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: Pratylenchus penetrans (PRATPE)


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):
 
-

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 (2003); Bulgaria (2003); Cyprus (2011); Czech Republic (2003); Denmark (2003); Estonia (2003); France (2003); Germany (2003); Greece (2003); Hungary (2003); Italy (2003); Netherlands (2003); Poland (2012); Portugal (2020); Romania (2003); Slovakia (2003); Spain (2003); Sweden (2003)

Conclusion:
 
Candidate

Justification (if necessary):
 
Pratylenchus penetrans is cosmopolitan but mainly found in temperate regions, whereas Pratylenchus vulnus is present mostly on woody plants in warmer (subtropical and Mediterranean) climates in different continents (Moens & Perry, 2009). 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: 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?
 
No
 
Conclusion:
 
Evaluation continues

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:
 
Pratylenchus penetrans is cosmopolitan and has more than 350 hosts including woody plants (e.g., fruit trees, roses) and herbaceous plants (e.g., potato, vegetables) (Moens & Perry, 2009, CABI, 2021), e.g., Malus is a good host for Pratylenchus penetrans (aaltjesschema, 2019). Also Pyrus spp., Cydonia oblonga, Pistacia vera and many Prunus spp. can be hosts of P. penetrans (Hoekstra & Oostenbrink, 1962; Askary et al., 2012; Merrifield, 2000). Ficus carica is not mentioned as hosts and information of Pratylenchus penetrans on Pistacia vera is scarce (PlantwisePlus Knowledge Bank, 2023; Fatemy, 2009), this could be linked to P. penetrans being a nematode from mostly temperate climates and fig and pistachio being more Mediterranean crops. P. penetrans can complete its entire life cycle within the roots of plants.
Pratylenchus spp. are migratory endoparasites that enter the host root for feeding and reproduction and move freely within the tissue. Consequently, they spend much of their life cycle in roots and are found in soil when the host plants are senescing, stressed or diseased, or when their hosts have been ploughed up after harvest (Castillo and Vovlas, 2007).
P. penetrans occurs mostly on sandy and peaty soil. The transport of infected plants or those growing in infested soils is one of the principal means by which these nematodes are disseminated (Lehman, 1994; Anonymous, 1999). Bare-rooted plants are often contaminated by soil particles which may contain nematodes. Roots can host endoparasitic nematodes that are not removed by washing treatments (Lehman, 1994). In this context, it is essential that the plant propagation material be free of this pathogen (Allen, 1949). Because it can survive in soil, it can be dispersed by land vehicles etc.; within a field by cultivation, and can be introduced to non-infested sites by poorly sanitized farm equipment. However, measures (including hygiene) can limit the importance of such alternative pathways.
In responses to the questionnaire, DE, FR and NL supported deregulation in the EU because soilborne and widespread in production areas.
Considering the numerous bibliographic references that highlight the importance of plants for planting as an important pathway, and the existence of measures that can reduce the role of the others reported pathways, host plants for planting with roots, with or without soil or growing media, are considered as a main pathway.

5 - Economic impact:

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

Justification:
 
In pome fruits, 25 to 150 individuals/100 cm3 soil of Pratylenchus spp. are considered damaging but can vary depending on soil texture (Anonymous, 1998). Apple rootstocks seem to be a better host for Pratylenchus penetrans than pear and quince rootstocks, which showed a moderate resistance (Söğüt et al., 2013). Cydonia oblonga mentioned as one of the main hosts (Plantwise).
In the NEMAPLEX (2024) database, Cydonia oblonga is reported as susceptible (= high level of nematode reproduction) to Pratylenchus penetrans (Goodey et al., 1965).
Pratylenchus species rank third to root-knot and cyst nematodes as having the greatest impact on crops worldwide (Jones et al., 2013). Apart from direct damage to roots, Pratylenchus species may also predispose plants to other pathogens (e.g., Verticillium and Fusarium), thereby increasing the damage extent. The elimination of the nematode or reduction of its population causes a marked reduction in the incidence of fungi and an increase in crop yield (Bucki et al., 2020).

In the responses to the questionnaire, FR supported deregulation in the EU, commenting that the pest had a 'low nuisance level on fruit plants'.

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 
Medium to 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?
 
