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Armillaria limonea

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Armillaria limonea

Summary

  • Last modified
  • 14 February 2020
  • Datasheet Type(s)
  • Invasive Species
  • Preferred Scientific Name
  • Armillaria limonea
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Fungi
  •     Phylum: Basidiomycota
  •       Subphylum: Agaricomycotina
  •         Class: Agaricomycetes
  • Summary of Invasiveness
  • Armillaria limonea is a white rot wood decay fungus and root disease pathogen that has confirmed presence in New Zealand only, where it is presumed to be indigenous. It is closely related to A. lut...

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Identity

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Preferred Scientific Name

  • Armillaria limonea (G. Stevenson) Boesewinkel

Other Scientific Names

  • Agaricus melleus sensu Cooke
  • Armillaria mellea sensu Massee
  • Armillariella limonea G. Stevenson
  • Armillariella mellea sensu G. Stevenson

Local Common Names

  • New Zealand: harore

Summary of Invasiveness

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Armillaria limonea is a white rot wood decay fungus and root disease pathogen that has confirmed presence in New Zealand only, where it is presumed to be indigenous. It is closely related to A. luteobubalina in Australia and South America, and to South American A. montagnei. A. limonea occurs naturally on woody debris and as a cause of butt rot in living trees in podocarp-hardwood and southern beech (Nothofagus) forests where it contributes beneficially to carbon and nutrient recycling. It fruits prolifically in native forests, forming large clusters of “toadstool” fruitbodies during winter. Like many other Armillaria species it is recognized by characteristic white mycelial fans or ribbons produced beneath host bark, and by its bootlace-like rhizomorphs by which it spreads vegetatively from colonized buried woody material or stump root systems to infect living host plants.

Armillaria limonea (along with A. novae-zelandiae) was the cause of substantial disease losses in plantations of Pinus radiata planted on sites cleared of native forest in New Zealand during the 1970s and 1980s. Its importance has declined since planting on such sites is no longer practised, although it remains widely distributed. Unlike A. novae-zelandiae, it has not spread to or caused disease in orchards of kiwifruit (Actinidia deliciosa) or in P. radiata plantations established on sites not previously holding indigenous forest cover, and there is no evidence that A. limonea is invasive. Risk of unintended international spread appears to be negligible to nil. If intercepted, isolates of A. limonea may be identified by laboratory culture testing or more rapidly and precisely by molecular sequencing procedures. Armillaria limonea features in the United States Department of Agriculture Agricultural Research Service Fungal Databases. It is considered a risk organism in Hawaiʻi.

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Fungi
  •         Phylum: Basidiomycota
  •             Subphylum: Agaricomycotina
  •                 Class: Agaricomycetes
  •                     Subclass: Agaricomycetidae
  •                         Order: Agaricales
  •                             Family: Marasmiaceae
  •                                 Genus: Armillaria
  •                                     Species: Armillaria limonea

Notes on Taxonomy and Nomenclature

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Armillaria limonea (G. Stevenson) Boesewinkel is a distinct species with its own unique morphology and molecular identity, which was found to be intersterile with other species, including the closely related Armillaria luteobubalina Watling and Kile, in pairing studies using haploid isolates (Kile and Watling, 1988).

In New Zealand, Armillariella mellea sensu G. Stevenson, Agaricus melleus sensu Cooke and Armillaria mellea sensu Massee were used for both A. limonea and Armillaria novae-zelandiae (G. Stevenson) Herink before it was accepted that Armillaria mellea (Vahl) Kumm. is not naturally present in the Southern Hemisphere. The Maori word harore is a term used especially for the common New Zealand Armillaria species fruiting in winter, but also loosely for other edible agarics or fungi in general. 

The holotype of A. limonea, collected by G. Stevenson in New Zealand in 1949, is in the Fungarium at the Royal Botanic Gardens, Kew (Kew Mycology Collection, 2020; New Zealand Fungi, 2020)

Description

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Descriptions of Armillaria limonea are provided by Stevenson (1964) and Gadgil (2005). See also van der Pas et al. (2008) and Cooper (2016).

As described by Gadgil (2005): “Basidiomata pileate, centrally stipitate. Pileus 80–130 mm in diameter, lemon yellow, with dark brown tufted scales sprinkled thickly at centre and more sparsely towards the margin, convex at first, becoming almost plane later, dry; flesh firm, white. Gills sinuately decurrent, moderately crowded, creamy white, becoming pinkish fawn. Stipe tapering towards the pileus, with a bulbous base, light brown above a substantial floccose annulus, shading to brown or olive green below, velutinate, solid, 100–150 mm long. Basidiospores ovoid, 7–8 × 5–7 m, non-amyloid; spore print white.”

Distribution

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Armillaria limonea occurs in native forests in New Zealand from the north of North Island to the north of South Island, and there are three records from the southern South Island (New Zealand Fungarium, 2020). Armillaria limonea is reported but not confirmed from South America. It was reported in Tierra del Fuego, Argentina (Raithelhuber, 1987; 1991; 1992; 2004; Niveiro and Albertό, 2013) but needs molecular validation (Pildain et al., 2010). Coetzee et al. (2003) found an isolate from an unknown fruitbody resembling A. limonea in Chile was actually of A. luteobubalina.

