Regulated Non-Quarantine Projects

Two EU funded projects for the benefit of the whole EPPO region

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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: Corylus avellana (CYLAV) 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?
 
Yes
 
Conclusion:
 
Evaluation continues

 
Justification (if necessary):
 
Inspection for 'Armillariella mellea' is recommended in EPPO Standard PM 4-31 Certification scheme for hazelnut. Any plant found to be infected should be recorded and immediately removed. However, in responses to the questionnaire, NL, PL and SI supported deregulation. NL and SI considered that plants for planting was not the 'main' pathway, whereas PL considered that economic impact was acceptable. Evaluation continues on pathway and economic impact.

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, also known as oak root rot or honey fungus, has a wide host range (CABI 2021: Raabe, 1962), Corylus avellana can be a host of Armillaria mellea (Guerrero et al., 2014).
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, A. 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).
Although A. mellea can spread by infected propagation material, however the major issue is planting orchards on land previously used for forestry (A. mellea is a common disease in forests).
[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?
 

Justification:
 
There is little information on Armillaria mellea affecting Corylus avellana. Guerrero et al. (2021) reports that the pathogen can be occasionally detected in individual hazelnut trees in soil where other susceptible tree species were present. It can spread by contact between diseased and healthy plants.
[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)
 

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:
 

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:
 

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:
  • Anselmi N, Saraceni A & Anselmi A (2021) Incidence of Armillaria species in agrarian, forest and ornamental ecosystems of the Lazio region. Agriculture & Forestry/Poljoprivreda i šumarstv 67(1).
  • Caruso FL (2017) Armillaria root rot. In Compendium of Blueberry, Cranberry, and Lingonberry Diseases and Pests 2nd edition (eds Polashock JJ, Caruso FL, Averill AL & Schilder AC). American Phytopathological Society, St Paul, MN, USA. pages 12-13.
  • 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
  • Downer J & Faber B (2019) Non-chemical control of Armillaria mellea infection of Prunus persica. Journal of Plant Science and Phytopathology 3, 050-055. https://doi.org/10.29328/journal.jpsp.1001031.
  • Guerrero JC, Pérez SF, Ferrada EQ, Cona LQ & Bensch ET (2014) Phytopathogens of hazelnut (Corylus avellana L.) in southern Chile. Acta Horticulturae 1052, 269-274.
  • Kedves O, Shahab D, Champramary S, Chen L, Indic B, Bóka B, Nagy VD, Vágvölgyi C, Kredics L & Sipos G (2021) Epidemiology, biotic interactions and biological control of Armillarioids in the Northern Hemisphere. Pathogens 10(1), 76. ttps://doi.org/10.3390/pathogens10010076
  • Palmieri L, Prodorutti D, Gobbin D, Pertot I & Gessler C (2006). Role of barks used in highbush blueberry mulching on Armillaria spp. infections. [Italian] Giornate Fitopatologiche, Riccione (RN), 27-29 marzo 2006. Atti, volume secondo. 301-306.
  • Prodorutti D, Vanblaere T, Gobbin D, Pellegrini A, Gessler C & Pertot I (2009) Genetic diversity of Armillaria spp. infecting highbush blueberry in Northern Italy (Trentino Region). Phytopathology 99(6), 651-658.
  • Raabe (1962). Host list of root rot fungus Armillaria mellea. Hilgardia 33 nr. 2
  • Raabe RD (2008) Plants resistant or susceptible to Armillaria mellea, the oak root fungus. University of California, Berkeley. https://alamedabackyardgrowers. org/wp-content/uploads/2019/01/List-of-Oak-Root-Fungus-Resistant-or-Susceptible-Trees-Plants. pdf.[accessed 28 Jul 2023].
  • Raziq F & Fox RTV (2006). The integrated control of Armillaria mellea 2. Field experiments. Biological agriculture & horticulture 23(3), 235-249.
  • Schnabel G (2017). Armillaria root rot. In Compendium of Apple and Pear Diseases and Pests 2nd edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, MN, USA. pages 70-71.
  • Termorshuizen AJ (2000) Ecology and epidemiology of Armillaria. In Armillaria Root Rot: Biology and Control of Honey Fungus (ed Fox RTV). Andover, Intercept, Pages 115-131.
  • Thomidis T & Exadaktylou E (2012) Effectiveness of cyproconazole to control Armillaria root rot of apple, walnut and kiwifruit. Crop Protection 36, 49-51.
  • UC PMG (2017a) Armillaria root rot (oak root fungus). In Apple - Pest management guidelines for agriculture. University of California Agriculture and Natural Resources, UC IPM Pest Management Guidelines: UC ANR Publication 3432 page 72.
  • UC PMG (2017b) Armillaria root and crown rot (oak root fungus). In Pear - Pest management guidelines for agriculture. University of California Agriculture and Natural Resources, UC IPM Pest Management Guidelines: UC ANR Publication 3455 page 78-79.

HOST PLANT N°2: Cydonia oblonga (CYDOB) 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?
 
Yes
 
Conclusion:
 
Evaluation continues

 
Justification (if necessary):
 
Inspection for Armillaria mellea recommended in EPPO Standard PM 4-27 Pathogen-tested material of Malus, Pyrus and Cydonia. However, 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. Evaluation continues on pathway and economic impact.

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, also known as honey fungus or oak root fungus, has a wide host range (CABI 2021; Raabe, 1962); although both citations list Cydonia oblonga as a host, little information on infection of this host is available.
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, A. 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).
Although A. mellea can spread by infected propagation material, however the major issue is planting orchards on land previously used for forestry (A. mellea is a common disease in forests).
[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?
 
No

Justification:
 
No information on damage. Raabe (2008) lists quince is moderately resistant to Armillaria mellea.
[In responses to the questionnaire, NL commented that infection during pruning was only causing damage on weak plants.]