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:
 
Cydonia oblonga is cited as a main host, having the potential to maintain high populations of this parasite with the capacity to cause direct (during its feeding on roots) and indirect (by increasing susceptibility to attack by other soil pathogens) economic damage. In addition, experience from Spain shows that the effects of this nematode on quince are significant.
The damage caused by Pratylenchus is usually most severe in light-textured soils that are low in nutrients (e.g. nitrogen, potassium, or calcium) and in organic matter (Anonymous, 1999).
Remark: Unacceptable economic impact may also be caused to other hosts (e.g. Malus, Pyrus, Prunus).

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:
 
Crop rotation is difficult because of the wide host range of Pratylenchus penetrans, including weeds. Pratylenchus penetrans can propagate well on many crops, sometimes without causing damage (symptomless) (aaltjesschema). Recent research indicated that with proper choice of selected cultivars of cover crops, P. penetrans can be controlled but further breeding efforts are needed. Although some cover crops can reduce the population of Pratylenchus penetrans (Taning et al., 2023). Since many weeds can also be a host, adequate weed control is important (Aaltjesschema, 2019). Crop rotation is also a limited option since woody crops remain in soil for decades and the host-range of many of this of the plant parasitic nematodes is wide (Castillo y Vovlas, 2007).

Growing Tagetes spp. (e.g. Tagetes patula) can reduce the population considerably (Evenhuis et al., 2004). The authors predicted that strawberries could be grown for about 7 successive years without economic damage due to the root lesion nematode. Pudasaini et al. (2006) showed that Tagetes can reduce P. penetrans exponentially in time under marigold. The effect of marigold was persistent as no increase in P. penetrans densities over the whole soil profile was noticed after two crop cycles of host plants.

Use of clean soil: The propagation material is kept either in containers of sterilized growing medium or in soil that has been tested and found free from various nematodes (e.g. EPPO 2022).

Soil fumigation: dependent on legislation. Preplant soil fumigation does not eradicate nematodes but dramatically reduces nematode numbers. The nematodes return to their original population density (or greater) within 2 or 3 years after planting, but the absence of nematode pressure during the initial years of establishment is critical for trees to develop strong, healthy root systems (Abawi & Mai, 2014). With the progressive phase-out of chemical nematicides such as Aldicarb, Carbofuran, and 1,3-Dichloropropene, the effectiveness and sustainability of current plant-parasitic nematode management strategies remain limited (Barbosa et al., 2022).

Healthy plants: To prevent the introduction of nematode problems, new orchards should be established with trees obtained from reputable nurseries that treat their soils for nematodes (Abawi & Mai, 2014).

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.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
Yes

Proposed Risk management measure:
 
Non-Certified material (‘Conformitas Agraria Communitatis (CAC)’):
• Mother plants have been produced in a pest free place/site of production
or
• Material obtained from mother plants does not contain roots and soil

AND

• Plants have been produced in soil/growing medium considered free from P. penetrans (e.g. tested soil, use of sterilized growing media or soil-free).

Justification (if necessary):
 
The risk of transmission of this nematode is restricted to materials with roots and soil. Generally, material obtained from mother plants (e.g. buds, cuttings...) doesn’t contain roots and soil. The critical point to avoid the spread of this pest is in the nurseries where certified and CAC seedlings are produced for marketing to growers or end users. Considering that symptoms may not be visible, that symptomology is non-specific (both above and below ground) and the complexity to perform laboratory testing, the Fruit SEWG considered that PFA should not be proposed as an option. The Fruit SEWG also considered that an option requiring not growing hosts during > 5 years was not realistic considering how polyphagous the pest is.
Hot water treatments with some time-temperature schedules have been shown to be effective against the pest (Anonymous, 1999; Lim et al., 2024). Further work would be needed to validate if these schedules are applicable to the different host species under practical circumstances.

[During consultation on draft recommendations, NL commented that it will be very difficult if not impossible to find production sites that are free, unless the plants are grown indoor in pots.] The Fruit SEWG considered that on one hand the pest has a very wide host range and is widespread in some countries (e.g. in NL); on the other hand, in other countries (e.g. in ES or other countries), soils are not so infested. But plant for planting is a significant pathway. It is an endoparasite, moving with plants for planting. It is difficult to see the symptoms since this involves uprooting the plant (only possible for Fragaria). The fruit SEWG considered that the decision should be taken later by risk managers on whether the measure is maintained to limit economic impact to end users or withdrawn to limit economic burden to the producer of plants for planting.

