Legend
Justification for qualification based on EPPO PM 4 Standards
Justification for disqualification
Additional or non-conclusive information
Standard text

back...

NAME OF THE ORGANISM: Aphelenchoides ritzemabosi (APLORI)

GENERAL INFORMATION ON THE PEST

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

Pest category:

Nematoda

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: DE suggested to list all Aphelenchoides at genus level to reduce diagnostic workload. Although differentiation between species may be difficult, the Fruit SEWG suggested to perform an assessment at species level. If needed, measures addressing the risk with different Aphelenchoides species can be defined.

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):

Bulgaria (2000); Germany (2000); Hungary (2000); Ireland (2000); Italy (2000); Latvia (2000); Netherlands (2000); Poland (2000); Portugal (2000); Portugal/Madeira (2000); Spain (2000); Spain/Islas Canárias (2000)

Conclusion:

Candidate

Justification (if necessary):

Data of the presence of this pest on the EU territory are available in EPPO Global Database (https://gd.eppo.int/).

HOST PLANT N°1: Fragaria (1FRAG) 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):

The pest is listed in EPPO Standard PM4-11 Certification scheme for strawberry. However, when responding to the questionnaire, NL considered that economic impact was acceptable and supported deregulation. Evaluation continues especially on the economic impact.

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

Yes

Conclusion:

Candidate

Justification:

At least 124 genera are alternate hosts of A. ritzemabosi, and these are mainly in the Compositae (Ferris 2022; cited in Westerdahl & Bello, 2023; CABI, 2021). Several weeds including goosegrass, chickweed, buttercup, sowthistle, and speedwell are hosts of A. ritzemabosi highlighting that for crop rotation to succeed it is important to control weeds in the alternate crops (CABI, 2021)
A. ritzemabosi is an obligate plant parasite, inhabiting leaves, buds, growing points and outer layers of stem; in soil it does not complete its life cycle or survive the winter. It feeds endoparasitically on mesophyll cells of leaves, and ectoparasitically on buds and growing points (Southey, 1952; Siddiqi, 1974; cited in CABI 2021). The nematodes move in the water film over plants, not within the stem tissue, to reach the leaves and buds. Rain splashes and leaf contacts contribute to re-infestation and spread (Wallace, 1959; cited from CABI, 2021). The leaves are invaded through the stomata. The nematodes feed on the parenchymatous tissue of the mesophyll and destroy the cells, resulting in leaf spots or blotches, easily seen on the under surface. The nematodes leave brown tissue through the stomata and migrate in the water film on the surface to infect terminal flower buds which produce deformed and under-sized blossoms (CABI, 2021)
No change in A. ritzemabosi population per number of hearts occurred when strawberry plants infested with A. ritzemabosi were stored at temperatures of 14-15°C or in an unheated glasshouse in winter. However, at 20°C, the population increased several times. Under cold-storage conditions at -2 to -1°C it performed well in plant tissues (Tacconi, 1972; Cited in CABI, 2022). A. ritzemabosi is a facultative parasite; when no host is available, it can survive, since it can also feed and survive on fungi, either in the soil or on decaying plant material (Desaeger & Norling, 2017).
Plants for planting is considered to be a significant pathway.

5 - Economic impact:

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

Yes

Justification:

