noticed a single sporophore
in 2008, and in June 2009 about 12 sporophores
developed over a 2–3 week period (B. Markotis pers.
comm.).
Although the garden is isolated, future occurrence of
sporophores will need to be monitored and the risk
of spread into P. radiata plantations, neighbouring
ornamental plantings or native forest will need to be
assessed. In southeastern Australia, N. cunninghamii
appears to be the main native species at risk to
hosting A. muscaria. Dunk (2002) conrmed from
Fig. 2 Basidia (left) and spores (right) from the Manjimup
collection of Amanita muscaria. Scale bar = 10 μm (drawn by
K. Syme).
Australasian Mycologist (2010) 29, 4–6
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© 2010 Australasian Mycological Society Inc.
morphological and molecular observations that A.
muscaria ectomycorrhizas were present on roots of
N. cunninghamii in Victoria. Many species of native
ectomycorrhizal fungi are known to associate with N.
cunninghamii (Dunk 2002; Tedersoo et al. 2009). It is
likely that the presence of the exotic Amanita reduces
the diversity of native ectomycorrhizal fungi on N.
cunninghamiis roots (Dunk 2002).
Nothofagus does not occur in WA but in glasshouse
experiments A. muscaria was shown to be capable of
forming ectomycorrhiza on several eucalypts, including
Eucalyptus diversicolor, E. marginata and Corymbia
calophylla, which are endemic to the south west of WA,
and on the eastern Australian E. regnans (Malajczuk
et al. 1982, 1984). The inoculation of these eucalypts
with A. muscaria took place under sterile conditions in
the laboratory. The proportion of short roots colonised
for the western species was relatively low at 0–29%.
In contrast 70–100% of the short roots of E. regnans
seedlings were colonized by A. muscaria (Malajczuk
et al. 1982). It is yet to be conrmed if mycorrhizal
formation would occur naturally on these species in
native eucalypt forest.
In Australia, whenever Amanita muscaria is found under
Eucalyptus, there are almost always exotic hosts in the
vicinity. In Tasmania A. muscaria has been recorded
from both wet and dry sclerophyll forest (Ratkowsky
& Gates 2002, 2005) but it was always associated with
P. radiata wildings or within mixed forest with rainforest
elements (D. Ratkowsky pers. comm.). However,
several recent reports submitted to Fungimap are of
A. muscaria fruiting in Eucalyptus plantations with no
exotic hosts nearby (T. May pers. comm.). Occurrence
of Amanita muscaria on planted eucalypts in eld
conditions needs to be conrmed by examination of
ectomycorrhizas. In New Zealand A. muscaria is found
associated with ornamental plantings of E. cifolia and
E. pauciora (Ridley 1991). E. cifolia is also endemic to
the south-west of WA and is widely planted throughout
southern Australian cities and towns.
Birch is a common ornamental tree in the Manjimup
region, Paxillus involutus, and an unidentied
Scleroderma, which fruit abundantly in early- to mid-
autumn, appear to be the most common fungal
associates (pers. obs.). The present situation requires
a range of surveys to be undertaken to conrm that A.
muscaria is not established elsewhere within the south-
west. Meanwhile, to reduce the potential of spread, the
owners of the property have been advised to destroy
any sporophores that may develop in the future, before
they reach maturity. It is also recommended that the
horticulture and nursery industry be alerted to the
potential spread of this fungus in Western Australia.
Acknowledgements
Thank you to B. Markotis for realizing the signicance
of her nd and J. Dearle for bringing my attention to it.
T. May, T. Lebel and an anonymous referee provided
valuable comment on an earlier draft of the manuscript.
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Australasian Mycologist (2010) 29, 4–6
... Coniferophyta and other primitive trees are the main hosts and in Australia and New Zealand, this fungus has been mostly associated with Pinus plantations (e.g. Stevenson, 1962;Chu-Chou, 1979, 1980Sawyer et al., 2001Sawyer et al., , 2003Robinson, 2010) although it is now invading native plant communities (e.g. Horan et al., 1988;Fuhrer & Robinson, 1992;Ratkowsky & Gates, 2002, 2005. ...
... temperate to arctic zones in boreal forests) (Hawkeswood, 2006). Recently, the species has been discovered in Western Australia (Manjimup) for the first time, where it appears to be associated with Betula pendula Roth (Betulaceae) (Robinson, 2010). Betula pendula is a widespread species in the northern hemisphere (Wikipedia, 2017a). ...
... As regards the Western Australian record of Betula pendula as an associated host for A. muscaria by Robinson (2010), this is quite an extraordinary record for Australia as all other associations of A. muscaria have been with Pinus spp. (Pinaceae) which are ancient plants belonging to Gymnospermae. ...