REFERENCES:
  • Aaltjesschema (2019). Website on information and crop rotation for various crops. The website is s product of Wageningen UR, nematology PPO-AGV. Website is accessible until 31 March 2024, only information for perennial plants and fruit crops will still be available. https://www.aaltjesschema.nl/Home.aspx
  • Abawi GS & Mai WF (2014) Root lesion nematodes (revised by Halbrendt JM). In Compendium of apple and pear diseases and pests, second edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, USA: 113-114.
  • Allen MW (1949). Root-lesion nematodes: resistant rootstocks most promising method of control. California Agriculture, January: 13-14.
  • Anonymous (1998) Pratylenchus on Oregon crops: Pratylenchus damage levels for Oregon crops: a literature survey. https://bpp.oregonstate.edu/pratylenchus-oregon-crops.
  • Anonymous (1999) Lesion nematodes. University of Illinois Extension. RPD, 1103. May 1999.
  • Askary TH, Banday SA, Iqbal U, Khan AA, Mir MM & Waliullah MIS (2012) Plant parasitic nematode diversity in pome, stone and nut fruits. In Agroecology and Strategies for Climate Change (ed Lichtfouse E). Springer Sicens+Business Media B.V. DOI 10.1007/978-94-007-1905-7_10. 237-268.
  • Barbosa P, Faria JMS, Figueiredo AC, Mota M & Vicente CSL (2022) Control of the root lesion Pratylenchus penetrans: the effect of nematicidal activity of plant-derived compounds. Revista de Ciencias Agrarias, 45 (4): 649-652. https://doi.org/10.19084/rca.28749
  • Bird GW & Melakeberhan H (1995) Root-Lesion Nematodes (Pratylenchus spp.). In Compendium of Stone Fruit Diseases (eds Ogawa JM, Zehr EI, Bird GW, Ritchie DF, Uriu K & Uyemoto JK)
  • Bucki P, Qing X, Castillo P, Gamliel A, Dobrinin S, Alon T, Miyara SB (2020) The genus Pratylenchus (Nematoda: Pratylenchidae) in Israel: from taxonomy to control practices. Plants 9, 1475; doi:10.3390/plants9111475.
  • Castillo P, Vovlas (2007) Biology and ecology of Pratylenchus. In “Pratylechus (Nematoda: Pratylenchidae): diagnosis, biology, pathogenicity and management”. Nematology Monographs & Perspective 6, 305-324.
  • Clavero-Camacho I, Archidona-Yuste A, Cantalapiedra-Navarrete C, Castillo P & Palomares-Rius JE (2024) Prevalence and ecological factors affecting the distribution of plant-parasitic nematodes in Prunus groves in Spain. Journal of Integrative Agriculture, 23(2): 585-589.
  • EPPO (2022) PM 4/17 (3) Certification scheme for olive trees and rootstocks. EPPO Bulletin 52, 590–60. DOI: 10.1111/epp.1288
  • Evenhuis A, Korthals G & Molendijk L. (2004). Tagetes patula as an effective catch crop for long-term control of Pratylenchus penetrans. Nematology, 6(6), 877-881. https://doi.org/10.1163/1568541044038632
  • Fatemy S (2009). Integrated management of pistachio nematodes. In Integrated Management of Fruit Crops and Forest Nematodes (eds Ciancio A & Mukerji KG). Springer Science+Business Media BV, 243-252.
  • Goodey JB, Franklin MT &Hooper DJ (1965) The nematode parasites of plants catalogued under their host. Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, England. Third Edition.
  • Hoestra H & Oostenbrink M (1962) Nematodes in relation to plant growth IV. Pratylenchus penetrans (Cobb) on orchard trees. Neth. J. agric. Sei., Vol. 10 (1962) No. 4 (November): 286-296
  • Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MGK, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WML & Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14 (9): 946-961.