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Last updated: 14 Feb 2020
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Oceania

New ZealandPresent, WidespreadNative1964Stevenson (1964)Present from north of Auckland in the North Island to the southern South Island. One of four Armillaria species indigenous to New Zealand.

South America

ArgentinaAbsent, Unconfirmed presence record(s)1980Horak (1980)Tierra del Fuego, Patagonia. However, occurrence needs molecular validation as an isolate from a fruitbody resembling A. limonea in Chile was found to actually be A. luteobubalina
ChileAbsent, Unconfirmed presence record(s)1969Singer (1969)Cordillera Pelada, Los Ríos Region; Puerto Hambre, Magallanes Region. However, occurrence needs molecular validation. An isolate from a fruitbody resembling A. limonea in Chile was found to actually be A. luteobubalina

History of Introduction and Spread

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There is no evidence that A. limonea has spread internationally due to human activity.

Risk of Introduction

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The risk of A. limonea spreading outside New Zealand to other countries appears to be negligible to nil. A. limonea is largely confined to roots and root collars of infected trees and shrubs. In young plants mycelial fans may extend above soil level only if host resistance declines prior to or after death, or because of physiological stress from some additional external physical, chemical or biological cause. In older indigenous trees A. limonea may form a butt rot or basal canker immediately above ground level. However, the export of old growth native timber from New Zealand is restricted (Forestry New Zealand, 2020). A. limonea (probably) and A. novae-zelandiae are present causing non-lethal infection at and below soil level in a proportion of mature (up to ca. 25 years old) Pinus radiata trees growing on land cleared of native forest, indicating minimal risk of their being present in harvested logs cut at stump height. However, butt rot does not develop prior to harvest in these trees and such first rotation P. radiata stands are now becoming uncommon. In New Zealand much P. radiata is grown on land that was previously non-forested, but in these stands there is virtually no infection by A. limonea (in contrast to A. novae-zelandiae), yielding logs that pose no risk from this species.

Armillaria limonea requires a supporting wood- or organic-based substrate to survive, so its presence in nurseries is rare. Any infected plants would normally show readily detectable disease symptoms. It is possible that soil admixtures such as peat or other organic material might support A. limonea saprotrophically if the pathogen was somehow introduced, but the risk of movement in nursery stock would seem low.

Discussion on the risk of introducing Armillaria species to North America in logs of P. radiata and Douglas fir is included in White et al. (1992), who estimate it as low risk. A. limonea features in the United States Department of Agriculture Agricultural Research Service fungal databases (USDA-ARS, 2019), but is not included in the EPPO Global Database (EPPO, 2019). A. limonea is considered to be a risk organism in Hawaiʻi (DeNitto et al., 2015).

Habitat

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In New Zealand, A. limonea occurs naturally (along with A. novae-zelandiae) as a very common saprotrophic fungus causing decay in coarse woody debris and as a butt rot species in living trees in native forests, both podocarp-hardwood and southern beech (Nothofagus) (Colenso, 1890; Birch, 1937a; Gilmour, 1954; 1966; Hood and Sandberg, 1987; Hood et al., 2004b; 2019). Rhizomorphs are prolific in the soil beneath podocarp-hardwood forests, growing epiphytically across healthy roots without infecting them. Roots of older trees can be found with Armillaria-caused decay, but it is not clear whether the fungus is the cause of death or if the roots were killed or weakened from some other cause. A. limonea is not generally seen as a pathogen of native trees (Rawlings, 1952) but Armillaria-caused mortality has occurred e.g., in densely stocked Nothofagusmenziesii saplings regenerating in gaps after storm damage (Birch, 1937b) and in the same host planted as an ornamental specimen tree in urban settings (Hood, 1989). Nevertheless, Armillaria species provide an indispensable service as important members of the indigenous wood decay community. Along with other decomposer fungi, A. limonea contributes significantly to carbon and nutrient recycling in the native forest ecosystem (Hood et al., 2019).

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
Terrestrial
Terrestrial – ManagedManaged forests, plantations and orchards Secondary/tolerated habitat Harmful (pest or invasive)
Managed forests, plantations and orchards Secondary/tolerated habitat Productive/non-natural
Urban / peri-urban areas Present, no further details Harmful (pest or invasive)
Urban / peri-urban areas Present, no further details Productive/non-natural
Terrestrial ‑ Natural / Semi-naturalNatural forests Principal habitat Natural
Scrub / shrublands Present, no further details Natural

Hosts/Species Affected

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Armillaria limonea occurs as a parasite on a wide range of host species, both angiosperms and gymnosperms. An online global list of hosts is provided by the United States Department of Agriculture Agricultural Research Service, Fungal Database (USDA-ARS, 2019). Host lists are given by Gilmour (1966), Dingley (1969), Laundon (1973), Shaw et al. (1976), Pennycook (1989), McKenzie et al. (1999; 2000), Gadgil (2005) and van der Pas et al. (2008). A. limonea and A. novae-zelandiae are not always distinguished in these lists. In New Zealand Armillaria species (A. limonea and A. novae-zelandiae) are or have been important in fruit orchards (Atkinson, 1971) and in forest plantations, particularly of Pinus radiata. Pathogenicity by A. limonea to P. radiata has been demonstrated by inoculation experiments with seedlings (Shaw et al., 1981; Benjamin, 1983; Kile, 1984; Hood and Sandberg, 1993b).