A. ritzemabosi is a serious pest of strawberry in Ireland, where yield reductions up to 60% due to A. ritzemabosi and A. fragariae infestations have been recorded (Duggan, 1969). The crown weight of strawberry cv. Senga Sengana was reduced by 51% by A. ritzemabosi and by 41% by A. fragariae. Fruit yield in the first year was reduced, owing largely to a decline in fruit number, by 65% and 54%, respectively, by these two species. The number of runners was reduced by 25-30% by A. ritzemabosi, but only by 11-15% by A. fragariae. Damage to the plant crowns and reduced yield were related to population density in winter and spring, but reduced runner production was due to the summer population density (Bohmer, 1981). Due to infection by A. ritzemabosi, average yield losses of the strawberry variety Korallovaya 100 were estimated as 53.4%. The variety Yasna seems to be somewhat less susceptible to A. ritzemabosi than Korallovaya 100 or Muto (Lebedeva et al., 1972; cited in CABI, 2021). In Poland, A. ritzemabosi infestation destroyed 45% of chrysanthemum plants on a holding, and for the most susceptible varieties the number could be as high as 92% (Baranowski, 1976; cited in CABI, 2021)
In Germany, A. ritzemabosi reduced yields by 65% (Blank, 1985). In tests in Poland, on seven strawberry varieties tested, A. fragariae and A. ritzemabosi reduced yields by 32–61% (McElroy 1972; Szczygiel 1967, cited in Westerdahl & Bello, 2023).
Cauliflower disease of strawberry can result from the interaction of either A. fragariae or A. ritzemabosi with the bacterium Rhodococcus fascians. In this disease, the flowers of stunted plants look like miniature cauliflowers (Crosse and Pitcher 1952; Pitcher and Crosse 1958; Potter & Noling, 1998).

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:

Candidate

Justification:

Economic impact was rated for plants for planting produced under outdoor conditions (not in vitro).

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?

Yes

Conclusion:

Candidate

Justification:

Healthy runners (certified stock enables growers to start clean)
Hot water treatments of runners before planting effectively control Aphelenchoides spp. (Qui et al., 1993)
Crop rotation

If a field becomes infected:
Removing (rouging) and disposal of symptomatic plants as soon as they appear can help to minimize the spread of nematodes to other plants (McElroy, 1972). In addition to rogueing of infested plants and propagating from clean mother plants, minimizing surface moisture on plants and contact between plants, planting on ridges, avoiding splashing water from sprinkler irrigation, and rooting runners in containers placed in the row can help to minimize nematode spread in the field (McElroy 1972; Siddiqi 1975; cited in Westerdahl & Bello, 2023)

7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?

Yes

Conclusion:

Candidate

Justification:

CONCLUSION ON THE STATUS:

Recommended for listing as an RNQP, based on data and EPPO PM 4 Standard.

8 - Tolerance level:

Is there a need to change the Tolerance level:

Yes

Proposed Tolerance levels:

See measures.

9 - Risk management measures:

Is there a need to change the Risk management measure:

Yes

Proposed Risk management measure:

The following measure is recommended for A. ritzemabosi, for CAC (in addition to the substantially free from requirement for traded material):
1. Plants for planting derived from in-vitro plants and grown in pots with pest-free growing media (e.g. tested soil, use of sterilized growing media or soil-free),
or
2. Plants for planting produced in a pest free production site and grown in pots with pest-free growing media (e.g. tested soil, use of sterilized growing media or soil-free),
or
3. The crop has been inspected at appropriate times during the growing season, and not more than 1% of the plants have been found to show symptoms of Aphelenchoides spp. infection during the whole growing season, and those symptomatic plants have been removed immediately. For plants for planting which are maintained for a period shorter than three months, only one inspection during this period is necessary.
or
4. Plants for planting have been found to be free of A. ritzemabozi after laboratory tests on a representative sample.

Additional measures in the certification scheme could include threshold in the field (for certified material), and testing, hot water treatment of the runners, soil requirements or selling plants without soil, etc. (for Pre-basic, Basic and Certified).

Remark: measures for A. besseyi should be adapted accordingly.

Justification (if necessary):

The Fruit SEWG considered that the PFA option was not practical to establish for this pest.
Option 4 can be performed after plants for planting have been subject to hot water treatment. When choosing option 3, testing may be performed for all Aphelenchoides species together if this is more practical.
The Fruit SEWG recommended that a threshold is established for symptoms on CAC material applicable to all the species together (see measures); and that the risk is managed along with the measures for other species of Aphelenchoides in the fruit marketing directive with tolerances for Pre-basic, Basic and Certified material. There was no reason identified for a different threshold for A. besseyi, A. fragariae and A. ritzemabosi for Basic and Certified material, and harmonization was recommended.

