| Legend |
|---|
| Justification for qualification based on EPPO PM 4 Standards |
| Justification for disqualification |
| Additional or non-conclusive information |
| Standard text |
NAME OF THE ORGANISM: Armillaria mellea (ARMIME)
GENERAL INFORMATION ON THE PEST
Name as submitted in the project specification (if different):
Pest category:
Fungi
1- Identity of the pest/Level of taxonomic listing:
Is the organism clearly a single taxonomic entity and can it be adequately distinguished from other entities of the same rank?
Yes
Is the pest defined at the species level or lower?:
Yes
Can listing of the pest at a taxonomic level higher than species be supported by scientific reasons or can species be identified within the taxonomic rank which are the (main) pests of concern?
- Not relevant: Fruits (including hops) sector
If necessary, please list the species:
-
Is it justified that the pest is listed at a taxonomic rank below species level?
Not relevant
Conclusion:
- Candidate: Fruits (including hops) sector
Justification (if necessary):
2 – Status in the EU:
Is this pest already a quarantine pest for the whole EU?
No
Presence in the EU:
Yes
List of countries (EPPO Global Database):
-
Conclusion:
Candidate
Justification (if necessary):
The pest is widespread in the EPPO region in particular in forests and in the environment where no phytosanitary measures are taken. GBIF includes reports from almost every EPPO country, but no reports from some areas of some Eastern Europe countries (https://www.gbif.org/fr/species/2536891).
HOST PLANT N°1: Juglans regia (IUGRE) for the Fruits (including hops) sector.
Origin of the listing:
Commission Implementing Directive (EU) 2014/98/EU and Commission Implementing Regulation (EU) 2019/2072
Plants for planting:
Plants intended for planting
3 - Is the pest already listed in a PM4 standard on the concerned host plant?
No
Conclusion:
Evaluation continues
Justification (if necessary):
In responses to the questionnaire, NL, PL and SI supported deregulation. NL and SI considered that plants for planting was not the 'main' pathway. NL and PL considered that economic impact was acceptable.
4 - Are the listed plants for planting the main* pathway for the "pest/host/intended use" combination? (*: significant compared to others):
No
Conclusion:
Not candidate
Justification:
Armillaria mellea has a wide host range (CABI 2021: Raabe, 1962); fig (Ficus carica, Papachatzis et al, 2008), walnut (Juglans regia, Baumgartner et al., 2013), apricot (Prunus armeniaca, UCARN, 2017) and peach (Prunus persica, Downer & Faber, 2019) can be hosts of / can suffer from Armillaria mellea.
The pathogen occurs in landscapes and urban soils as well as a natural pathogen in forests and on lands converted to farming (Downer & Faber, 2019). Armillaria mellea can spread though soil using rhizomorphs, a multicellular structure formed through the aggregation and interweaving of many hyphae (shoe-string-like surviving structures). Their appearance is similar to the roots of higher plants. The growth and distribution of A. mellea rhizomorphs are mainly located between 2.5 and 20 cm below the soil surface and are rare below 30 cm. Rhizomorphs grow slowly through the soil and searching for nutrients; disease foci can grow 0.2-2.5 m per year. When Armillaria mycelium/rhizomorph encounter the root, they start to grow epiphytically over the host root surface and produce branches of hyphae that grow into the tissues. Woody roots are more susceptible to infection by Armillaria spp. than the fine roots (Termorshuizen, 2000; Devkota & Hammerschmidt, 2020).
Once trees are infected, Armillaria spp. can also spread by root-to-root contact. This root-to-root infection results in the outward expansion of clusters of diseased trees as neighboring trees subsequently become infected (Termorshuizen, 2000).
New sites of infection also can become established in non-infested areas of the orchard by moving infected root pieces through cultivation, erosion gullies, and careless tree removal practices (Cox, 2004); or when plants that are infected, or contain soil infested with A. mellea are introduced (Termorshuizen, 2000).
Besides its parasitic behavior, Armillaria mellea can also persist as a saprophyte in the form of a mycelium, colonizing the dead roots and wood in the soil of e.g. orchards and timber plantations. The colonized and infected plant tissue or woody debris in soil serve as a long-term source of inoculum, colonizing and infecting the roots of new-planted trees through physical contact, which also increases the risk of mortality in the next rotation of trees. The saprophytic behavior enables the fungal inoculum residing inside the roots and wood to persist for many years in a forest stand (Kedves et al., 2021).
Armillaria mellea can also spread by basidiospores, although the spores are speculated to have low epidemiological importance relative to the infection by fungal rhizomorphs. Nevertheless, they are regarded as an important source of genetic variation within species and a means of long-distance dispersal. Difficulties in tracking the dispersal and establishment of windborne spores may have made it difficult to understand their absolute role in infection (Devkota & Hammerschmidt, 2020).
[In responses to the questionnaire, NL commented that the pest was 'airborne and widespread in nature'. NL and SI did not consider plants for planting as the main pathway.]