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 

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:
 

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:
 

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:
  • Anselmi N, Saraceni A & Anselmi A (2021) Incidence of Armillaria species in agrarian, forest and ornamental ecosystems of the Lazio region. Agriculture & Forestry/Poljoprivreda i šumarstv 67(1).
  • Caruso FL (2017) Armillaria root rot. In Compendium of Blueberry, Cranberry, and Lingonberry Diseases and Pests 2nd edition (eds Polashock JJ, Caruso FL, Averill AL & Schilder AC). American Phytopathological Society, St Paul, MN, USA. pages 12-13.
  • 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
  • Downer J & Faber B (2019) Non-chemical control of Armillaria mellea infection of Prunus persica. Journal of Plant Science and Phytopathology 3, 050-055. https://doi.org/10.29328/journal.jpsp.1001031.
  • Guerrero JC, Pérez SF, Ferrada EQ, Cona LQ & Bensch ET (2014) Phytopathogens of hazelnut (Corylus avellana L.) in southern Chile. Acta Horticulturae 1052, 269-274.
  • Kedves O, Shahab D, Champramary S, Chen L, Indic B, Bóka B, Nagy VD, Vágvölgyi C, Kredics L & Sipos G (2021) Epidemiology, biotic interactions and biological control of Armillarioids in the Northern Hemisphere. Pathogens 10(1), 76. ttps://doi.org/10.3390/pathogens10010076
  • Palmieri L, Prodorutti D, Gobbin D, Pertot I & Gessler C (2006). Role of barks used in highbush blueberry mulching on Armillaria spp. infections. [Italian] Giornate Fitopatologiche, Riccione (RN), 27-29 marzo 2006. Atti, volume secondo. 301-306.
  • Prodorutti D, Vanblaere T, Gobbin D, Pellegrini A, Gessler C & Pertot I (2009) Genetic diversity of Armillaria spp. infecting highbush blueberry in Northern Italy (Trentino Region). Phytopathology 99(6), 651-658.
  • Raabe (1962). Host list of root rot fungus Armillaria mellea. Hilgardia 33 nr. 2
  • Raabe RD (2008) Plants resistant or susceptible to Armillaria mellea, the oak root fungus. University of California, Berkeley. https://alamedabackyardgrowers. org/wp-content/uploads/2019/01/List-of-Oak-Root-Fungus-Resistant-or-Susceptible-Trees-Plants. pdf.[accessed 28 Jul 2023].
  • Raziq F & Fox RTV (2006). The integrated control of Armillaria mellea 2. Field experiments. Biological agriculture & horticulture 23(3), 235-249.
  • Schnabel G (2017). Armillaria root rot. In Compendium of Apple and Pear Diseases and Pests 2nd edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, MN, USA. pages 70-71.
  • Termorshuizen AJ (2000) Ecology and epidemiology of Armillaria. In Armillaria Root Rot: Biology and Control of Honey Fungus (ed Fox RTV). Andover, Intercept, Pages 115-131.
  • Thomidis T & Exadaktylou E (2012) Effectiveness of cyproconazole to control Armillaria root rot of apple, walnut and kiwifruit. Crop Protection 36, 49-51.
  • UC PMG (2017a) Armillaria root rot (oak root fungus). In Apple - Pest management guidelines for agriculture. University of California Agriculture and Natural Resources, UC IPM Pest Management Guidelines: UC ANR Publication 3432 page 72.
  • UC PMG (2017b) Armillaria root and crown rot (oak root fungus). In Pear - Pest management guidelines for agriculture. University of California Agriculture and Natural Resources, UC IPM Pest Management Guidelines: UC ANR Publication 3455 page 78-79.

HOST PLANT N°3: Ficus carica (FIUCA) 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. 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.

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)
Ficus carica:
Armillaria mellea was observed as an aggressive rot pathogens of Ficus carica cultivar (Smyrna) in central Greece. It caused fig rot root (together with Rosellinia necatrix), stressed old trees and killed young plants. Common symptoms shown by infected trees were, yellowing of the leaves, early leaf fall, premature autumn color, splitting of the bark, plant defoliation and plant death. Infections are common in fig cultivars near the forest (Papachatzis et al., 2008).
[In responses to the questionnaire, NL commented that infection during pruning was only causing damage on weak plants.]

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).