  • Lehman PS (1994) Dissemination of phytoparasitic nematodes. Nematology Circular, No 28. Fla. Dept. Agric.& Consumer Services. Division of Plant Industry.
  • Lim G-E, Heo M-S & Park M-G (2024) Hot Water Treatment as a Quarantine Measure for Controlling Pratylenchus penetrans Cobb in Syngonium podophyllum Schott and Perilla frutescens Britton. Agriculture 14, 582. https://doi.org/10.3390/agriculture14040582.
  • Moens M & Perry RN (2009) Migratory plant endoparasitic nematodes: a group rich in contrasts and divergence. Annual Review of Phytopathology 47, 313–32.
  • NEMAPLEX (2024) Host Status of a Plant Genus and species to Nematodes. http://nemaplex.ucdavis.edu/ (accessed: 07/11/2024)
  • Nyczepir AP (1991) Nematode management strategies in stone fruits in the United States. Journal of Nematology 23(3), 334-341.
  • Mai WF & Abawi GS (1978) Determining the cause and extent of apple, cherry, and pear replant diseases under controlled conditions. Phytopathology 68, 1540-1544.
  • Merrifield K (2000) Plant-parasitic damage levels for Oregon nursery crops: A literature survey. Biology, host ranges, and damage levels of root-parasitic nematodes on Oregon nursery crops (Draft: 2000). https://bpp.oregonstate.edu/sites/agscid7/files/plant-parasitic-damage-levels-for-oregon-nursery-crops.pdf
  • Nyczepier A P & Halbrendt JM (1993) Nematode pests of deciduous fruit and nut trees. In Plant Parasitic Nematodes in Temperate Agriculture (eds Evans K, Trudgill DL & Webster JM). CAB International, Wallingford, England. pp. 381-425
  • PlantwisePlus Knowledge Bank (2023). Pratylenchus penetrans (nematode, northern root lesion). (accessed 26/Apr/2024). https://plantwiseplusknowledgebank.org/doi/full/10.1079/pwkb.species.43900
  • Pudasaini MP, Viaene N & Moens M (2006) Effect of marigold (Tagetes patula) on population dynamics of Pratylenchus penetrans in a field. Nematology 8, 477-84.
  • Schmitt DP & Sipes BS (2000) Plant-parasitic nematodes and their management. From “Plant Nutrient Management in Hawaii’s Soils, Approaches for Tropical and Subtropical Agriculture”. College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa.
  • Sharma GC, Thakur BS, Kashyap AS (2005) Impact of NPK on the nematode populations and yield of plum (Prunus salicina). SHS Acta Horticulturae, 696: VII International Symposium on Temperate Zone Fruits in the Tropics and Subtropics - Part Two. doi: 10.17660/ActaHortic.2005.696.77
  • Siddiqui IA, Sher SA & French AM (1973) Distribution of Plant Parasitic Nematodes in California. State of California Department of Food and Agriculture, Division of Plant Industry. 324p.
  • Söğüt MA, Devran Z, Arici ŞE, Şan B, Yildirim AN (2013) Host reactions of root lesion nematodes (Pratylenchus spp.) on the rootstocks of pome and stone. Turkish Journal of Entomology 37(2), 239-248.
  • Taning LM, Lippens L, Formesyn E, Wesemael W (2023) Impact of cover crops on population density of the root-lesion nematode Pratylenchus penetrans. Preprint DOI: https://doi.org/10.21203/rs.3.rs-3338686/v1
  • Townshend JL (1990) Growth of ‘Bartlett’ pear seedlings in response to number of root-lesions nematodes and temperature. HortSci, 25: 318-320
  • Yorston J M (1969). The interactions of Pratylenchus penetrans with host plants, Longidorus elongatus and Verticillium dahliae. PhD Thesis Oregon State University, 55 pp.