REFERENCES:

Baranowski T (1976) Investigations on harmful influence of fauna on Chrysanthemum X hortorum Bailey grown in Poznan and its close neighbourhood. Roczniki Nauk Rolniczych, Seria E 6(1), 17-39.
Bohmer B (1981) The harmful effect of Aphelenchoides fragaria and A. ritzemabosi on Fragaria ananassa. Gesunde Pflanzen 33(5):113-117.
CABI (2021) Aphelenchoides ritzemabosi (Chrysanthemum foliar eelworm). CABI Crop Protection Compendium (Accessed 9/Aug/2024). https://www.cabidigitallibrary.org/doi/full/10.1079/cabicompendium.6384.
CABI (2022) Aphelenchoides fragariae (strawberry crimp nematode) (accessed 12/Aug/2024). https://www.cabidigitallibrary.org/doi/10.1079/cabicompendium.6381
Crosse JE & Pitcher RS (1952) Studies in the relationship of eelworms and bacteria to certain plant diseases. I. The etiology of strawberry cauliflower disease. Annals of Applied Biology 39, 475–486.
Desaeger J & Norling JW (2017) Foliar or Bud Nematodes in Florida Strawberries: ENY-068/IN1184, 11/2017. EDIS, 2017(6).
Duggan JJ (1969) Leaf and bud eelworms of strawberries. Farm Research News 10(6), 134-136.
Ferris H (2022) Host range search: Aphelenchoides ritzemabosi (Nemaplex). http://nemaplex.ucdavis.edu/ Nemabase2010/NematodeHostRangeDDResults.aspx?Susc=%&NgenusNspec1= Aphelenchoides%20ritzemabosi.
Lebedeva ME, Metlitskii OZ & Drozdovskii EM (1972). Chrysanthemum eelworm as a parasite of strawberry in southern Ukraine. Kul'tura zemlyaniki v SSSR. Doklady simpoziuma, (28 iyunya - 1 iyulya 1971). "Kolos". Moscow USSR, 446-450.
McElroy FD (1972) Nematodes of tree fruits and small fruits (Chapter 15). In Economic Nematology (ed Webster JM). Academic Press, London, pp 335–376.
Pitcher RS, Crosse JE (1958) Studies in the relationship of the eelworms and bacteria to certain plant diseases. II. Further analysis of the strawberry cauliflower disease complex. Nematologica 3, 244–256.
Potter JW & Noling JW (1998) Spring dwarf and cauliflower disease. In Compendium of Strawberry Diseases 2nd edition (ed Maas JL). American Phytopathological Society, St Paul, MN, USA. pages 76-77.
Siddiqi MR (1974) Aphelenchoides ritzemabosi. CIH Descriptions of Plant-parasitic Nematodes, Set 3, No. 32. Wallingford, UK: CAB International.
Southey JF (1952). Unusual chrysanthemum eelworm symptoms. Plant Pathology 1, 48-49.
Szczygiel A (1967) Preliminary estimation of the harmfulness of nematodes of the genus Aphelenchoides to strawberries in South Poland. Prace Instytutu Sadownictwa 11, 211–224.
Tacconi R (1972) Infestations of Aphelenchoides fragariae, Aphelenchoides ritzemabosi and Ditylenchus dipsaci on strawberry in some Italian provinces. Redia 53, 313-319.
Wallace HR (1959) Movement of eelworms. V. Observations on Aphelenchoides ritzema-bosi (Schwartz, 1912) Steiner, 1932 on florists' chrysanthemums. Annals of Applied Biology 47, 350-360.
Westerdahl BB & Bello OM (2023) Leaf and bud nematodes in agricultural crops and their management by biotechnological approaches (chapter 16). In Novel biological and biotechnological applications in plant nematode management (ed Kahn MJ). Springer, Singapore. 359-376.

HOST PLANT N°2: Ribes (1RIBG) 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):

The pest is listed in Standard PM 4-9 Certification scheme for Ribes. However, when responding to the questionnaire, NL considered that economic impact was acceptable and supported deregulation. Evaluation continues especially on the economic impact.