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:
  • Baumgartner K & Rizzo DM (2013). Armillaria root rot. In Grape pest management, 3rd edition (ed Bettia L) CA: University of California, Division of Agriculture and Natural Resources, Oakland, pages 83-86.
  • 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
  • https://doi.org/10.1079/cabicompendium.7002 (accessed on 8/Apr/2024).
  • Chandelier A, Gerarts F, San Martin G, Herman M & Delahaye L (2016) Temporal evolution of collar lesions associated with ash dieback and the occurrence of Armillaria in Belgian forests. Forest Pathology 46(4), 289-297.
  • 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
  • Dowding P & Smith L (2008) Forest fungi In Ireland. COFORD, Dublin.
  • Downer J & Faber B (2019) Non-chemical control of Armillaria mellea infection of Prunus persica. Journal of Plant Science and Phytopathology 3, 050-055. https://doi.org/10.29328/journal.jpsp.1001031
  • Georgieva M, Georgieva M, Hristova M, Georgiev G (2023) Assessment of plane trees health status in urban green areas of Sofia, Bulgaria. Ecologia Balkanica 15(1), 117-125.
  • Ivić D, Petrović E & Godena S (2023) Fungi associated with canker diseases on olive in Istria (Croatia). Journal of Central European Agriculture 24(2), 470-475.
  • Jankovský L (2003) Distribution and ecology of Armillaria species in some habitats of southern Moravia, Czech Republic. Czech Mycology 55(3-4), 173-186.
  • Kedves O, Shahab D, Champramary S, Chen L, Indic B, Bóka B, Nagy VD, Vágvölgyi C, Kredics L & Sipos G (2021) Epidemiology, biotic interactions and biological control of Armillarioids in the Northern Hemisphere. Pathogens 10(1), 76. https://doi.org/10.3390/pathogens10010076.
  • Łakomy P (2006) New location of Armillaria mellea in polish forests. mp was rolled down. Phytopathologia Polonica 41, 83–86.
  • Liesebach M, Schüler S & Weissenbacher L (2008). Herkunftsversuche der Küstentanne (Abies grandis [D. Don] Lindl.) in Österreich - Eignung, Wuchsleistung und Variation. Austrian Journal of Forest Science 125(3), 183-200.
  • McGranahan GH & Leslie CA (1990). Walnuts (Juglans). In Genetic resources of fruit and nut crops (eds Moore JN & Ballington JR) Volume 2. Acta Horticulturae 290, 907–951.
  • Marxmüller H, Holdenrieder O & Müller ED (1990). Zur Verbreitung, Phönologie und Ökologie von Armillaria mellea s.l. in Südbayern. Bericht Bayerischer Botanischer Gesellschaft, 61:115-134. https://www.zobodat.at/pdf/Berichte-Bayerischen-Bot-Ges-Erforschung-Flora_61_0115-0134.pdf
  • Mesanza N, Patten CL & Iturritxa E (2017) Distribution and characterization of Armillaria complex in Atlantic Forest Ecosystems of Spain. Forests 2017, 8(7), 235; https://doi.org/10.3390/f8070235
  • NDFF (2024) NDFF Verspreidingsatlas, NMV verspreidingsatlas paddenstoelen, Armillaria mellea (Vahl) P. Kumm. https://www.verspreidingsatlas.nl/0005040 (accessed 19/Mar/2024).
  • Papachatzis A, Eliopoulos P, Statharas G & Vagelas I (2008) Ficus carica rot rot disease caused by Armillaria mellea and Rosellinia necatrix in Greece. Universitatea Din Craiova (University Of Craiova) XIII (XLIX), 143-148.
  • Raabe (1962). Host list of root rot fungus Armillaria mellea. Hilgardia 33 nr. 2
  • Romagnesi H, 1973. Observations sur les Armillariella - II. Bulletin de la Société Mycologique de France, 89:195-206.
  • Termorshuizen AJ (2000). Ecology and epidemiology of Armillaria. In Armillaria Root Rot: Biology and Control of Honey Fungus (ed Fox RTV). Andover, Intercept, Pages 115-131.
  • Termorshuizen AJ & Arnolds EJM (1994). Geographical distribution of the Armillaria species in the Netherlands in relation to soil type and hosts. European Journal of Forest Pathology 24(3), 129-136.
  • UCANR (1998) Crop Profile for Walnuts in California. University of California Agriculture and Natural Resources. https://ucanr.edu/datastoreFiles/391-47.pdf
  • UCANR (2017) Apricot. Pest management guidelines for agriculture. University of California Agriculture and Natural Resources, UC IPM Pest Management Guidelines: Apricot, UC ANR Publication 3433. https://ipm.ucanr.edu/legacy_assets/pdf/pmg/pmgapricot.pdf (last accessed 24/Apr/2024)

HOST PLANT N°4: 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.

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.]

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).

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:
  • Baumgartner K & Rizzo DM (2013). Armillaria root rot. In Grape pest management, 3rd edition (ed Bettia L) CA: University of California, Division of Agriculture and Natural Resources, Oakland, pages 83-86.
  • 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
  • https://doi.org/10.1079/cabicompendium.7002 (accessed on 8/Apr/2024).
  • Chandelier A, Gerarts F, San Martin G, Herman M & Delahaye L (2016) Temporal evolution of collar lesions associated with ash dieback and the occurrence of Armillaria in Belgian forests. Forest Pathology 46(4), 289-297.
  • 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
  • Dowding P & Smith L (2008) Forest fungi In Ireland. COFORD, Dublin.
  • Downer J & Faber B (2019) Non-chemical control of Armillaria mellea infection of Prunus persica. Journal of Plant Science and Phytopathology 3, 050-055. https://doi.org/10.29328/journal.jpsp.1001031
  • Georgieva M, Georgieva M, Hristova M, Georgiev G (2023) Assessment of plane trees health status in urban green areas of Sofia, Bulgaria. Ecologia Balkanica 15(1), 117-125.
  • Ivić D, Petrović E & Godena S (2023) Fungi associated with canker diseases on olive in Istria (Croatia). Journal of Central European Agriculture 24(2), 470-475.
  • Jankovský L (2003) Distribution and ecology of Armillaria species in some habitats of southern Moravia, Czech Republic. Czech Mycology 55(3-4), 173-186.
  • Kedves O, Shahab D, Champramary S, Chen L, Indic B, Bóka B, Nagy VD, Vágvölgyi C, Kredics L & Sipos G (2021) Epidemiology, biotic interactions and biological control of Armillarioids in the Northern Hemisphere. Pathogens 10(1), 76. https://doi.org/10.3390/pathogens10010076.
  • Łakomy P (2006) New location of Armillaria mellea in polish forests. mp was rolled down. Phytopathologia Polonica 41, 83–86.
  • Liesebach M, Schüler S & Weissenbacher L (2008). Herkunftsversuche der Küstentanne (Abies grandis [D. Don] Lindl.) in Österreich - Eignung, Wuchsleistung und Variation. Austrian Journal of Forest Science 125(3), 183-200.
  • McGranahan GH & Leslie CA (1990). Walnuts (Juglans). In Genetic resources of fruit and nut crops (eds Moore JN & Ballington JR) Volume 2. Acta Horticulturae 290, 907–951.
  • Marxmüller H, Holdenrieder O & Müller ED (1990). Zur Verbreitung, Phönologie und Ökologie von Armillaria mellea s.l. in Südbayern. Bericht Bayerischer Botanischer Gesellschaft, 61:115-134. https://www.zobodat.at/pdf/Berichte-Bayerischen-Bot-Ges-Erforschung-Flora_61_0115-0134.pdf
  • Mesanza N, Patten CL & Iturritxa E (2017) Distribution and characterization of Armillaria complex in Atlantic Forest Ecosystems of Spain. Forests 2017, 8(7), 235; https://doi.org/10.3390/f8070235
  • NDFF (2024) NDFF Verspreidingsatlas, NMV verspreidingsatlas paddenstoelen, Armillaria mellea (Vahl) P. Kumm. https://www.verspreidingsatlas.nl/0005040 (accessed 19/Mar/2024).
  • Papachatzis A, Eliopoulos P, Statharas G & Vagelas I (2008) Ficus carica rot rot disease caused by Armillaria mellea and Rosellinia necatrix in Greece. Universitatea Din Craiova (University Of Craiova) XIII (XLIX), 143-148.
  • Raabe (1962). Host list of root rot fungus Armillaria mellea. Hilgardia 33 nr. 2
  • Romagnesi H, 1973. Observations sur les Armillariella - II. Bulletin de la Société Mycologique de France, 89:195-206.
  • Termorshuizen AJ (2000). Ecology and epidemiology of Armillaria. In Armillaria Root Rot: Biology and Control of Honey Fungus (ed Fox RTV). Andover, Intercept, Pages 115-131.
  • Termorshuizen AJ & Arnolds EJM (1994). Geographical distribution of the Armillaria species in the Netherlands in relation to soil type and hosts. European Journal of Forest Pathology 24(3), 129-136.
  • UCANR (1998) Crop Profile for Walnuts in California. University of California Agriculture and Natural Resources. https://ucanr.edu/datastoreFiles/391-47.pdf
  • UCANR (2017) Apricot. Pest management guidelines for agriculture. University of California Agriculture and Natural Resources, UC IPM Pest Management Guidelines: Apricot, UC ANR Publication 3433. https://ipm.ucanr.edu/legacy_assets/pdf/pmg/pmgapricot.pdf (last accessed 24/Apr/2024)

