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Justification for qualification based on EPPO PM 4 Standards
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NAME OF THE ORGANISM: Exobasidium vaccinii (EXOBVA)

GENERAL INFORMATION ON THE PEST

Name as submitted in the project specification (if different):

Exobasidium vaccinii (Exobasidium vaccinii
var. vaccinii)

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):

Remark on host plants: In this RNQP summarysheet, Exobasidium vaccinii is considered to be limited to Vaccinium spp., and data on Azalea and Rhododendron is not considered:
• On the website from Plant parasites Europe, the host range is described as: Hosts Ericaceae, narrowly monophagous: Vaccinium vitis-idaea. So, this could indicate that Vaccinium myrtillus should not be included; Index Fungorum reports on a different species Exobasidium myrtilli Siegm. (Mitt. Ver. Nat. Reich: 19, 1879). On the plant parasites Europe website common names are cowberry redleaf, azalea leaf and flower gall are mentioned, but no data on Rhododendron or Azalea are included in the literature references.
• In Compendium of blueberry, cranberry, lingonberry diseases and pests, it is indicated that the host range of E. vaccinii is broad including Rhododendron and Camellia.
• On Azalea, Exobasidium japonicum is reported; however, isolates of E. vaccinii (from Vaccinium vitis-idaea) and E. japonicum (from azalea) in cross-inoculations could not infect the other host (Graafland, 1960).
• A new disease is emerging in the South-East USA: Exobasidium maculosum (Brewer et al., 2014; Ingram et al., 2019). This is a different species from Exobasidium
vaccinii. Losses mainly occur because the fungus infects the fruits – symptoms are distinct from red leaf disease.
Many websites & publications indicated that Exobasidium vaccinii is also causing galls on Azalea & Rhododendron. Some authors indicate Exobasidium vaccinii a species complex (Ingram et al., 2015), however without a literature reference.

Restricting E. vaccinii to Vaccinium spp. was supported in an analysis provided by DEFRA and made available at https://upload.eppo.int/download/2459o421016689. This may be corrected in the future if molecular sequencing data is available where E. vaccinii is confirmed on Azalae or Rhododendron.

2 – Status in the EU:

Is this pest already a quarantine pest for the whole EU?

Presence in the EU:

Yes

List of countries (EPPO Global Database):

Conclusion:

Candidate

Justification (if necessary):

Exobasidium vaccinii has been reported from most European countries (Mervielde, 2001) on native Vaccinium spp. e.g. Austria (Negrean, 1996), Belgium (Mervielde, 2001), France (Pellicier, 2001), Germany (Doppelbaur & Doppelbauer, 1973), Italia (Tomasi, 2003), Netherlands (Mervielde, 2001), Poland (Kozłowska et al., 2015), Slovenia (Ogris & Jurc, 2013).

Doppelbaur H & Doppelbaur H (1973). Germany: Vaccinium oxycoccus, Vaccinium uliginosum, Vaccinium vitis-idaea.
Kozłowska M, Mułenko W & Heluta VP (2015). Poland: Vaccinium vitis-idaea.
Mervielde H (2001) Belgium & Netherlands: Vaccinium vitis-idaea.
Negrean G (1996) Austria: Vaccinium myrtillus.
Ogris N & Jurc D (2013) Slovenia: Vaccinium myrtillus
Pellicier P (2001) France: Vaccinium myrtillus
Tomasi E (2003) Italy: Vaccinium vitis-idaea.

HOST PLANT N°1: Vaccinium (1VACG) 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):

EPPO Standard PM 4-18 Certification scheme for Vaccinium recommends inspection for 'Exobasidium vaccinii var. vaccinii' with same tolerance levels as in the EU regulation. The pest was selected for further assessment, initially to discuss with the EWG whether 'Exobasidium vaccinii var. vaccinii' or 'Exobasidium vaccinii' should be listed. Preferred name under EPPO GD is Exobasidium vaccinii. When discussing this pest, the Fruit SEWG recommended first to assess whether plants for planting was a significant pathway.

4 - Are the listed plants for planting the main* pathway for the "pest/host/intended use" combination? (*: significant compared to others):

Conclusion:

Not candidate

Justification:

Exobasidium vaccinii is a pathogen of Ericaceae, mostly infecting Vaccinium spp. (Anonymous, 2023). In Europe is reported on native Vaccinium spp. like Vaccinium myrtillus and Vaccinium vitis-idaea (e.g. Kozłowska et al., 2015; Mervielde, 2001; Pellicier, 2001; Tomasi, 2003).
The disease is spread by basidiospore, but knowledge on the disease cycle is incomplete (Bristow 1995, revised by Schilder, 2017). Circumstantial evidence suggests that infections in highbush blueberry plantings may originate from infected wild (low-bush) blueberry stands in the surrounding landscape (Schilder, 2017). Leaves become infected by basidiospores or by conidia budded from them, these can be carried by wind or rain (Smith et al. 1988). The fungus is already reported in Europe, but is unclear whether Exobasidium vaccinii reported in the EU in native Vaccinium spp. could infect commercial Vaccinium spp., like V. corymbosum.