Host Plants and Other Plants Affected

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Plant nameFamilyContext
Acacia melanoxylon (Australian blackwood)FabaceaeUnknown
Agathis australis (kauri)AraucariaceaeUnknown
Aristotelia serrataGelechiidaeUnknown
Beilschmiedia tawaLauraceaeUnknown
Cedrus atlantica (Atlas cedar)PinaceaeUnknown
Chamaecyparis lawsoniana (Port Orford cedar)CupressaceaeUnknown
Citrus sinensis (navel orange)RutaceaeUnknown
Cryptomeria japonica (Japanese cedar)TaxodiaceaeUnknown
Cupressus macrocarpa (Monterey cypress)CupressaceaeUnknown
Dacrycarpus dacrydioides (white pine)PodocarpaceaeUnknown
Dacrydium cupressinumPodocarpaceaeUnknown
DeutziaHydrangeaceaeUnknown
Discaria toumatouRhamnaceaeUnknown
Eucalyptus delegatensis (alpine ash)MyrtaceaeUnknown
Eucalyptus regnans (mountain ash)MyrtaceaeUnknown
Euonymus japonicus (Japanese spindle tree)CelastraceaeUnknown
Hedycarya arboreaMonimiaceaeUnknown
Jacaranda mimosifolia (jacaranda)BignoniaceaeUnknown
Knightia excelsaProteaceaeUnknown
Larix decidua (common larch)PinaceaeUnknown
Larix kaempferi (Japanese larch)PinaceaeUnknown
Leycesteria formosaCaprifoliaceaeUnknown
Liriodendron tulipifera (tuliptree)MagnoliaceaeUnknown
Lycium ferocissimum (African boxthorn)SolanaceaeUnknown
Malus domestica (apple)RosaceaeUnknown
Manoao colensoiPodocarpaceaeUnknown
Metasequoia glyptostroboides (water fir)TaxodiaceaeUnknown
Metrosideros robustaMyrtaceaeUnknown
NothofagusNothofagaceaeUnknown
Nothofagus fusca (red beech)NothofagaceaeUnknown
Nothofagus menziesiiNothofagaceaeUnknown
Nothofagus solandriNothofagaceaeUnknown
Nothofagus solandri var. cliffortioidesNothofagaceaeUnknown
Nothofagus truncataNothofagaceaeUnknown
Olearia avicenniifoliaAsteraceaeUnknown
Paraserianthes lophantha (brush wattle)FabaceaeUnknown
Persea americana (avocado)LauraceaeUnknown
Phyllocladus alpinusPodocarpaceaeUnknown
Pinus caribaea (Caribbean pine)PinaceaeUnknown
Pinus contorta (lodgepole pine)PinaceaeUnknown
Pinus elliottii (slash pine)PinaceaeUnknown
Pinus muricata (bishop pine)PinaceaeUnknown
Pinus nigra ssp. laricioPinaceaeUnknown
Pinus palustris (longleaf pine)PinaceaeUnknown
Pinus patula (Mexican weeping pine)PinaceaeUnknown
Pinus pinaster (maritime pine)PinaceaeUnknown
Pinus ponderosa (ponderosa pine)PinaceaeUnknown
Pinus radiata (radiata pine)PinaceaeMain
Pinus strobus (eastern white pine)PinaceaeUnknown
Pinus taeda (loblolly pine)PinaceaeUnknown
Pittosporum crassifoliumPittosporaceaeUnknown
Podocarpus totara (totara)PodocarpaceaeUnknown
Populus sp. (poplar)SalicaceaeUnknown
Prumnopitys taxifoliaPodocarpaceaeUnknown
Prunus armeniaca (apricot)RosaceaeUnknown
Prunus persica (peach)RosaceaeUnknown
Pseudotsuga menziesii (Douglas-fir)PinaceaeUnknown
Pyrus communis (European pear)RosaceaeUnknown
Rhododendron (Azalea)EricaceaeUnknown
Ribes nigrum (blackcurrant)GrossulariaceaeUnknown
Ribes uva-crispa (gooseberry)GrossulariaceaeUnknown
Rubus idaeus (raspberry)RosaceaeUnknown
Salix (willows)SalicaceaeUnknown
Salix alba var. vitellinaUnknown
Salix fragilis (crack willow)SalicaceaeUnknown
Schefflera digitataAraliaceaeUnknown
Tecoma capensis (Cape honeysuckle)BignoniaceaeUnknown
Thuja plicata (western redcedar)CupressaceaeUnknown
Tsuga heterophylla (western hemlock)PinaceaeUnknown
Vitis vinifera (grapevine)VitaceaeUnknown
Weinmannia racemosa (maori)CunoniaceaeUnknown

Growth Stages

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Symptoms

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As with other Armillaria species, plants infected by A. limonea suffer injury and death of tissues in the roots and root collar region, accompanied by resinosis or gummosis (depending on the host). Characteristic signs are black, shoelace-like rhizomorphs and white mycelial sheeting or ribbons beneath the bark. Younger plants wilt or show crown discoloration and retain dead foliage for a time if they are killed rapidly. Older trees may decline more slowly or, in the case of Pinus radiata, retain green foliage, to all intents and purposes appearing healthy, although infected at the root collar. Old, mature trees may develop butt rot.