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... Ces analyses ont été réalisées grâce deux logiciels : Dong et al., 2011), au Zimbabwe (Heinemann, 1966b ;Eyi Dong et al., 2011), au Togo (Data base BR), en Guinée (Data base BR ), Madagascar (Buyck, 2008) et au Burundi (Buyck, 1994b (Härkönen et al., 1995 ), en Zambie (Pegler & Shah-Smith, 1997), au Malawi (Data base BR), au Zimbabwe (Mikola, 1969), au Rwanda (Data base BR), au Swaziland (Reid & Eicker, 1991), en Afrique du Sud (Mikola, 1969 ;Reid & Eicker, 1991) (Mikola, 1969), en Nouvelle Zélande (Mikola, 1969) ainsi qu'en Australie (Mikola, 1969 ;Robinson, 2010) (Robinson, 2010). Toutes les sources affirment qu'elle a été introduite avec les plantations de conifères depuis l'hémisphère nord. ...
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... Australie sous Eucalyptus (Robinson, 2010). Selon Thoen (comm. ...
... muscaria probably corresponds to clade II, with distribution from Eurasia to Alaska and the Pacifi c Northeastern region of the United States; in temperate, boreal and coastal forests with various species of conifers and deciduous trees, relatively common in Europe (Beardslee 1905;Jenkins & Petersen 1976;Breitenbach & Kränzlin 1995;Mattock 1995, Castro 1996Vaasma 2009). For other parts of the world, this taxon certainly corresponds to material collected from exotic plantations, growing under Pinus and other tree species (e.g., Quercus, Picea and Pseudoptsuga) imported from Europe to Tanzania (Härkönen et al. 1994, Tulloss personal communication), Australia (Reid 1979;Grgurinovic 1997, Wood 1997Hawkeswood 2006;Robinson 2010), South Africa (Pearson 1950;Reid & Eicker 1991) and New Zealand (Stevenson 1962;Ridley 1991). In Brazil, this taxon is reportedly found in the plateau region of Rio Grande do Sul among the "European pines" planted there (Homrich 1965). ...
... Cortez 097/08; URM 82988, RET) was collected under a Eucalyptus sp. It is of note that A. muscaria sensu lato has oft en been cited in Australia, albeit associated with exotic plantations (Reid 1979;Grgurinovic 1997, Wood 1997Hawkeswood 2006, Robinson 2010). However, a study conducted by Malajczuk et al. (1982) demonstrated that this species, in its broader sense, is also associated with Eucalyptus. ...
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The generic and sub-generic relationships in the Boletineae (Boletales) were studied using nuclear large subunit (nuc-lsu), translation elongation factor 1-alpha (tef1), and DNA directed RNA polymerase largest subunit (RPB1). The Boletineae, with the exclusion of Hydnomerulius pinastri, was strongly supported and the status of the families Boletaceae and Paxillaceae is discussed. Members of the genus Boletus are found throughout the phylogeny, with the majority not closely related to the type species, Boletus edulis. Many of the traditional, morphologically defined genera are not supported as monophyletic and additional sampling and taxonomic revisions are needed. The majority of the Boletineae are confirmed or putatively ectomycorrhizal (ECM), but two putatively mycoparasitic lineages (one lineage of Buchwaldoboletus lignicola and Chalciporus piperatus and the second Pseudoboletus parasiticus) are strongly supported.
... In New Zealand, Ridley (1991) recorded A. muscaria in association with ornamental plantings of Eucalytpus ficifolia and Eucalytpus pauciflora; E. ficifolia is endemic to the south-west of Western Australia and is widely planted throughout southern Australian. The recent discovery of A. muscaria (on an exotic host) in the south-west of Western Australia is therefore cause for some concern (Robinson 2010). Thus there is a potential threat of A. muscaria establishing itself on Eucalyptus. ...
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The occurrence of the exotic ectomycorrhizal fungus Amanita muscaria in a mixed Nothofagus-Eucalyptus native forest was investigated to determine if A. muscaria has switched hosts to form a successful association with a native tree species in a natural environment. A mycorrhizal morphotype consistently found beneath A. muscaria sporocarps was examined, and a range of morphological and anatomical characteristics in common with those described for ectomycorrhizae formed by A. muscaria on a broad range of hosts were observed. A full description is provided. The likely plant associate was determined to be Nothofagus cunninghamii based upon anatomy of the roots. Analysis of ITS-1 and ITS-2 regions of nuclear ribosomal DNA sequences confirmed the identities of both fungal and plant associates. These findings represent conclusive evidence of the invasion of a non-indigenous ectomycorrhizal fungus into native forest and highlight the ecological implications of this discovery.
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DAR). *Author for correspondence. This work continues the process of documenting the macrofungi of Mt Wellington. Two earlier publications were concerned with the gilled and non-gilled Basidiomycota, respectively, excluding the sequestrate species. The present work deals with the non-sequestrate Ascomycota, of which 42 species were found on Mt Wellington.