HOST PLANT N°2: 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

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:
 
Pratylenchus penetrans is cosmopolitan and has more than 350 hosts including woody plants (e.g., fruit trees, roses) and herbaceous plants (e.g., potato, vegetables) (Moens & Perry, 2009, CABI, 2021), e.g., Malus is a good host for Pratylenchus penetrans (aaltjesschema, 2019). Also Pyrus spp., Cydonia oblonga, Pistacia vera and many Prunus spp. can be hosts of P. penetrans (Hoekstra & Oostenbrink, 1962; Askary et al., 2012; Merrifield, 2000). Ficus carica is not mentioned as hosts and information of Pratylenchus penetrans on Pistacia vera is scarce (PlantwisePlus Knowledge Bank, 2023; Fatemy, 2009), this could be linked to P. penetrans being a nematode from mostly temperate climates and fig and pistachio being more Mediterranean crops. In Spain, this nematode has been frequently found on other plant species such as olive (Castillo et al., 2003) strawberry (Talavera et al., 2019) and Prunus spp. (Clavero-Camacho et al., 2024), but has never been reported on Ficus carica. P. penetrans can complete its entire life cycle within the roots of plants.
Pratylenchus spp. are migratory endoparasites that enter the host root for feeding and reproduction and move freely within the tissue. Consequently, they spend much of their life cycle in roots and are found in soil when the host plants are senescing, stressed or diseased, or when their hosts have been ploughed up after harvest (Castillo and Vovlas, 2007).
P. penetrans occurs mostly on sandy and peaty soil. The transport of infected plants or those growing in infested soils is one of the principal means by which these nematodes are disseminated (Lehman, 1994; Anonymous, 1999). Bare-rooted plants are often contaminated by soil particles which may contain nematodes. Roots can host endoparasitic nematodes that are not removed by washing treatments (Lehman, 1994). In this context, it is essential that the plant propagation material be free of this pathogen (Allen, 1949). Because it can survive in soil, it can be dispersed by land vehicles etc.; within a field by cultivation, and can be introduced to non-infested sites by poorly sanitized farm equipment. However, measures (including hygiene) can limit the importance of such alternative pathways.
In responses to the questionnaire, DE, FR and NL supported deregulation in the EU because soilborne and widespread in production areas.

5 - Economic impact:

Are there documented reports of any economic impact on the host?
 
No

Justification:
 
In the responses to the questionnaire, FR supported deregulation in the EU, commenting that the pest had a 'low nuisance level on fruit plants'.
Remark: Among the species of phytopathogenic nematodes associated with Ficus carica, the only ones that cause damage in fig-producing regions in Spain are those of the genus Meloidogyne, especially M. arenaria (Melgarejo, 1999; Casadomet et al., 2015; Navarro and Bartual, 2020), although they are not generally considered to be a major pest (Melgarejo, 1999).

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:
 
No information is available to confirm the economic impact of this pest on Ficus carica.

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:
 
Crop rotation is difficult because of the wide host range of Pratylenchus penetrans, including weeds. Pratylenchus penetrans can propagate well on many crops, sometimes without causing damage (symptomless) (aaltjesschema). Recent research indicated that with proper choice of selected cultivars of cover crops, P. penetrans can be controlled but further breeding efforts are needed. Although some cover crops can reduce the population of Pratylenchus penetrans (Taning et al., 2023). Since many weeds can also be a host, adequate weed control is important (Aaltjesschema, 2019). Crop rotation is also a limited option since woody crops remain in soil for decades and the host-range of many of this of the plant parasitic nematodes is wide (Castillo y Vovlas, 2007).

Growing Tagetes spp. (e.g. Tagetes patula) can reduce the population considerably (Evenhuis et al., 2004). The authors predicted that strawberries could be grown for about 7 successive years without economic damage due to the root lesion nematode. Pudasaini et al. (2006) showed that Tagetes can reduce P. penetrans exponentially in time under marigold. The effect of marigold was persistent as no increase in P. penetrans densities over the whole soil profile was noticed after two crop cycles of host plants.

Use of clean soil: The propagation material is kept either in containers of sterilized growing medium or in soil that has been tested and found free from various nematodes (e.g. EPPO 2022).

Soil fumigation: dependent on legislation. Preplant soil fumigation does not eradicate nematodes but dramatically reduces nematode numbers. The nematodes return to their original population density (or greater) within 2 or 3 years after planting, but the absence of nematode pressure during the initial years of establishment is critical for trees to develop strong, healthy root systems (Abawi & Mai, 2014). With the progressive phase-out of chemical nematicides such as Aldicarb, Carbofuran, and 1,3-Dichloropropene, the effectiveness and sustainability of current plant-parasitic nematode management strategies remain limited (Barbosa et al., 2022).

Healthy plants: To prevent the introduction of nematode problems, new orchards should be established with trees obtained from reputable nurseries that treat their soils for nematodes (Abawi & Mai, 2014).