HOST PLANT N°5: Malus (1MABG) 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?
 
Yes
 
Conclusion:
 
Evaluation continues

 
Justification (if necessary):
 
Inspection for Armillaria mellea recommended in EPPO Standard PM 4-27 Pathogen-tested material of Malus, Pyrus and Cydonia. However, in responses to the questionnaire, NL, PL and SI supported deregulation. NL and SI considered that plants for planting was not the 'main' pathway, whereas PL considered that economic impact was acceptable. Evaluation continues on pathway and economic impact.

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, also known as honey fungus or oak root fungus, has a wide host range (CABI 2021; Raabe, 1962). Malus domestica can be a host (Raziq & Fox, 2006; Thomidis & Exadaktylou, 2012; UC PMG, 2017); Raabe (2008) lists some Malus spp. as resistant to honey fungus, others as moderately resistant or susceptible.
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, A. 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).
Although A. mellea can spread by infected propagation material, however the major issue is planting orchards on land previously used for forestry (A. mellea is a common disease in forests).[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?
 

Justification:
 
Although Armillaria mellea is a significant problem in e.g. forestry, it is not of major economic importance on apple and pear The pathogen is most likely to be found in orchards established on recently cleared woodlands with well-drained sandy of clay soil (Schnabel, 2017).
Apple roots infected with Armillaria mellea have white to yellowish fan-shaped mycelial mats between the bark and the wood. Dark brown to black rhizomorphs sometimes can be seen on the root surface. Apple rootstocks have some resistance to Armillaria, but if the level of inoculum is high in the soil and the strain of Armillaria is highly virulent, or the tree is already weakened by some other factor, the fungus can overcome this resistance (UC PMG, 2017).
[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)
 

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:
 

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:
 

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:
  • Anselmi N, Saraceni A & Anselmi A (2021) Incidence of Armillaria species in agrarian, forest and ornamental ecosystems of the Lazio region. Agriculture & Forestry/Poljoprivreda i šumarstv 67(1).
  • Caruso FL (2017) Armillaria root rot. In Compendium of Blueberry, Cranberry, and Lingonberry Diseases and Pests 2nd edition (eds Polashock JJ, Caruso FL, Averill AL & Schilder AC). American Phytopathological Society, St Paul, MN, USA. pages 12-13.
  • 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
  • Downer J & Faber B (2019) Non-chemical control of Armillaria mellea infection of Prunus persica. Journal of Plant Science and Phytopathology 3, 050-055. https://doi.org/10.29328/journal.jpsp.1001031.
  • Guerrero JC, Pérez SF, Ferrada EQ, Cona LQ & Bensch ET (2014) Phytopathogens of hazelnut (Corylus avellana L.) in southern Chile. Acta Horticulturae 1052, 269-274.
  • Kedves O, Shahab D, Champramary S, Chen L, Indic B, Bóka B, Nagy VD, Vágvölgyi C, Kredics L & Sipos G (2021) Epidemiology, biotic interactions and biological control of Armillarioids in the Northern Hemisphere. Pathogens 10(1), 76. ttps://doi.org/10.3390/pathogens10010076
  • Palmieri L, Prodorutti D, Gobbin D, Pertot I & Gessler C (2006). Role of barks used in highbush blueberry mulching on Armillaria spp. infections. [Italian] Giornate Fitopatologiche, Riccione (RN), 27-29 marzo 2006. Atti, volume secondo. 301-306.
  • Prodorutti D, Vanblaere T, Gobbin D, Pellegrini A, Gessler C & Pertot I (2009) Genetic diversity of Armillaria spp. infecting highbush blueberry in Northern Italy (Trentino Region). Phytopathology 99(6), 651-658.
  • Raabe (1962) Host list of root rot fungus Armillaria mellea. Hilgardia 33 nr. 2
  • Raabe RD (2008) Plants resistant or susceptible to Armillaria mellea, the oak root fungus. University of California, Berkeley. https://alamedabackyardgrowers. org/wp-content/uploads/2019/01/List-of-Oak-Root-Fungus-Resistant-or-Susceptible-Trees-Plants. pdf.[accessed 28 Jul 2023].
  • Raziq F & Fox RTV (2006) The integrated control of Armillaria mellea 2. Field experiments. Biological agriculture & horticulture 23(3), 235-249.
  • Schnabel G (2017). Armillaria root rot. In Compendium of Apple and Pear Diseases and Pests 2nd edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, MN, USA. pages 70-71.
  • Termorshuizen AJ (2000) Ecology and epidemiology of Armillaria. In Armillaria Root Rot: Biology and Control of Honey Fungus (ed Fox RTV). Andover, Intercept, Pages 115-131.
  • Thomidis T & Exadaktylou E (2012) Effectiveness of cyproconazole to control Armillaria root rot of apple, walnut and kiwifruit. Crop Protection 36, 49-51.
  • UC PMG (2017a) Armillaria root rot (oak root fungus). In Apple - Pest management guidelines for agriculture. University of California Agriculture and Natural Resources, UC IPM Pest Management Guidelines: UC ANR Publication 3432 page 72.
  • UC PMG (2017b) Armillaria root and crown rot (oak root fungus). In Pear - Pest management guidelines for agriculture. University of California Agriculture and Natural Resources, UC IPM Pest Management Guidelines: UC ANR Publication 3455 page 78-79.