List of Symptoms/Signs

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SignLife StagesType
Leaves / abnormal colours
Leaves / wilting
Leaves / yellowed or dead
Roots / 'dirty' roots
Roots / fungal growth on surface
Roots / reduced root system
Roots / rot of wood
Stems / gummosis or resinosis
Stems / internal discoloration
Stems / mycelium present
Stems / rot
Whole plant / discoloration
Whole plant / dwarfing
Whole plant / plant dead; dieback
Whole plant / uprooted or toppled
Whole plant / wilt

Biology and Ecology

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Genetics

Like many other Armillaria species, A. limonea is assumed to have a diploid vegetative mycelium, undergoing meiosis to form haploid basidiospores.

Virulence

Inherently, A. limonea appears to show an intermediate level of virulence when compared with other saprotrophic and pathogenic species of Armillaria. In New Zealand, A. limonea has not shown secondary spread between adjacent root systems of young infected Pinus radiata trees as occurs, for instance, with the more virulent Armillariaostoyae in Pinus pinaster stands in the Landes de Gascogne forest region in southwest France (Roth et al., 1979; van der Pas, 1981b; Lung-Escarmant and Guyon, 2004). Inoculation studies have demonstrated that different A. limonea isolates vary innately in their level of virulence to P. radiata (Shaw et al., 1981; Benjamin, 1983; Hood and Sandberg, 1993b).

Reproductive Biology

Fruiting occurs over several weeks between April and July (Hood et al., 2004a; Hood and Gardner, 2005) (Southern Hemisphere autumn-winter). Small and often very large clusters of fruitbodies appear in natural forests (along with those of A. novae-zelandiae) on woody debris in indigenous forests, producing copious quantities of basidiospores. Fruiting is rare on infected introduced host trees and shrubs. There is no asexual stage.

Physiology and Phenology

MacKenzie (1987) found that plantation P. radiata trees older than ca. 10 years (near mid-rotation) are not killed but interact dynamically with Armillaria while remaining green and apparently healthy. Over time, infection at the root collar decreases in some trees while increasing in others. This behavior has been confirmed for A. novae-zelandiae (Hood et al., 2002) and is also probably true of A. limonea.

Armillaria limonea demonstrates bioluminescence in both the fruitbody gills (Cooper, 2016) and mycelium, and Armillaria-decayed wood may be seen faintly glowing in native forests on dark nights. Cultures are also bioluminescent, especially when young and actively growing.

Population Size and Structure

In native forests, populations of A. limonea are composed of comparatively high colony densities per unit ground area. In a study in natural podocarp hardwood forest in New Zealand, cultural pairing of isolates demonstrated a density of colonies (vegetative compatibility groups) of A. limonea ranging from 15-56 colonies/ha (Hood and Sandberg, 1987; Hood, 1989). Similar studies in young P. radiata plantations that had replaced native forest yielded equivalent values of 3 colonies/ha (Benjamin, 1983; Shaw, 1984) and between 15 and 46 colonies/ha (Hood and Sandberg, 1993b). Although numerous, these were not as high as values for A. novae-zelandiae in the same stands.

Rhizomorphs are produced prolifically. Hood and Sandberg (1987) recorded an average aggregate rhizomorph length (comprising both A. limonea and A. novae-zelandiae) ranging from 2 to 9 m/m2 of soil surface down to a depth of 22 cm beneath a podocarp-hardwood forest logged of the podocarp element three decades earlier.

Climate

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ClimateStatusDescriptionRemark
Cf - Warm temperate climate, wet all year Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year

Means of Movement and Dispersal

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Natural Dispersal

Like many other Armillaria species, A. limonea spreads vegetatively from colonized woody matter by means of rhizomorphs. Infection of live hosts by this means leads to the formation of small disease centres. Although basidiospores are no doubt significant in setting up new centres, they do not appear to be as relevant to dispersal as those of A. novae-zelandiae.

Accidental Introduction

Low to no risk of accidental introduction - see “Risk of Introduction”.

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Forestry Yes Yes
Horticulture Yes Yes
Nursery trade Yes Yes

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Plants or parts of plants Yes Yes

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Growing medium accompanying plants Yes Yes Pest or symptoms usually visible to the naked eye
Roots Yes Yes Pest or symptoms usually visible to the naked eye
Seedlings/Micropropagated plants Yes Yes Pest or symptoms usually visible to the naked eye
Stems (above ground)/Shoots/Trunks/Branches Yes Yes Pest or symptoms usually visible to the naked eye

Impact Summary

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CategoryImpact
Cultural/amenity Negative
Cultural/amenity Positive
Economic/livelihood Negative

Economic Impact

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In New Zealand, A. limonea, along with A. novae-zelandiae, at one time caused serious damage in Pinus radiata plantations. General accounts of the disease in forests have been published by Gilmour (1966), Shaw (1976), Ridley and Dick (2001) and van der Pas et al. (2008), and a review was produced by Hood (1989). Growth loss and economic analyses in P. radiata plantations have been undertaken by Shaw and Calderon (1977), MacKenzie (1987), Self and MacKenzie (1995) and Kimberley at al. (2002).