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 report of fig being a host and no report of economic impact


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:
  • Aaltjesschema (2019). Website on information and crop rotation for various crops. The website is s product of Wageningen UR, nematology PPO-AGV. Website is accessible until 31 March 2024, only information for perennial plants and fruit crops will still be available. https://www.aaltjesschema.nl/Home.aspx
  • Abawi GS & Mai WF (2014) Root lesion nematodes (revised by Halbrendt JM). In Compendium of apple and pear diseases and pests, second edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, USA: 113-114.
  • Allen MW (1949). Root-lesion nematodes: resistant rootstocks most promising method of control. California Agriculture, January: 13-14.
  • Anonymous (1998) Pratylenchus on Oregon crops: Pratylenchus damage levels for Oregon crops: a literature survey. https://bpp.oregonstate.edu/pratylenchus-oregon-crops.
  • Anonymous (1999) Lesion nematodes. University of Illinois Extension. RPD, 1103. May 1999.
  • Askary TH, Banday SA, Iqbal U, Khan AA, Mir MM & Waliullah MIS (2012) Plant parasitic nematode diversity in pome, stone and nut fruits. In Agroecology and Strategies for Climate Change (ed Lichtfouse E). Springer Sicens+Business Media B.V. DOI 10.1007/978-94-007-1905-7_10. 237-268.
  • Barbosa P, Faria JMS, Figueiredo AC, Mota M & Vicente CSL (2022) Control of the root lesion Pratylenchus penetrans: the effect of nematicidal activity of plant-derived compounds. Revista de Ciencias Agrarias, 45 (4): 649-652. https://doi.org/10.19084/rca.28749
  • Bird GW & Melakeberhan H (1995) Root-Lesion Nematodes (Pratylenchus spp.). In Compendium of Stone Fruit Diseases (eds Ogawa JM, Zehr EI, Bird GW, Ritchie DF, Uriu K & Uyemoto JK)
  • Bucki P, Qing X, Castillo P, Gamliel A, Dobrinin S, Alon T, Miyara SB (2020) The genus Pratylenchus (Nematoda: Pratylenchidae) in Israel: from taxonomy to control practices. Plants 9, 1475; doi:10.3390/plants9111475.
  • Casadomet E, López M, Pérez F, Senero M, Pérez J & Del Moral J (2015) Parásitos, patógenos y fisiopatías de la higuera. Phytoma, 271: 30-39.
  • Castillo P, Vovlas (2007) Biology and ecology of Pratylenchus. In “Pratylechus (Nematoda: Pratylenchidae): diagnosis, biology, pathogenicity and management”. Nematology Monographs & Perspective 6, 305-324.
  • Clavero-Camacho I, Archidona-Yuste A, Cantalapiedra-Navarrete C, Castillo P & Palomares-Rius JE (2024) Prevalence and ecological factors affecting the distribution of plant-parasitic nematodes in Prunus groves in Spain. Journal of Integrative Agriculture, 23(2): 585-589.
  • EPPO (2022) PM 4/17 (3) Certification scheme for olive trees and rootstocks. EPPO Bulletin 52, 590–60. DOI: 10.1111/epp.1288
  • Evenhuis A, Korthals G & Molendijk L. (2004). Tagetes patula as an effective catch crop for long-term control of Pratylenchus penetrans. Nematology, 6(6), 877-881. https://doi.org/10.1163/1568541044038632
  • Fatemy S (2009). Integrated management of pistachio nematodes. In Integrated Management of Fruit Crops and Forest Nematodes (eds Ciancio A & Mukerji KG). Springer Science+Business Media BV, 243-252.
  • Goodey JB, Franklin MT &Hooper DJ (1965) The nematode parasites of plants catalogued under their host. Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, England. Third Edition.
  • Hoestra H & Oostenbrink M (1962) Nematodes in relation to plant growth IV. Pratylenchus penetrans (Cobb) on orchard trees. Neth. J. agric. Sei., Vol. 10 (1962) No. 4 (November): 286-296
  • Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MGK, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WML & Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14 (9): 946-961.