HOST PLANT N°6: Prunus armeniaca (PRNAR) for the Fruits (including hops) sector.


Origin of the listing:
 
New proposal

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):
 
Remark: the assessment performed covers the given host species as well as interspecific hybrids with other Prunus species.

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.

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)
Prunus armeniaca / Prunus persica
Affected trees often show a general decline in vigour a year or more before the entire tree collapses. Trees often die in circular areas within an orchard; the circular area expands each year as the fungus grows along roots of infected trees to roots of adjacent healthy trees. Tree death usually occurs in late spring. Aboveground symptoms can be easily confused with any other root problem. All stone fruit rootstocks are susceptible to Armillaria root rot. Generally, once an apricot tree (or any other tree) becomes infected with Armillaria mellea, it cannot be saved and should be removed (UCARN, 2017).

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 
Medium

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:
 
Remarks: 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. In France, professional operators can bear the current level of presence in fields (with no regulation in place) but they worry about the possible spreading of this pest due to infested plant material. Production period for Prunus is earlier in the season than for nuts, figs or pome fruits, allowing earlier detection, managing the pest earlier in the season (Infected plants are destroyed and soil removed), and consequently causing less impact. Further research programs on resistant rootstocks are requested by producers.

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).

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:
 
No (new regulation proposal)

Proposed Tolerance levels:
 
No listing.

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
No

Proposed Risk management measure:
 
No listing.


REFERENCES:
  • Baumgartner K & Rizzo DM (2013). Armillaria root rot. In Grape pest management, 3rd edition (ed Bettia L) CA: University of California, Division of Agriculture and Natural Resources, Oakland, pages 83-86.
  • 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
  • https://doi.org/10.1079/cabicompendium.7002 (accessed on 8/Apr/2024).
  • Chandelier A, Gerarts F, San Martin G, Herman M & Delahaye L (2016) Temporal evolution of collar lesions associated with ash dieback and the occurrence of Armillaria in Belgian forests. Forest Pathology 46(4), 289-297.
  • 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
  • Dowding P & Smith L (2008) Forest fungi In Ireland. COFORD, Dublin.
  • Downer J & Faber B (2019) Non-chemical control of Armillaria mellea infection of Prunus persica. Journal of Plant Science and Phytopathology 3, 050-055. https://doi.org/10.29328/journal.jpsp.1001031
  • Guillaumin JJ, Pierson J & Grassely C (1991) The susceptibility to Armillaria mellea of different Prunus species used as stone fruit rootstocks. Scientia Horticulturae 46, 43-54.
  • Georgieva M, Georgieva M, Hristova M, Georgiev G (2023) Assessment of plane trees health status in urban green areas of Sofia, Bulgaria. Ecologia Balkanica 15(1), 117-125.
  • Ivić D, Petrović E & Godena S (2023) Fungi associated with canker diseases on olive in Istria (Croatia). Journal of Central European Agriculture 24(2), 470-475.
  • Jankovský L (2003) Distribution and ecology of Armillaria species in some habitats of southern Moravia, Czech Republic. Czech Mycology 55(3-4), 173-186.
  • Kedves O, Shahab D, Champramary S, Chen L, Indic B, Bóka B, Nagy VD, Vágvölgyi C, Kredics L & Sipos G (2021) Epidemiology, biotic interactions and biological control of Armillarioids in the Northern Hemisphere. Pathogens 10(1), 76. https://doi.org/10.3390/pathogens10010076.
  • Łakomy P (2006) New location of Armillaria mellea in polish forests. mp was rolled down. Phytopathologia Polonica 41, 83–86.
  • Liesebach M, Schüler S & Weissenbacher L (2008). Herkunftsversuche der Küstentanne (Abies grandis [D. Don] Lindl.) in Österreich - Eignung, Wuchsleistung und Variation. Austrian Journal of Forest Science 125(3), 183-200.
  • McGranahan GH & Leslie CA (1990). Walnuts (Juglans). In Genetic resources of fruit and nut crops (eds Moore JN & Ballington JR) Volume 2. Acta Horticulturae 290, 907–951.
  • Marxmüller H, Holdenrieder O & Müller ED (1990). Zur Verbreitung, Phönologie und Ökologie von Armillaria mellea s.l. in Südbayern. Bericht Bayerischer Botanischer Gesellschaft, 61:115-134. https://www.zobodat.at/pdf/Berichte-Bayerischen-Bot-Ges-Erforschung-Flora_61_0115-0134.pdf
  • Mesanza N, Patten CL & Iturritxa E (2017) Distribution and characterization of Armillaria complex in Atlantic Forest Ecosystems of Spain. Forests 2017, 8(7), 235; https://doi.org/10.3390/f8070235
  • NDFF (2024) NDFF Verspreidingsatlas, NMV verspreidingsatlas paddenstoelen, Armillaria mellea (Vahl) P. Kumm. https://www.verspreidingsatlas.nl/0005040 (accessed 19/Mar/2024).
  • Papachatzis A, Eliopoulos P, Statharas G & Vagelas I (2008) Ficus carica rot rot disease caused by Armillaria mellea and Rosellinia necatrix in Greece. Universitatea Din Craiova (University Of Craiova) XIII (XLIX), 143-148.
  • Raabe (1962). Host list of root rot fungus Armillaria mellea. Hilgardia 33 nr. 2
  • Romagnesi H, 1973. Observations sur les Armillariella - II. Bulletin de la Société Mycologique de France, 89:195-206.
  • Termorshuizen AJ (2000). Ecology and epidemiology of Armillaria. In Armillaria Root Rot: Biology and Control of Honey Fungus (ed Fox RTV). Andover, Intercept, Pages 115-131.
  • Termorshuizen AJ & Arnolds EJM (1994). Geographical distribution of the Armillaria species in the Netherlands in relation to soil type and hosts. European Journal of Forest Pathology 24(3), 129-136.
  • UCANR (1998) Crop Profile for Walnuts in California. University of California Agriculture and Natural Resources. https://ucanr.edu/datastoreFiles/391-47.pdf
  • UCANR (2017) Apricot. Pest management guidelines for agriculture. University of California Agriculture and Natural Resources, UC IPM Pest Management Guidelines: Apricot, UC ANR Publication 3433. https://ipm.ucanr.edu/legacy_assets/pdf/pmg/pmgapricot.pdf (last accessed 24/Apr/2024)

HOST PLANT N°7: Prunus persica (PRNPS) for the Fruits (including hops) sector.