First rotation pine plantations on cleared indigenous forest sites

Little indigenous forest is now converted to exotic pine plantation in New Zealand, but this practice was widespread during the 1970s and 1980s leading to severe mortality due to Armillaria (A. limonea, along with A. novae-zelandiae) in the young pine crops (Beveridge et al., 1973). Tracts of remnant podocarp-hardwood and southern beech forest previously logged of commercially valuable trees were clear felled, desiccated and burnt prior to planting. Heat from the fire temporarily reduced the level of Armillaria inoculum (Hood and Sandberg 1989), but recolonization of dead wood was rapid with signs of mycelial fans, rhizomorphs and (in season) prolific fruiting by A. limonea and A. novae-zelandiae on charred stumps and logs within 1-2 years. Mortality of pine seedlings commenced 3 to 6 months after planting and continued at an increasing rate for 3-5 years before declining (MacKenzie and Shaw, 1977; Roth et al., 1979; van der Pas, 1981a). Resultant mortality gaps were associated with indigenous hardwood stump root systems, which acted as a substrate providing an enhanced inoculum potential (Shaw and Calderon, 1977; Roth et al., 1979; van der Pas, 1981b; Benjamin, 1983; Kile, 1984; van der Pas and Hood, 1984; Hood and Sandberg, 1993b). Mortality then declined up to about age 10 years, but infection continued on through the remainder of the 25- to 30-year rotation in ca. 15% of the residual crop trees in a cryptic, non-lethal form (trees infected at the root collar, presumably by both species, retained green crowns and appeared healthy). There was no evidence of secondary spread between pine trees (Shaw and Toes, 1977; Roth et al., 1979; MacKenzie, 1987).

Estimates of seedling deaths during the first 5 years ranged from 10-50% over an area of between 50,000 and 60,000 ha of land formerly covered in remnant podocarp-hardwood forest, with lower values on former southern beech forest sites (Shaw and Calderon, 1977; van der Pas, 1981a; Hood, 1989). The uneven distribution of mortality resulted in potentially lower stem wood quality in surviving trees because of excessive branch growth and hence knot size in stand gaps. Estimates of wood volume loss per unit land area in a rotation varied between 6% and 32% as a result of a combination of underutilized ground space due to mortality gaps and reduced growth increment from non-lethal infection in surviving trees (Shaw and Calderon, 1977; MacKenzie, 1987; Kimberley at al., 2002).

Second rotation pine plantations

There is now little planting of pine directly onto indigenous forest cutover sites in New Zealand, and early mortality in second and third rotation pine stands on such sites is generally lower (up to 5% of trees killed in small, scattered disease centres) and of little concern, with some exceptions (van der Pas, 1981a; MacKenzie and Self, 1988). Non-lethal infection is widespread, but variable in pine stands throughout New Zealand, ranging from less than 1% to 38% of trees affected, depending on the pre-plantation vegetation cover (Hood and Sandberg, 1993a; Self et al., 1998; Hood et al., 2002). Non-lethal infection makes up a significant but smaller component of the overall growth loss (Kimberley et al., 2002). However, on former native forest sites it has not been determined how much is due to A. limonea, and on non-indigenous forest sites A. limonea is largely absent. 

Impact: Biodiversity

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A. limonea is not known to threaten species or affect biodiversity.

Social Impact

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In New Zealand, Armillaria is common in mainly introduced hosts in parks and urban gardens where it is responsible for a probably substantial number of deaths of amenity trees and shrubs. It is not certain how much of this is due to A. limonea.

Risk and Impact Factors

Top of page Invasiveness
  • Has a broad native range
  • Abundant in its native range
  • Pioneering in disturbed areas
  • Tolerant of shade
  • Capable of securing and ingesting a wide range of food
Impact outcomes
  • Host damage
  • Negatively impacts agriculture
  • Negatively impacts forestry
  • Negatively impacts livelihoods
Impact mechanisms
  • Pest and disease transmission
  • Parasitism (incl. parasitoid)
  • Pathogenic
Likelihood of entry/control
  • Difficult/costly to control

Uses

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Economic Value

Armillaria limonea has no economic benefit.

Social Benefit

The young fruitbodies of A. limonea are edible. Known as “harore” they are harvested by some Maori.