  • Lehman PS (1994) Dissemination of phytoparasitic nematodes. Nematology Circular, No 28. Fla. Dept. Agric.& Consumer Services. Division of Plant Industry.
  • Melgarejo P (1999) El cultivo de la higuera (Ficus carica L.). A. Madrid Vicente, Ediciones.
  • Moens M & Perry RN (2009) Migratory plant endoparasitic nematodes: a group rich in contrasts and divergence. Annual Review of Phytopathology 47, 313–32.
  • Navarro MJ, Bartual J (2020) Cultivo de la higuera. Formación y Tranferencia – Ficha técnica. Consellería de Agricultura, Desarrollo Rural, Emergencia Climática y Transición Ecológica. Generalitat Valencian.
  • NEMAPLEX (2024) Host Status of a Plant Genus and species to Nematodes. http://nemaplex.ucdavis.edu/ (accessed: 07/11/2024)
  • Nyczepir AP (1991) Nematode management strategies in stone fruits in the United States. Journal of Nematology 23(3), 334-341.
  • Mai WF & Abawi GS (1978) Determining the cause and extent of apple, cherry, and pear replant diseases under controlled conditions. Phytopathology 68, 1540-1544.
  • Merrifield K (2000) Plant-parasitic damage levels for Oregon nursery crops: A literature survey. Biology, host ranges, and damage levels of root-parasitic nematodes on Oregon nursery crops (Draft: 2000). https://bpp.oregonstate.edu/sites/agscid7/files/plant-parasitic-damage-levels-for-oregon-nursery-crops.pdf
  • Nyczepier A P & Halbrendt JM (1993) Nematode pests of deciduous fruit and nut trees. In Plant Parasitic Nematodes in Temperate Agriculture (eds Evans K, Trudgill DL & Webster JM). CAB International, Wallingford, England. pp. 381-425
  • PlantwisePlus Knowledge Bank (2023). Pratylenchus penetrans (nematode, northern root lesion). (accessed 26/Apr/2024). https://plantwiseplusknowledgebank.org/doi/full/10.1079/pwkb.species.43900
  • Pudasaini MP, Viaene N & Moens M (2006) Effect of marigold (Tagetes patula) on population dynamics of Pratylenchus penetrans in a field. Nematology 8, 477-84.
  • Schmitt DP & Sipes BS (2000) Plant-parasitic nematodes and their management. From “Plant Nutrient Management in Hawaii’s Soils, Approaches for Tropical and Subtropical Agriculture”. College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa.
  • Sharma GC, Thakur BS, Kashyap AS (2005) Impact of NPK on the nematode populations and yield of plum (Prunus salicina). SHS Acta Horticulturae, 696: VII International Symposium on Temperate Zone Fruits in the Tropics and Subtropics - Part Two. doi: 10.17660/ActaHortic.2005.696.77
  • Siddiqui IA, Sher SA & French AM (1973) Distribution of Plant Parasitic Nematodes in California. State of California Department of Food and Agriculture, Division of Plant Industry. 324p.
  • Söğüt MA, Devran Z, Arici ŞE, Şan B, Yildirim AN (2013) Host reactions of root lesion nematodes (Pratylenchus spp.) on the rootstocks of pome and stone. Turkish Journal of Entomology 37(2), 239-248.
  • Talavera M, Miranda L, Gómez-Mora JA, Vela MD & Verdejo-Lucas S (2019) Nematode management in the strawberry fields of southern Spain. Agronomy 9, 252: doi:10.3390/agronomy9050252
  • Taning LM, Lippens L, Formesyn E, Wesemael W (2023) Impact of cover crops on population density of the root-lesion nematode Pratylenchus penetrans. Preprint DOI: https://doi.org/10.21203/rs.3.rs-3338686/v1
  • Townshend JL (1990) Growth of ‘Bartlett’ pear seedlings in response to number of root-lesions nematodes and temperature. HortSci, 25: 318-320
  • Yorston J M (1969). The interactions of Pratylenchus penetrans with host plants, Longidorus elongatus and Verticillium dahliae. PhD Thesis Oregon State University, 55 pp.