The Fruit SEWG agreed that plants for planting should not be considered as a significant pathway compared to other pathways: it only infects weak plants and the role of nursery plants in infections may not be significant. Although Armillaria mellea can spread by infected propagation material, the main risk is when planting orchards on land previously used for forestry (Armillaria mellea is a common disease in forests). Nevertheless, the Fruit SEWG highlighted the lack of measures available when the pest becomes present in an orchard.
The pathogen occurs in landscapes and urban soils as well as a natural pathogen in forests and on lands converted to farming (Downer & Faber, 2019). Armillaria mellea can spread though soil using rhizomorphs, a multicellular structure formed through the aggregation and interweaving of many hyphae (shoe-string-like surviving structures). Their appearance is similar to the roots of higher plants. The growth and distribution of A. mellea rhizomorphs are mainly located between 2.5 and 20 cm below the soil surface and are rare below 30 cm. Rhizomorphs grow slowly through the soil and searching for nutrients; disease foci can grow 0.2-2.5 m per year. When Armillaria mycelium/rhizomorph encounter the root, they start to grow epiphytically over the host root surface and produce branches of hyphae that grow into the tissues. Woody roots are more susceptible to infection by Armillaria spp. than the fine roots (Termorshuizen, 2000; Devkota & Hammerschmidt, 2020).
Once trees are infected, Armillaria spp. can also spread by root-to-root contact. This root-to-root infection results in the outward expansion of clusters of diseased trees as neighboring trees subsequently become infected (Termorshuizen, 2000).
New sites of infection also can become established in non-infested areas of the orchard by moving infected root pieces through cultivation, erosion gullies, and careless tree removal practices (Cox, 2004); or when plants that are infected, or contain soil infested with A. mellea are introduced (Termorshuizen, 2000).
Besides its parasitic behavior, Armillaria mellea can also persist as a saprophyte in the form of a mycelium, colonizing the dead roots and wood in the soil of e.g. orchards and timber plantations. The colonized and infected plant tissue or woody debris in soil serve as a long-term source of inoculum, colonizing and infecting the roots of new-planted trees through physical contact, which also increases the risk of mortality in the next rotation of trees. The saprophytic behavior enables the fungal inoculum residing inside the roots and wood to persist for many years in a forest stand (Kedves et al., 2021).
Armillaria mellea can also spread by basidiospores, although the spores are speculated to have low epidemiological importance relative to the infection by fungal rhizomorphs. Nevertheless, they are regarded as an important source of genetic variation within species and a means of long-distance dispersal. Difficulties in tracking the dispersal and establishment of windborne spores may have made it difficult to understand their absolute role in infection (Devkota & Hammerschmidt, 2020).
[In responses to the questionnaire, NL commented that the pest was 'airborne and widespread in nature'. NL and SI did not consider plants for planting as the main pathway.]
The Fruit SEWG agreed that plants for planting should not be considered as a significant pathway compared to other pathways: it only infects weak plants and the role of nursery plants in infections may not be significant. Although Armillaria mellea can spread by infected propagation material, the main risk is when planting orchards on land previously used for forestry (Armillaria mellea is a common disease in forests). Nevertheless, the Fruit SEWG highlighted the lack of measures available when the pest becomes present in an orchard.
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Yes
Justification:
The fungus infects many orchard trees, including walnut, peach, and almond, as well as grape and many woody landscape plants (e.g., rose). Armillaria root rot does not affect as many acres as do some other fungal diseases, but where it does occur, it is extremely difficult to eradicate from the soil and reduces yields throughout the life of an infected vineyard or orchards and that of successive plantings (Baumgartner & Rizzo, 2013). In southern France and California the damage on stone fruits (peaches, almonds, apricots, cherries) and walnuts can be severe. Unfortunately, few quantitative data are available concerning the overall mortality rates in orchards and vineyards (CABI, 2021)
Juglans regia:
The severity of this fungus disease depends on the rootstock and the strain of A. mellea. The pathogen invades the roots, crown and basal trunk, eventually girdling the crown region and destroying the entire root system causing death of the tree. Symptoms of the disease are creamy white, fan-shaped plaques of fungal mycelia beneath the bark. After rains in the fall or spring, a cluster of mushrooms often appears at the base of infected trees. The fungus develops most rapidly in moist cool soil. It can survive for many years in dead or living roots of many different species of trees. Generally, clusters of trees may be infected at one or several sites in the orchard. A localized problem but can cause 25% yield loss in infected orchards (UCARN, 1998). However there are conflicting reports on the impact of Armillaria mellea on walnut, which suggests that there may be a great deal of variation between walnut species, pathogen strain and environment. Walnut on rootstock ‘Paradox’ seemed to survive better than its parents (McGranahan & Leslie, 1990); ‘Pradox’ is a hybrid of J. hindsii and J. regia, and is more vigorous (Baumgartner et al., 2013).
[In responses to the questionnaire, NL commented that infection during pruning was only causing damage on weak plants. PL considered damage negligeable.]