Uses List

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Human food and beverage

  • Food

Diagnosis

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To identify the species first requires laboratory isolation of fungal cultures from infected tissue, mycelial sheeting, rhizomorphs or, if present, fruitbody tissue. This is done by antiseptically transferring small pieces onto plates of an Armillaria-selective medium such as malt extract agar with suitable antibiotic &/or biocidal additives (e.g., o-phenylphenol or benomyl) to discourage contaminating bacteria and other unwanted fungi (Morrison et al., 1991; Worrall, 1991). One recipe prescribes the addition of from 2 to 10 ppm benomyl and (after autoclaving and cooling before pouring plates) 100 ppm streptomycin sulphate to a 2% malt extract agar base (although a substitute may need to be found if the fungicide Benlateä, active ingredient 50% benomyl, becomes unavailable). Cultures may be maintained in the laboratory by sub-culturing on potato dextrose or 2% malt extract agar. Armillaria isolates are readily recognized in culture from their reddish-purple crustose appearance and production of characteristic rhizomorphs (distinct in appearance, however, from those formed in the field), but additional techniques are necessary for distinguishing species.

An older procedure to identify an unknown diploid field isolate, first developed with Northern Hemisphere Armillaria species (Korhonen, 1978), was to pair it with a range of selected, white, fluffy, single spore, haploid, tester isolates of known species. The paired tester isolate that changed from white fluffy to a dark purple, crustose, diploid form identified the unknown as being of the same species (Kile and Watling, 1988; Hood and Sandberg, 1987). The method is mostly reliable but takes time and the result is not always clear cut. Isolates of A. limonea can also be distinguished from those of A. novae-zelandiae by the production of rhizomorphs only in the former after growing for ca. three weeks under a 24-hour photoperiod using specified lighting conditions (Shaw et al., 1981; Benjamin, 1983; Hood and Sandberg, 1987).

More recently, cultures of A. limonea have been distinguished from other Armillaria species using molecular techniques (Coetzee et al. 2001; 2003; Maphosa et al. 2006; Pildain et al. 2009; 2010). Molecular procedures have been developed for identifying A. limonea using the ribosomal internal transcriber spacer region (Dodd et al. 2006; 2010).

Detection and Inspection

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As with other Armillaria species, first evidence of disease in a crop will be symptoms of wilting or crown discoloration. Removal of soil to expose the root collar using a small trowel or grubber may reveal evidence of oozing resin or gum in conifers or hardwood species, respectively. This presence of resinosis or gummosis indicates damage to the living host, implying that the pathogen is acting parasitically and not simply feeding saprotrophically on already dead tissue. Black, branching, bootlace-like rhizomorphs consisting of a thin, outer, black rind and a soft, inner, pinkish, hyphal core, may be present. Another defining feature is characteristic, thick, white mycelial sheets, fans or ribbons which are revealed by using a knife to cut and prise away the bark. If the host is already dead and no longer resisting the pathogen, these sheets may be present more extensively running up into the stem. Rarely, fruitbodies may be present (see “Description”, above). Unlikely in crop plants, but in older, mature trees, a butt heartwood rot may be present with a distinctive moist, cheesy, yellowish, fibrous decay interspersed with thin, black zone lines (the edges of sclerotial sheeting forming large, 2-3 cm “pockets” within the wood) which give rise to a scalloped appearance on drying.

Similarities to Other Species/Conditions

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Armillaria limonea is one of many Armillaria species broadly similar in appearance and behavior (Watling et al., 1991; Pegler, 2000). All have white basidiospores, an anulus or ring (partial veil) around the fruitbody stipe (toadstool stalk), and many produce rhizomorphs (species without a ring belong in the recently erected genus, Desarmillaria (Koch et al., 2017)). Species vary in their level of intrinsic pathogenicity against different hosts, but many are responsible for economic diseases in crops, plantations and managed natural forests around the world (Hood et al., 1991; Kile et al., 1991). All species also feed saprotrophically, colonizing and producing a white rot in wood, on which they fruit. Molecular analysis has shown that A. limonea belongs in a broad group of Southern Hemisphere Armillaria species that cluster separately from those in the Northern Hemisphere (Maphosa et al., 2006; Coetzee et al., 2011; Klopfenstein et al., 2017). Armillaria limonea is closest to A. luteobubalina, found in Australia and South America, and to South American A. montagnei (Coetzee et al., 2003; 2011; 2018; Maphosa et al., 2006; Pildain et al., 2009; 2010; Klopfenstein et al., 2017). Fruitbodies of these species are very similar morphologically, but tissues of A. limonea lack the persistent unpleasant taste of those of A. luteobubalina and A. montagnei (Podger et al., 1978; Coetzee et al., 2018). These species likely diverged after the breakup of Gondwana (Coetzee et al., 2011; 2018; Klopfenstein et al., 2017).

In New Zealand A limonea and A. novae-zelandiae are the two most common Armillaria species. The rhizomorphs of these species are difficult to distinguish in the field (Hood and Sandberg, 1987) but according to Benjamin (1983) those of Anovae-zelandiae are slightly thicker on average and produced in greater abundance than those of AlimoneaArmillaria limonea fruit bodies tend to be larger than those of Anovae-zelandiae, and unlike the latter the cap is not viscid (tacky) when first formed. Rhizomorphs are common, dichotomous in form (Benjamin, 1983Morrison, 1989).

Unusually for Armillaria species, Alimonea was first recognized as a distinct taxon on morphological grounds (Stevenson, 1964). However, to distinguish it confidently from other species internationally requires cultural or molecular procedures (see “Diagnosis”).