Origin of the listing:
 
New proposal

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):
 
Remark: the assessment performed covers the given host species as well as interspecific hybrids with other Prunus species.

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.

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)
Prunus armeniaca / Prunus persica
Affected trees often show a general decline in vigour a year or more before the entire tree collapses. Trees often die in circular areas within an orchard; the circular area expands each year as the fungus grows along roots of infected trees to roots of adjacent healthy trees. Tree death usually occurs in late spring. Aboveground symptoms can be easily confused with any other root problem. All stone fruit rootstocks are susceptible to Armillaria root rot. Generally, once an apricot tree (or any other tree) becomes infected with Armillaria mellea, it cannot be saved and should be removed (UCARN, 2017).

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 
Medium

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:
 
Remarks: 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. In France, professional operators can bear the current level of presence in fields (with no regulation in place) but they worry about the possible spreading of this pest due to infested plant material. Production period for Prunus is earlier in the season than for nuts, figs or pome fruits, allowing earlier detection, managing the pest earlier in the season (Infected plants are destroyed and soil removed), and consequently causing less impact. Further research programs on resistant rootstocks are requested by producers.

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).

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:
 
No (new regulation proposal)

Proposed Tolerance levels:
 
No listing.

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
No

Proposed Risk management measure:
 
No listing.


REFERENCES:
  • Baumgartner K & Rizzo DM (2013). Armillaria root rot. In Grape pest management, 3rd edition (ed Bettia L) CA: University of California, Division of Agriculture and Natural Resources, Oakland, pages 83-86.
  • 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
  • https://doi.org/10.1079/cabicompendium.7002 (accessed on 8/Apr/2024).
  • Chandelier A, Gerarts F, San Martin G, Herman M & Delahaye L (2016) Temporal evolution of collar lesions associated with ash dieback and the occurrence of Armillaria in Belgian forests. Forest Pathology 46(4), 289-297.
  • 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
  • Dowding P & Smith L (2008) Forest fungi In Ireland. COFORD, Dublin.
  • Downer J & Faber B (2019) Non-chemical control of Armillaria mellea infection of Prunus persica. Journal of Plant Science and Phytopathology 3, 050-055. https://doi.org/10.29328/journal.jpsp.1001031
  • Georgieva M, Georgieva M, Hristova M, Georgiev G (2023) Assessment of plane trees health status in urban green areas of Sofia, Bulgaria. Ecologia Balkanica 15(1), 117-125.
  • Guillaumin JJ, Pierson J & Grassely C (1991) The susceptibility to Armillaria mellea of different Prunus species used as stone fruit rootstocks. Scientia Horticulturae 46, 43-54.
  • Ivić D, Petrović E & Godena S (2023) Fungi associated with canker diseases on olive in Istria (Croatia). Journal of Central European Agriculture 24(2), 470-475.
  • Jankovský L (2003) Distribution and ecology of Armillaria species in some habitats of southern Moravia, Czech Republic. Czech Mycology 55(3-4), 173-186.
  • Kedves O, Shahab D, Champramary S, Chen L, Indic B, Bóka B, Nagy VD, Vágvölgyi C, Kredics L & Sipos G (2021) Epidemiology, biotic interactions and biological control of Armillarioids in the Northern Hemisphere. Pathogens 10(1), 76. https://doi.org/10.3390/pathogens10010076.
  • Łakomy P (2006) New location of Armillaria mellea in polish forests. mp was rolled down. Phytopathologia Polonica 41, 83–86.
  • Liesebach M, Schüler S & Weissenbacher L (2008). Herkunftsversuche der Küstentanne (Abies grandis [D. Don] Lindl.) in Österreich - Eignung, Wuchsleistung und Variation. Austrian Journal of Forest Science 125(3), 183-200.
  • McGranahan GH & Leslie CA (1990). Walnuts (Juglans). In Genetic resources of fruit and nut crops (eds Moore JN & Ballington JR) Volume 2. Acta Horticulturae 290, 907–951.
  • Marxmüller H, Holdenrieder O & Müller ED (1990). Zur Verbreitung, Phönologie und Ökologie von Armillaria mellea s.l. in Südbayern. Bericht Bayerischer Botanischer Gesellschaft, 61:115-134. https://www.zobodat.at/pdf/Berichte-Bayerischen-Bot-Ges-Erforschung-Flora_61_0115-0134.pdf
  • Mesanza N, Patten CL & Iturritxa E (2017) Distribution and characterization of Armillaria complex in Atlantic Forest Ecosystems of Spain. Forests 2017, 8(7), 235; https://doi.org/10.3390/f8070235
  • NDFF (2024) NDFF Verspreidingsatlas, NMV verspreidingsatlas paddenstoelen, Armillaria mellea (Vahl) P. Kumm. https://www.verspreidingsatlas.nl/0005040 (accessed 19/Mar/2024).
  • Papachatzis A, Eliopoulos P, Statharas G & Vagelas I (2008) Ficus carica rot rot disease caused by Armillaria mellea and Rosellinia necatrix in Greece. Universitatea Din Craiova (University Of Craiova) XIII (XLIX), 143-148.
  • Raabe (1962). Host list of root rot fungus Armillaria mellea. Hilgardia 33 nr. 2
  • Romagnesi H, 1973. Observations sur les Armillariella - II. Bulletin de la Société Mycologique de France, 89:195-206.
  • Termorshuizen AJ (2000). Ecology and epidemiology of Armillaria. In Armillaria Root Rot: Biology and Control of Honey Fungus (ed Fox RTV). Andover, Intercept, Pages 115-131.
  • Termorshuizen AJ & Arnolds EJM (1994). Geographical distribution of the Armillaria species in the Netherlands in relation to soil type and hosts. European Journal of Forest Pathology 24(3), 129-136.
  • UCANR (1998) Crop Profile for Walnuts in California. University of California Agriculture and Natural Resources. https://ucanr.edu/datastoreFiles/391-47.pdf
  • UCANR (2017) Apricot. Pest management guidelines for agriculture. University of California Agriculture and Natural Resources, UC IPM Pest Management Guidelines: Apricot, UC ANR Publication 3433. https://ipm.ucanr.edu/legacy_assets/pdf/pmg/pmgapricot.pdf (last accessed 24/Apr/2024)