The closely related Exobasidium maculosum was reported to survive epiphytically on leaf surfaces (Ingram et al., 2019). Spores can remain viable until appropriate conditions are present, and can be spread wind, splashing water, and insects (Liu, 2023).

The Fruit SEWG considered that plants for planting should not be considered as a significant pathway.

5 - Economic impact:

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

Yes

Justification:

In the USA the fungus is known to cause red leaf in blueberry (Vaccinium corymbosum). In Michigan the disease is especially observed during very cool, wet seasons. While disease incidence is generally low, as many as 20-30% of the bushes in a field may be infected. Reports on red leaf are rare on highbush blueberry in the northeastern and southeastern USA and on rabbitey blueberry in the south. Although the pathogen attacks native Vaccinium spp. and cultivated cranberry in the Pacific Northwest, the disease “red leaf” has not been reported in this region. The pathogen systemically invades the plant and can cause significant losses when disease incidence is high. Most of the information currently available on red leaf disease comes from research conducted on lowbush blueberry (Vaccinium angustifolium) (Bristow 1995, revised by Schilder 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 as 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:

Anonymous (2023) Exobasidium vaccinii. Plant Parasites of Europe: leafminers, galls and fungi. (Last modified 27.vii.2023; accessed 28/May/2024). https://bladmineerders.nl/parasites/fungi/dikarya/basidiomycota/ustilaginomycotina/exobasidiomycetes/exobasidiales/exobasidiaceae/exobasidium/exobasidium-vaccinii/
Brewer MT, Turner AN, Brannen PM, Cline WO & Richardson EA (2017) Exobasidium maculosum, a new species causing leaf and fruit spots on blueberry in the southeastern USA and its relationship with other Exobasidium spp. parasitic to blueberry and cranberry. Mycologia 106(3) 415-423.
Bristow PR (1995) revised by Schilder AMC (2017) Red leaf. In Compendium of blueberry, cranberry and lingonberry diseases and pests second edition (eds Polashock, JJ, Caruso FL, Averill AL, Schilder AC). American Phytopathological Society, St. Paul, Minnesota USA. 40-41.
Doppelbaur H & Doppelbaur H (1973) Parasitische Pilze aus dem Bayerischen Wald. Berichte der bayerischen botanischen Gesellschaft 44, 239-248.
Graafland W (1960) The parasitism of Exobasidium japonicum Shir. on Azalea. Acta Botanica Neerlandica 9, 347-379.
Ingram RJ, Ludwig HD & Scherm H (2019) Epidemiology of Exobasidium leaf and fruit spot of rabbiteye blueberry: Pathogen overwintering, primary infection, and disease progression on leaves and fruit. Plant disease 103(6), 1293-1301.
Kozłowska M, Mułenko W & Heluta VP (2015) Fungi of the Roztocze Region (Poland and Ukraine). 2. A checklist of microfungi and larger Ascomycota. pp 204.
Liu B (2023) Exobasidium leaf and fruit spot of blueberry. [Exobasidium maculosum] https://extension.unh.edu/resource/exobasidium-leaf-fruit-spot-blueberry.
Mervielde H (2001) Enige aantekeningen over het geslacht Exobasidium Woronin (Bladgast) in België en Nederland. Coolia 44(1): 1-11.
Negrean G (1996) Beitrag zum Vorkommen parasitischer Pilze in Oberösterreich. Beiträge zur Naturkunde Oberösterreichs 4: 281-297.
Ogris N & Jurc D (2013) Tree diseases determined by the reporting, prognostic and diagnostic service for forests in Slovenia 1982–2012. Acta Silvae et Ligni 102, 31-42.
Pellicier P (2001) Contribution à l'étude systématique et écologique des micromycètes parasites des plantes sauvages des Alpes Françaises (neuvième note): récoltes du département de la Haute-Savoie et de quelques autres des Alpes Françaises, Valaisannes et Valdôtaines. Bulletin mensuel de la Société linnéenne de Lyon 70 (10): 26I-268.
Smith IM, Dunez J, Lelliott RA, Phillips DH & Archer SA (1988) Exobasidiales, Exobasidium vaccinii. In European Handbook of Plant Diseases. Blackwell Scientific Publications, Oxford, UK. 504.
Tomasi E (2003) Indagine cecidologica nella foresta di Tarvisio (Friuli-Venezia Giulia, Italia). 1. Atti del Museo civico di Storia naturale di Trieste 50, 59-88.