Juglans regia:
The severity of this fungus disease depends on the rootstock and the strain of A. mellea. The pathogen invades the roots, crown and basal trunk, eventually girdling the crown region and destroying the entire root system causing death of the tree. Symptoms of the disease are creamy white, fan-shaped plaques of fungal mycelia beneath the bark. After rains in the fall or spring, a cluster of mushrooms often appears at the base of infected trees. The fungus develops most rapidly in moist cool soil. It can survive for many years in dead or living roots of many different species of trees. Generally, clusters of trees may be infected at one or several sites in the orchard. A localized problem but can cause 25% yield loss in infected orchards (UCARN, 1998). However there are conflicting reports on the impact of Armillaria mellea on walnut, which suggests that there may be a great deal of variation between walnut species, pathogen strain and environment. Walnut on rootstock ‘Paradox’ seemed to survive better than its parents (McGranahan & Leslie, 1990); ‘Pradox’ is a hybrid of J. hindsii and J. regia, and is more vigorous (Baumgartner et al., 2013).
[In responses to the questionnaire, NL commented that infection during pruning was only causing damage on weak plants. PL considered damage negligeable.]
What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
Major
Is the economic impact due to the presence of the pest on the named host plant for planting, acceptable to the propagation and end user sectors concerned?
Is there unacceptable economic impact caused to other hosts (or the same host with a different intended use) produced at the same place of production due to the transfer of the pest from the named host plant for planting?
Conclusion:
Justification:
Remark: Once there, management options for Armillaria root rot are extremely limited, since Armillaria can survive in infected root pieces for decades, crop rotation has very little effect in reducing inoculum potential.
6 - Are there feasible and effective measures available to prevent the presence of the pest on the plants for planting at an incidence above a certain threshold (including zero) to avoid an unacceptable economic impact as regards the relevant host plants?
Conclusion:
Justification:
Choice of site for planting: Sites can be hazardous either because they can predispose the host in some way, or because the inoculum potential of pathogenic Armillaria species is likely to be important. The sites of recent deforestation are particularly risky, depending also on the composition of the natural vegetation (CABI 2021).
Preparation of site: Stump and root removal is commonly practiced in preparing sites for plantation of fruit orchards. Several rippings at different depths (possibly including subsoiling) are followed by hand removal of the remaining roots. (CABI, 2021). If Prunus persica was planted as grafted saplings in a previously infested plot with Armillaria mellea, survival of trees planted in a large hole were more likely to survive than in a smaller hole (P=0.07) and trees in large holes with fresh organic matter added were the most likely to survive (P=0.04) (Downer & Faber, 2019).
Choice of rootstock: For apricot some rootstock are more resistant to Armillaria mellea than others, but they are not immune (UCANR, 2017). Also for walnut research for tolerant/resistant rootstocks is ongoing (Baumgartner et al., 2013).
Cultural control: If the disease is caught early enough, excavating the soil around the base of the tree down to the first layer of lateral roots may delay the progress of the disease from progressing further. This aeration prevents the fungus from gaining access to the crown of the tree (UCANR, 2017).
Preparation of site: Stump and root removal is commonly practiced in preparing sites for plantation of fruit orchards. Several rippings at different depths (possibly including subsoiling) are followed by hand removal of the remaining roots. (CABI, 2021). If Prunus persica was planted as grafted saplings in a previously infested plot with Armillaria mellea, survival of trees planted in a large hole were more likely to survive than in a smaller hole (P=0.07) and trees in large holes with fresh organic matter added were the most likely to survive (P=0.04) (Downer & Faber, 2019).
Choice of rootstock: For apricot some rootstock are more resistant to Armillaria mellea than others, but they are not immune (UCANR, 2017). Also for walnut research for tolerant/resistant rootstocks is ongoing (Baumgartner et al., 2013).
Cultural control: If the disease is caught early enough, excavating the soil around the base of the tree down to the first layer of lateral roots may delay the progress of the disease from progressing further. This aeration prevents the fungus from gaining access to the crown of the tree (UCANR, 2017).
7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
Conclusion:
Justification:
CONCLUSION ON THE STATUS:
Disqualified: plants for planting is not considered to be a significant pathway
8 - Tolerance level:
Is there a need to change the Tolerance level:
Yes
Proposed Tolerance levels:
Delisting
9 - Risk management measures:
Is there a need to change the Risk management measure:
Yes
Proposed Risk management measure:
Delisting
REFERENCES:
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- Baumgartner K, Fujiyoshi P & Browne GT (2013). Evaluating Paradox walnut rootstocks for resistance to Armillaria root disease. Hortscience 48(1), 68–72. 2013.
- CABI (2021) Armillaria mellea (armillaria root rot). Crop protection compendium. CABI Compendium
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- Cox KD (2004) Armillaria root rot of peach: detection of residual inoculum, biochemical characterization, and interspecies competition. PhD Thesis, University of Georgia, Athens. 164 pp.
- Devkota P & Hammerschmidt R (2020) The Infection process of Armillaria mellea and Armillaria solidipes. Physiological and Molecular Plant Pathology 112(4), 101543. DOI: 10.1016/j.pmpp.2020.101543
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