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Decaying wood provides an important habitat for animals and forms a seed bed for many shade-intolerant, small-seeded plants, particularly Nothofagus. Using morphotyping and rDNA sequence analysis, we compared the ectomycorrhizal fungal community of isolated N. cunninghamii seedlings regenerating in decayed wood against that of mature tree roots in the forest floor soil. The /cortinarius, /russula-lactarius, and /laccaria were the most species-rich and abundant lineages in forest floor soil in Australian sites at Yarra, Victoria and Warra, Tasmania. On root tips of seedlings in dead wood, a subset of the forest floor taxa were prevalent among them species of /laccaria, /tomentella-thelephora, and /descolea, but other forest floor dominants were rare. Statistical analyses suggested that the fungal community differs between forest floor soil and dead wood at the level of both species and phylogenetic lineage. The fungal species colonizing isolated seedlings on decayed wood in austral forests were taxonomically dissimilar to the species dominating in similar habitats in Europe. We conclude that formation of a resupinate fruit body type on the underside of decayed wood is not necessarily related to preferential root colonization in decayed wood. Rather, biogeographic factors as well as differential dispersal and competitive abilities of fungal taxa are likely to play a key role in structuring the ectomycorrhizal fungal community on isolated seedlings in decaying wood.
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A checklist of 4700 records of 45 species of Amanita and 6 of Limacella is presented for the Iberian Peninsula (Spain and Portugal) and the Balearic Island (Spain). Synonymy, distribution, habitat and herbaria are noted for each taxon, as well as some observations.
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The genus Amanita in New Zealand is reviewed. Fourteen species are accepted of which 10 are endemic to New Zealand. Seven new species are described: Amanita taiepa, A, nehuta, A. pekeoides, A. karea, A. mumura, A. pumatona and A. pareparina. The endemic species are placed in the Amanita sections Amanita, Vaginatae, Validae and Lepidella.
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Ultrastmcture of Eucalyptus ectomycorrhizas initiated by compatible, host-specific fungi and by broad-host range fungi was compared with that of roots inoculated with incompatible, conifer-specific ectomycorrhizal fungi. The results indicate little difference in morphology between ectomycorrhizas formed by compatible, host-specific fungi and those formed by broad-host-range fungi. However, interaction between eucalypt roots and incompatible fungus species known to be conifer-specific induced either deposition of tannins in root tissue or, in the case of the Pseudotsuga-speciiic Suillus lakei, a characteristic hypersensitive reaction which resulted in lysis of hyphae and of epidermal and outer cortical cells of roots.
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Basidiomes of Amanita muscaria were collected from sites in three 30-36-yr-old Pinus radiata plantations in New South Wales, Australia. Following DNA extraction from basidiome stipes, inter-simple sequence repeat PCR using the degenerate primers 5’DHB(CGA)5 and 5’DDB(CCA)5, was used to identify the mycelial genotypes from which basidiomes arose. Each site was found to contain 8-10 A. muscaria genotypes, with six genotypes common to all three sites and one common to two sites. The presence of common genotypes at the three sites is taken to indicate that they were introduced as vegetative inocula when seedlings were planted and have persisted for < 36 yr.
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Although pines have been established in plantations in Western Australia for over 100 years, knowledge of the ectomycorrhizal fungal flora is incomplete, or lies in unpublished reports. A survey of ectomycorrhizal fungi associated with Pinus spp. was conducted throughout south-western Australia. Compared with other regions in the Southern Hemisphere where pines have been introduced, the ectomycorrhizal flora of pines in Western Australia is particularly depauperate, with only nine species of fungi identified from sporocarps and a further two taxa identified from mycorrhizas. Species identified from sporocarps (Hebeloma crustuliniforme, Lactarius deliciosus, Paxillus involutus, Rhizopogon luteolus, R. roseolus, R. vulgaris, Suillus luteus, S. granulatus, Thelephora terrestris) and Cenococcum geophilum are a subset of a larger pine mycorrhizal flora found in eastern Australia, and 8 of the 10 identified species are common to all regions in the Southern Hemisphere where pines have been introduced. These fungi are typically associated with trees, including pines, in the Northern Hemisphere and, apart from Cenococcum geophilum and T. terrestris, are not associated with indigenous vegetation in Western Australia. The mycorrhizal flora colonising roots in a plantation of Pinus radiata D. Don was also investigated, and compared with species identified as present by above-ground sporocarp production. Potential reasons for the limited ectomycorrhizal flora of pines in Western Australia are discussed.
The dependence of certain pine species on a biological soil factor
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Fuhrer BA, Robinson R M 1992. Rainforest Fungi of South-east Australia. CSIRO, Melbourne and the Forestry Commission, Tasmania. 95 pp. Grgurinovic CA 1997. Larger Fungi of South Australia. The Botanic Gardens of Adelaide and State Herbarium. 725 pp.