HOST PLANT N°8: Pyrus (1PYUG) 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?
 
Yes
 
Conclusion:
 
Evaluation continues

 
Justification (if necessary):
 
Inspection for Armillaria mellea recommended in EPPO Standard PM 4-27 Pathogen-tested material of Malus, Pyrus and Cydonia. However, 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. Evaluation continues on pathway and economic impact.

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, also known as honey fungus or oak root fungus, has a wide host range (CABI 2021; Raabe, 1962); pear (Pyrus spp.) can be a host of this pathogen .
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, A. 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).
Although A. mellea can spread by infected propagation material, however the major issue is planting orchards on land previously used for forestry (A. mellea is a common disease in forests).
[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?
 

Justification:
 
Although Armillaria mellea is a significant problem in e.g. forestry, it is not of major economic importance on apple and pear. The pathogen is most likely to be found in orchards established on recently cleared woodlands with well-drained sandy of clay soil (Schnabel, 2017). Affected trees usually show a general decline in vigour over many years. Sometimes trees that look healthy will suddenly wilt and die in a matter of weeks. The aboveground symptoms are similar to other root problems, including too much water, Phytophthora root rot, rodents, etc. The key symptom to look for is trees that are declining in infection centers (patches of diseased trees with the earliest infected trees typically in the middle) that potentially can expand annually (UC PMG, 2017b).

[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)
 

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:
 

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:
 

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:
  • Anselmi N, Saraceni A & Anselmi A (2021) Incidence of Armillaria species in agrarian, forest and ornamental ecosystems of the Lazio region. Agriculture & Forestry/Poljoprivreda i šumarstv 67(1).
  • Caruso FL (2017) Armillaria root rot. In Compendium of Blueberry, Cranberry, and Lingonberry Diseases and Pests 2nd edition (eds Polashock JJ, Caruso FL, Averill AL & Schilder AC). American Phytopathological Society, St Paul, MN, USA. pages 12-13.
  • 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
  • Downer J & Faber B (2019) Non-chemical control of Armillaria mellea infection of Prunus persica. Journal of Plant Science and Phytopathology 3, 050-055. https://doi.org/10.29328/journal.jpsp.1001031.
  • Guerrero JC, Pérez SF, Ferrada EQ, Cona LQ & Bensch ET (2014) Phytopathogens of hazelnut (Corylus avellana L.) in southern Chile. Acta Horticulturae 1052, 269-274.
  • Kedves O, Shahab D, Champramary S, Chen L, Indic B, Bóka B, Nagy VD, Vágvölgyi C, Kredics L & Sipos G (2021) Epidemiology, biotic interactions and biological control of Armillarioids in the Northern Hemisphere. Pathogens 10(1), 76. ttps://doi.org/10.3390/pathogens10010076
  • Palmieri L, Prodorutti D, Gobbin D, Pertot I & Gessler C (2006). Role of barks used in highbush blueberry mulching on Armillaria spp. infections. [Italian] Giornate Fitopatologiche, Riccione (RN), 27-29 marzo 2006. Atti, volume secondo. 301-306.
  • Prodorutti D, Vanblaere T, Gobbin D, Pellegrini A, Gessler C & Pertot I (2009) Genetic diversity of Armillaria spp. infecting highbush blueberry in Northern Italy (Trentino Region). Phytopathology 99(6), 651-658.
  • Raabe (1962). Host list of root rot fungus Armillaria mellea. Hilgardia 33 nr. 2
  • Raabe RD (2008) Plants resistant or susceptible to Armillaria mellea, the oak root fungus. University of California, Berkeley. https://alamedabackyardgrowers. org/wp-content/uploads/2019/01/List-of-Oak-Root-Fungus-Resistant-or-Susceptible-Trees-Plants. pdf.[accessed 28 Jul 2023].
  • Raziq F & Fox RTV (2006). The integrated control of Armillaria mellea 2. Field experiments. Biological agriculture & horticulture 23(3), 235-249.
  • Schnabel G (2017). Armillaria root rot. In Compendium of Apple and Pear Diseases and Pests 2nd edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, MN, USA. pages 70-71.
  • Termorshuizen AJ (2000) Ecology and epidemiology of Armillaria. In Armillaria Root Rot: Biology and Control of Honey Fungus (ed Fox RTV). Andover, Intercept, Pages 115-131.
  • Thomidis T & Exadaktylou E (2012) Effectiveness of cyproconazole to control Armillaria root rot of apple, walnut and kiwifruit. Crop Protection 36, 49-51.
  • UC PMG (2017a) Armillaria root rot (oak root fungus). In Apple - Pest management guidelines for agriculture. University of California Agriculture and Natural Resources, UC IPM Pest Management Guidelines: UC ANR Publication 3432 page 72.
  • UC PMG (2017b) Armillaria root and crown rot (oak root fungus). In Pear - Pest management guidelines for agriculture. University of California Agriculture and Natural Resources, UC IPM Pest Management Guidelines: UC ANR Publication 3455 page 78-79.

HOST PLANT N°9: Vaccinium (1VACG) for the Fruits (including hops) sector.


Origin of the listing:
 
New proposal

Plants for planting:
 
Plants intended for planting


3 - Is the pest already listed in a PM4 standard on the concerned host plant?
 
