| Legend |
|---|
| Justification for qualification based on EPPO PM 4 Standards |
| Justification for disqualification |
| Additional or non-conclusive information |
| Standard text |
NAME OF THE ORGANISM: Aphelenchoides fragariae (APLOFR)
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?
No
Presence in the EU:
Yes
List of countries (EPPO Global Database):
Belgium (1992); Bulgaria (2002); Denmark (1993); Estonia (2002); France (1992); Germany (2014); Hungary (2002); Ireland (2002); Italy (2002); Latvia (2002); Netherlands (2002); Poland (2002); Portugal (2002); Portugal/Azores (2002); Portugal/Madeira (2002); Slovakia (2002); Spain (2002); Spain/Islas Canárias (2002); Sweden (1992)
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 with a focus 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:
Aphelenchoides fragariae is a polyphagous foliar nematode, over 250 plants in 47 families are recorded as hosts (Sturhan, 1962 cited in CABI, 2022; Ferris, 2022). A. fragariae is an obligate parasite of above-ground plant parts and may be ecto- or endoparasitic. On strawberry it is ectoparasitic on folded crown and runner buds, feeding caused small, dry brown areas, delimited by the midrib and major veins. The nematodes may be found feeding endoparasitically on leaf tissues and have occasionally been found in fruit pulp (Tacconi, 1972; cited in CABI, 2022).
The nematode cannot survive in soil without a host for more than 3 months (Szczygiel and Hasior, 1971; cited in CABI, 2021). It survived in a dormant state in fern fronds buried in soil for at least 46 days (Stewart, 1921; cited in CABI). A. fragariae is a facultative parasite; when no host is available it can also feed and survive on fungi, either in the soil or on decaying plant material (Desaeger & Norling, 2017).
No change in A. fragariae population per number of hearts occurred when strawberry plants infested with A. fragariae 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). Relatively few individuals of A. fragariae survived at -20°C (Hirling, 1972; cited in CABI, 2022). Under dry conditions, A. fragariae survived in damaged lily leaves for more than 600 days (Yamada & Takakura, 1987; cited in CABI 2022).
It can move with infected plant material, however, plant material can be treated (see section on measures available). The Fruit SEWG considered that plants for planting was a significant pathway when cultivating plants for planting under outdoor conditions (not for in vitro plants).
The nematode cannot survive in soil without a host for more than 3 months (Szczygiel and Hasior, 1971; cited in CABI, 2021). It survived in a dormant state in fern fronds buried in soil for at least 46 days (Stewart, 1921; cited in CABI). A. fragariae is a facultative parasite; when no host is available it can also feed and survive on fungi, either in the soil or on decaying plant material (Desaeger & Norling, 2017).
No change in A. fragariae population per number of hearts occurred when strawberry plants infested with A. fragariae 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). Relatively few individuals of A. fragariae survived at -20°C (Hirling, 1972; cited in CABI, 2022). Under dry conditions, A. fragariae survived in damaged lily leaves for more than 600 days (Yamada & Takakura, 1987; cited in CABI 2022).
It can move with infected plant material, however, plant material can be treated (see section on measures available). The Fruit SEWG considered that plants for planting was a significant pathway when cultivating plants for planting under outdoor conditions (not for in vitro plants).
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Yes
Justification:
A. fragariae is most active in cool spring weather when plant growth is beginning, therefore also called 'spring dwarf'. Ectoparasitic feeding activity begins in the crown of the plant from which distorted buds and puckered leaves with short stems emerge. Brown patches may be visible near the mid-rib of leaves. Fruit either fails to develop from the distorted buds or is small and deformed. If runners are allowed to develop, they will likely be infested. During warmer weather, nematodes may become quiescent and symptoms may disappear (McElroy, 1972).
In Germany, A. fragariae reduced yields by 45% (Blank 1985; cited in CABI, 2022). A. fragariae has also caused significant losses in both France and Italy (Clerfeau et al. 1983; Tacconi 1985; cited in CABI, 2022). In tests in Poland, on seven strawberry varieties tested, A. fragariae could reduce yields by 32–61% (McElroy 1972; Szczygiel 1967; cited in CABI, 2022). In the United States, losses are infrequent but serious when they occur. For example, in Massachusetts losses as high as 60–70% from A. fragariae were reported following the planting of infested planting stock.
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; cited in CABI, 2022).
In Germany, A. fragariae reduced yields by 45% (Blank 1985; cited in CABI, 2022). A. fragariae has also caused significant losses in both France and Italy (Clerfeau et al. 1983; Tacconi 1985; cited in CABI, 2022). In tests in Poland, on seven strawberry varieties tested, A. fragariae could reduce yields by 32–61% (McElroy 1972; Szczygiel 1967; cited in CABI, 2022). In the United States, losses are infrequent but serious when they occur. For example, in Massachusetts losses as high as 60–70% from A. fragariae were reported following the planting of infested planting stock.
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; cited in CABI, 2022).
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?
No
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)
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. fragariae, 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. fragariae 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.
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. fragariae 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.
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:
- Blank W (1985) Leaf and stem nematodes in strawberries - a serious problem. Mitteilungen des Obstbauversuchsringes des Alten Landes 40, 229–234.
- CABI (2022) Aphelenchoides fragariae (strawberry crimp nematode). https://www.cabidigitallibrary.org/doi/10.1079/cabicompendium.6381 (accessed 12/Aug/2024).
- Clerfeau M, Rancillac M, Veschambre D (1983) The position regarding strawberry decline in France. Pepinieristes Horticulteurs Maraichers Revue Horticole 237:39–42.
- 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).
- Ferris H (2022) Host range search: Aphelenchoides fragariae (Nemaplex). http://nemaplex.ucdavis.edu/
- Hirling W (1972) On the technique of examining strawberry plants and chrysanthemum leaves for leaf nematodes (Aphelenchoides fragariae and A. ritzemabosi). Part III. Anzeiger fur Schadlingskunde und Pflanzenschutz 45, 6-10.
- 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.
- Qiu J, Westerdahl BB, Buchner RP & Anderson CA (1993) Refinement of hot water treatment for management of Aphelenchoides fragariae in strawberry. Journal of Nematology 25(4 suppl), 95–99
- Siddiqi MR (1975) Aphelenchoides fragariae. CIH Descriptions of Plant-parasitic Nematodes Set 5, No. 7.
- Sturhan D, 1962. Über neue Wirtspflanzen der Blattälchen Aphelenchoides fragariae und A. ritzemabosi, mit Bemerkungen zu den Wirtspflanzenkreisen beider Nematodenarten. Anzeiger für Schädlingskunde 35(5), 65-67.
- 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
- Szczygiel A & Hasior H (1971). Possibility of persistence of leaf and bud nematode (Aphelenchoides fragariae) on strawberry plants and in the soil. Zeszyty Problemowe Postepow Nauk Rolniczych 121, 101-106.
- Tacconi R (1972) Infestations of Aphelenchoides fragariae, Aphelenchoides ritzemabosi and Ditylenchus dipsaci on strawberry in some Italian provinces. Redia 53, 313-319.
- Tacconi R (1985) Nematological problems in Emilia Romagna. Redia 68:1–15
- 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.
- Yamada E & Takakura S (1987) Ecological investigations on the strawberry nematode, Aphelenchoides fragaria on lilies. Japanese Journal of Nematology 17(12), 1-7