Prevention and Control

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Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Cultural Control and Sanitary Measures

Field experiments have demonstrated the importance of the quality of the planting stock on sites known to be infested with A. novae-zelandiae and A. limonea. In a first rotation Pinusradiata stand on a site cleared of podocarp-hardwood forest in New Zealand mortality from the disease among newly planted seedlings was lower than among rooted cuttings (Klomp and Hong, 1985). However, with improved quality of P. radiata cuttings, the trend was reversed when a second rotation trial stand was established on the same site (Hood et al., 2006). In each case, better planting stock was at an advantage when exposed to Armillaria inoculum.

Physical/Mechanical Control

Removal of stumps and woody debris before planting is the most effective method of control of Armillaria root disease. However, this procedure has been applied only occasionally in forest plantations in New Zealand because benefits are not seen by forest managers to outweigh the initial expense, despite economic analyses to the contrary (Shaw and Calderon, 1977; MacKenzie, 1987; Self and MacKenzie, 1995). Unlike some other management options, stump extraction also benefits subsequent rotations by removing inoculum from the site, although its effects on soil quality (removal of topsoil, compaction) must also be considered. Soil cultivation without stump removal has a number of advantages e.g., improved planting efficiency and better establishment, but it is not clear if this procedure reduces disease levels.

In one study, removal of indigenous forest stumps reduced mortality among planted pine seedlings to 12-21% after 5 years, compared with 52% on the untreated site (Shaw and Calderon, 1977; van der Pas, 1981a). In another, similar trial, which included clearing debris into windrows after removing indigenous forest stumps, mortality after 4 years was 1% in treated and 23% in untreated plots (van der Pas and Hood, 1984). In a third trial, in a second rotation Pinus radiata pine plantation following Pinus ponderosa that had been planted on a cleared indigenous forest site and subsequently poison thinned, mortality was reduced after 5 years from 22% (untreated) to 5% (stumps removed) at one site and from 10% to less than 1% at another (Self and MacKenzie; 1995). After 8 years, non-lethal infection in the same trial was reduced from 67% to 31% of trees affected and from 85% to 10% of trees, in the respective sites. In all these studies no attempt was made to distinguish A. limonea from A. novae-zelandiae.

Biological Control

Isolates of Trichoderma fungi species have been tested for controlling Armillaria root disease in New Zealand. In one trial Pinusradiata seedling root systems were immersed in a selected Trichoderma slurry treatment before planting on an Armillaria-infested site. Mortality after 2 years was 6% of treated plants compared with 22% in the untreated controls (Cutler and Hill, 1994). Surviving treated plants were healthier. Certain basidiomycete fungi showing promise against A. novae-zelandiae and A. limonea in laboratory testing were not effective when inoculated into P. radiata thinning stumps in a field trial (Li and Hood, 1992; Hood et al., 2015). This work has not continued.

Chemical Control

There has been some research to test the effectiveness of chemical treatments in reducing the incidence of Armillaria root disease in forest plantations (without distinguishing the causal species) although none have been used operationally. Mortality 4 years after planting Pinus radiata on an indigenous forest cutover site was 9% in plots with stumps treated with a commercial hydrocarbon mixture containing methyl isothiocyanate, compared with 23% in untreated plots, despite there being no difference in the frequencies and quantities of soil rhizomorphs between sites (van der Pas and Hood, 1984). A similar result was obtained after applying agricultural lime to the soil surface. Sodium pentachlorphenate and pentachlorphenol introduced to the soil gave no protection to container grown P. radiata against artificial inoculum of A. limonea (Shaw et al., 1980).

Host Resistance (Incl. Vaccination)

There is evidence that host species vary in resistance or tolerance to A. limonea. In inoculation studies, Benjamin and Newhook (in Kile, 1984) found more seedlings of Pinus radiata became infected and died than did those of Eucalyptus species, among which variation also occurred. Field observations of the effects of Armillaria root disease (A. novae-zelandiae and A. limonea) on tree species planted on sites cleared of indigenous forest have been published (Weston, 1957, Gilmour, 1966). Most susceptible were P. radiata, species of Larix and Chamaecyparislawsoniana, while least affected were Cryptomeria japonica and Thuja plicata (Hocking and Mayfield, 1939; Jolliffe, 1940; Lysaght, 1942). Douglas fir (Pseudotsuga menziesii) was as susceptible as P. radiata but showed lower rates of mortality. Losses were low among eucalypts (Newhook, 1964). Although apparently less vulnerable, C. japonica was found to develop butt heart rot caused by Armillaria. A list of species recorded as susceptible to the disease in New Zealand (without distinguishing between A. novae-zelandiae and A. limonea) was published by van der Pas et al. (2008).