Yes
 
Conclusion:
 
Evaluation continues

 
Justification (if necessary):
 
Inspection for Armillaria mellea recommended in EPPO Standard PM 4-18 Pathogen-tested material of Vaccinium. However, in responses to the questionnaire, NL and SI did not support regulationsince plants for planting was not the 'main' pathway. Evaluation continues on pathway.

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, also known as honey fungus or oak root fungus, has a wide host range (CABI 2021; Raabe, 1962). The pathogen can infect Vaccinium corymbosum (Caruso, 2017; Prodorutti et al., 2009).
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). The presence of infected roots (of various plant species) is an important and likely source of inoculum for highbush blueberry (Prodorutti et al., 2017). 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, A. 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). In particular, Armillaria spp. have been found on coniferous bark used as mulch in highbush blueberry plantings (Prodorutti et al., 2007).
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).
Armillaria spp. could be isolated from infected bark which was used to mulch plants (Palmieri et al., 2006).
Although A. mellea can spread by infected propagation material, the major issue is planting orchards on land previously used for forestry (A. mellea is a common disease in forests).
[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. When Vaccinium fruits are produced indoor, sterilized soil/new substrate is used and plants for planting is neither considered as a significant pathway.

5 - Economic impact:

Are there documented reports of any economic impact on the host?
 

Justification:
 
Affected bushes may display a range of symptoms. Plants low in vigour may appear to be suffering from nutritional disorders and may slowly decline in vitality of several years (Caruso, 2017). As observed with A. gallica, symptoms may take months (e.g. 10 months - 2 years) before to develop (Prodorutti et al., 2006). Affected bushes may be distributed in patches around focal points of fungal inoculum (Caruso, 2017).

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 

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:
 

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:
 

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:
 
No (new regulation proposal)

Proposed Tolerance levels:
 
No listing.

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
No

Proposed Risk management measure:
 
No listing.


REFERENCES:
  • Anselmi N, Saraceni A & Anselmi A (2021) Incidence of Armillaria species in agrarian, forest and ornamental ecosystems of the Lazio region. Agriculture & Forestry/Poljoprivreda i šumarstv 67(1).
  • Caruso FL (2017) Armillaria root rot. In Compendium of Blueberry, Cranberry, and Lingonberry Diseases and Pests 2nd edition (eds Polashock JJ, Caruso FL, Averill AL & Schilder AC). American Phytopathological Society, St Paul, MN, USA. pages 12-13.
  • 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
  • Downer J & Faber B (2019) Non-chemical control of Armillaria mellea infection of Prunus persica. Journal of Plant Science and Phytopathology 3, 050-055. https://doi.org/10.29328/journal.jpsp.1001031.
  • Guerrero JC, Pérez SF, Ferrada EQ, Cona LQ & Bensch ET (2014) Phytopathogens of hazelnut (Corylus avellana L.) in southern Chile. Acta Horticulturae 1052, 269-274.
  • Kedves O, Shahab D, Champramary S, Chen L, Indic B, Bóka B, Nagy VD, Vágvölgyi C, Kredics L & Sipos G (2021) Epidemiology, biotic interactions and biological control of Armillarioids in the Northern Hemisphere. Pathogens 10(1), 76. ttps://doi.org/10.3390/pathogens10010076
  • Palmieri L, Prodorutti D, Gobbin D, Pertot I & Gessler C (2006) Role of barks used in highbush blueberry mulching on Armillaria spp. infections. [Italian] Giornate Fitopatologiche, Riccione (RN), 27-29 marzo 2006. Atti, volume secondo. 301-306.
  • Prodorutti D, Palmieri L, Gobbin D & Pertot (2006) First report of Armillaria gallica on highbush blueberry (Vaccinium corymbosum) in Italy. Plant pathology 55(4), 583-583.
  • Prodorutti D, Perlot I, Giongo L & Gessler (2007) Highbush Blueberry: Cultivation, Protection, Breeding and Biotechnology. Phytopathology 99(6), 651-658.
  • Prodorutti D, Vanblaere T, Gobbin D, Pellegrini A, Gessler C & Pertot I (2009) Genetic diversity of Armillaria spp. infecting highbush blueberry in Northern Italy (Trentino Region). The European Journal of Plant Science and Biotechnology 1(1), 44-56. Available at http://www.globalsciencebooks.info/Online/GSBOnline/images/0706/EJPSB_1(1)/EJPSB_1(1)44-56o.pdf.
  • Raabe (1962). Host list of root rot fungus Armillaria mellea. Hilgardia 33 nr. 2
  • Raabe RD (2008) Plants resistant or susceptible to Armillaria mellea, the oak root fungus. University of California, Berkeley. https://alamedabackyardgrowers. org/wp-content/uploads/2019/01/List-of-Oak-Root-Fungus-Resistant-or-Susceptible-Trees-Plants. pdf.[accessed 28 Jul 2023].
  • Raziq F & Fox RTV (2006). The integrated control of Armillaria mellea 2. Field experiments. Biological agriculture & horticulture 23(3), 235-249.
  • Schnabel G (2017). Armillaria root rot. In Compendium of Apple and Pear Diseases and Pests 2nd edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, MN, USA. pages 70-71.
  • Termorshuizen AJ (2000) Ecology and epidemiology of Armillaria. In Armillaria Root Rot: Biology and Control of Honey Fungus (ed Fox RTV). Andover, Intercept, Pages 115-131.
  • Thomidis T & Exadaktylou E (2012) Effectiveness of cyproconazole to control Armillaria root rot of apple, walnut and kiwifruit. Crop Protection 36, 49-51.
  • UC PMG (2017a) Armillaria root rot (oak root fungus). In Apple - Pest management guidelines for agriculture. University of California Agriculture and Natural Resources, UC IPM Pest Management Guidelines: UC ANR Publication 3432 page 72.
  • UC PMG (2017b) Armillaria root and crown rot (oak root fungus). In Pear - Pest management guidelines for agriculture. University of California Agriculture and Natural Resources, UC IPM Pest Management Guidelines: UC ANR Publication 3455 page 78-79.