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

Yes

Conclusion:

Candidate

Justification:

At least 124 genera are alternate hosts of A. ritzemabosi, and these are mainly in the Compositae (Ferris 2022; cited in Westerdahl & Bello, 2023; CABI, 2021). Several weeds including goosegrass, chickweed, buttercup, sowthistle, and speedwell are hosts of A. ritzemabosi highlighting that for crop rotation to succeed it is important to control weeds in the alternate crops (CABI, 2021). It has also been reported on Ribes spp. (Kohl et al., 2011; Chałańska et al., 2014).
A. ritzemabosi is an obligate plant parasite, inhabiting leaves, buds, growing points and outer layers of stem; in soil it does not complete its life cycle or survive the winter. It feeds endoparasitically on mesophyll cells of leaves, and ectoparasitically on buds and growing points (Southey, 1952; Siddiqi, 1974; cited in CABI 2021). The nematodes move in the water film over plants, not within the stem tissue, to reach the leaves and buds. Rain splashes and leaf contacts contribute to re-infestation and spread (Wallace, 1959; cited from CABI, 2021). The leaves are invaded through the stomata. The nematodes feed on the parenchymatous tissue of the mesophyll and destroy the cells, resulting in leaf spots or blotches, easily seen on the under surface. The nematodes leave brown tissue through the stomata and migrate in the water film on the surface to infect terminal flower buds which produce deformed and under-sized blossoms (CABI, 2021).
Plants for planting is considered to be a significant pathway.

5 - Economic impact:

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

Justification:

Although A. ritzemabosi has been recorded on Ribes spp. there are no records on impact of this foliar nematode on Ribes.

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?

Conclusion:

Not candidate

Justification:

Although A. ritzemabosi occur on and cause damage to strawberries, the fruit SEWG considered that there was not enough data to consider regulating the pest on Ribes for indirect economic impact on strawberry.

Conclusion:

Justification:

The results of more than 8 years of voluntary certification schemes for strawberry stocks in Italy indicate that A. ritzemabosi, A. fragariae, D. dipsaci and Meloidogyne spp. can be successfully controlled by means of plant certification schemes (Tacconi and Lamberti, 1994; cited in CABI 2021)

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: no data of economic impact on Ribes

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:

CABI (2021) Aphelenchoides ritzemabosi (Chrysanthemum foliar eelworm). CABI Crop Protection Compendium (Accessed 9/Aug/2024). https://www.cabidigitallibrary.org/doi/full/10.1079/cabicompendium.6384.
Chałańska A, Bogumił A, Machnicka K & Dzięgielewska M (2014) First record of chrysanthemum foliar nematode Aphelenchoides ritzemabosi (Schwarz 1911) Steiner & Buhrer 1932 (Nematoda: Aphelechoididae) in leaf buds of black currant (Ribes nigrum L.) in Poland. Progress In Plant Protection 54(4),403-406. DOI: http://dx.doi.org/10.14199/ppp-2014-068.
Kohl LM (2011) Floria nematodes: a summary of biology and control with a compilation on the host range. Online. Plant Health Progress doi:10.1094/PHO-2011-1129-01-RV.
Siddiqi MR (1974) Aphelenchoides ritzemabosi. CIH Descriptions of Plant-parasitic Nematodes, Set 3, No. 32. Wallingford, UK: CAB International.
Southey JF (1952) Unusual chrysanthemum eelworm symptoms. Plant Pathology 1, 48-49.
Wallace HR (1959) Movement of eelworms. V. Observations on Aphelenchoides ritzema-bosi (Schwartz, 1912) Steiner, 1932 on florists' chrysanthemums. Annals of Applied Biology 47, 350-360.
Westerdahl BB & Bello OM (2023) Leaf and bud nematodes in agricultural crops and their management by biotechnological approaches (chapter 16). In Novel biological and biotechnological applications in plant nematode management (ed Kahn MJ). Springer, Singapore. 359-376.