Monitoring and Surveillance (Incl. Remote Sensing)

Monitoring of mortality is normally undertaken on the ground by means of transects or other appropriate field design (Hood and Kimberley, 2002). In Pinusradiata plantations, non-lethal infection is estimated in the same way, except that in the absence of crown symptoms it is also necessary to expose the root collar to reveal the presence and extent of girdling infection (Shaw and Toes, 1977). Firth and Brownlie (2002) found that by using high resolution, colour, stereo aerial photography it was possible to detect most trees greater than 2 m tall that had been killed by Armillaria (without distinguishing species), reducing the time and investment necessary for ground monitoring. Mapping of infested sites in second rotation stands indicated that the distribution of non-lethally infected trees showed a broad approximation to that of trees visibly killed by the disease (e.g., areas with an average pre-thinning mortality greater than 3% of trees killed were reasonable indicators of stand areas with non-lethal infection exceeding 25%). This implied that it might be possible to use the distribution of visible mortality (e.g., from aerial photography) to produce contour maps that predict and delineate areas requiring treatment, either during or at the end of the rotation (Hood and Kimberley, 2002; Hood et al., 2006). This work has not proceeded further.

References

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Shaw, C. G., III, 1984. Pathogenicity and pathogenicity testing. In: Proceedings of the Sixth International Conference on Root and Butt Rots of Forest Trees. Melbourne, Victoria and Gympie, Queensland, Australia, August 25-31, 1983 [Proceedings of the Sixth International Conference on Root and Butt Rots of Forest Trees. Melbourne, Victoria and Gympie, Queensland, Australia, August 25-31, 1983], [ed. by Kile, G.A.]. Melbourne, Australia: CSIRO, Division of Forest Research, International Union of Forestry Research Organizations (IUFRO) Working Party S2.06.01. 131-197.

Shaw, C. G., III, Calderon, S., 1977. Impact of Armillaria root rot in plantations of Pinus radiata established on sites converted from indigenous forest. New Zealand Journal of Forestry Science, 7(3), 359-373.

Shaw, C. G., III, MacKenzie, M., Toes, E. H. A., 1980. Pentachlorophenol fails to protect seedlings of Pinus radiata from Armillaria root rot. European Journal of Forest Pathology, 10(6), 344-349.

Shaw, C. G., III, MacKenzie, M., Toes, E. H. A., Hood, I. A., 1981. Cultural characteristics and pathogenicity to Pinus radiata of Armillaria novae-zelandiae and A. limonea. New Zealand Journal of Forestry Science, 11(1), 65-70.

Shaw, C. G., III, Sijnja, D., MacKenzie, M., 1976. Toetoe (Cortaderia fulvida) - a new graminaceous host for Armillaria root rot. New Zealand Journal of Forestry, 21(2), 265-268.

Shaw, C. G., III, Toes, E. H. A., 1977. Impact of Dothistroma needle blight and Armillaria root rot on diameter growth of Pinus radiata. Phytopathology, 67(11), 1319-1323. doi: 10.1094/Phyto-67-1319

SINGER, R., 1969. Mycoflora Australis. Nova Hedwigia, 29, 405 pp.

Stevenson G, 1964. The Agaricales of New Zealand: V. Tricholomataceae. 19(1) : Kew Bulletin. 1-59. https://www.jstor.org/stable/4108283

USDA-ARS, 2019. Germplasm Resources Information Network (GRIN). Online Database. In: Germplasm Resources Information Network (GRIN). Online Database Beltsville, Maryland, USA: National Germplasm Resources Laboratory.https://npgsweb.ars-grin.gov/gringlobal/taxon/taxonomysimple.aspx

Watling R, Kile GA, Burdsall Jr HH, 1991. (Chapter 1 Nomenclature, taxonomy and identification). In: Armillaria Root Disease. Agriculture Handbook No. 691, [ed. by Shaw III CG, Kile GA]. Washington DC, USA: United States Department of Agriculture, Forest Service.

Weston, G. C., 1957. Exotic forest trees in New Zealand. In: Seventh British Commonwealth Forestry Conference, Australia and New Zealand, 1957 [Seventh British Commonwealth Forestry Conference, Australia and New Zealand, 1957], xxvii + 104 pp.

White, W. B., Nitto, G. A. de, Hanson, J. B., Bellinger, M. D., Russell, T. H., Jr., 1992. Pest risk assessment [including termites and other insect pests, root disease and decay fungi] of the importation of Pinus radiata and Douglas fir [Pseudotsuga menziesii] logs from New Zealand. In: Miscellaneous Publication - USDA Forest Service , (No. 1508) . Washington, USA: USDA Forest Service.v + 235 pp.

Worrall, J. J., 1991. Media for selective isolation of Hymenomycetes. Mycologia, 83(3), 296-302. doi: 10.2307/3759989

Distribution References

Horak E, 1980. (Fungi, Basidiomycetes. Agaricales y Gasteromycetes secotioides). Flora Criptogámica de Tierra del Fuego. 11 (6), 1-524.

Singer R, 1969. Mycoflora Australis. Nova Hedwigia. 405 pp.

Stevenson G, 1964. The Agaricales of New Zealand: V. Tricholomataceae. In: Kew Bulletin. 19 (1) 1-59. https://www.jstor.org/stable/4108283

Contributors

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16/10/19 Original text by:

Ian Hood, New Zealand Forest Research Institute (Scion), Rotorua, New Zealand.

Charles Shaw, Consultant, USA

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