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: 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.