HOST PLANT N°3: Fragaria (1FRAG) for the Fruits (including hops) sector.


Origin of the listing:
 
New proposal from the Spanish expert

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

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:
 
Pratylenchus penetrans is cosmopolitan and has more than 350 hosts including woody plants (e.g., fruit trees, roses) and herbaceous plants (e.g., potato, vegetables) (Moens & Perry, 2009, CABI, 2021), e.g., Malus is a good host for Pratylenchus penetrans (aaltjesschema, 2019). Also Pyrus spp., Cydonia oblonga, Pistacia vera and many Prunus spp. can be hosts of P. penetrans (Hoekstra & Oostenbrink, 1962; Askary et al., 2012; Merrifield, 2000). Ficus carica is not mentioned as hosts and information of Pratylenchus penetrans on Pistacia vera is scarce (PlantwisePlus Knowledge Bank, 2023; Fatemy, 2009), this could be linked to P. penetrans being a nematode from mostly temperate climates and fig and pistachio being more Mediterranean crops. P. penetrans can complete its entire life cycle within the roots of plants.
Pratylenchus spp. are migratory endoparasites that enter the host root for feeding and reproduction and move freely within the tissue. Consequently, they spend much of their life cycle in roots and are found in soil when the host plants are senescing, stressed or diseased, or when their hosts have been ploughed up after harvest (Castillo and Vovlas, 2007).
P. penetrans occurs mostly on sandy and peaty soil. The transport of infected plants or those growing in infested soils is one of the principal means by which these nematodes are disseminated (Lehman, 1994; Anonymous, 1999). Bare-rooted plants are often contaminated by soil particles which may contain nematodes. Roots can host endoparasitic nematodes that are not removed by washing treatments (Lehman, 1994). In this context, it is essential that the plant propagation material be free of this pathogen (Allen, 1949). Because it can survive in soil, it can be dispersed by land vehicles etc.; within a field by cultivation, and can be introduced to non-infested sites by poorly sanitized farm equipment. However, measures (including hygiene) can limit the importance of such alternative pathways.
Considering the numerous bibliographic references that highlight the importance of plants for planting as an important pathway, and the existence of measures that can reduce the role of the others reported pathways, host plants for planting with roots, with or without soil or growing media, are a considered as a main pathway.

5 - Economic impact:

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

Justification:
 
Pratylenchus penetrans has been reported as a pathogen for Fragaria in several countries (e.g. United States, Canada, Costa Rica, Israel, Spain) (Anonymous, 1999; Montes et al., 2006; Qing, 2008; Jackson-Ziems, 2016; MAPA, 2019; Talavera et al., 2019; Sandoval-Ruíz et al., 2023).

In Spain, this species is among the main plant pathogenic nematodes in strawberry crops (López-Aranda, 2008; MAPA, 2019; Talavera et al., 2019; Talavera, 2021; De los Santos et al., 2022). Talavera et al. (2019) found it in 20% of the commercial strawberry plantations of Huelva with an abundance range between 3 and 94 nematodes per 100 g of soil.

The pathogenicity of P. penetrans on strawberry plants has been demonstrated under both controlled and field conditions (see references in Bélair et al., 2018). Affected plants show a marked reduction of the root system and several associated non-specific aerial symptoms (dwarfism, chlorosis, wilting, lack of vigour, smaller fruits), sometimes leading to plant death (Montes et al., 2006; MAPA, 2019).

The wounds inflicted in the root system also favors the entry of other pathogens, especially fungi (e.g. Macrophomina phaseolina, Fusarium spp., Verticillim dahliae), causing complex diseases in strawberries (McKinley y Talboys, 1979, MAPA, 2019; Talavera et al., 2021). In fact, P. penetrans is one of the main components of the black root rot (BRR) complex (together with members of the genera Fusarium, Rhizoctonia, Pythium, Cylindrocarpon and Pestalotia) (Montes et al., 2006; López-Aranda, 2008; MAPA, 2019), an important strawberry pathology that, according to some experts, would have an even greater economic impact than crown rot caused by Phytophthora cactorum (López-Aranda, 2008).

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?
 
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:
 
Its economic impact on Fragaria, both direct and indirect (in association with other pathogens), is well documented.

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:
 
Crop rotation is difficult because of the wide host range of Pratylenchus penetrans, including weeds. Pratylenchus penetrans can propagate well on many crops, sometimes without causing damage (symptomless) (aaltjesschema). Recent research indicated that with proper choice of selected cultivars of cover crops, P. penetrans can be controlled but further breeding efforts are needed. Although some cover crops can reduce the population of Pratylenchus penetrans (Taning et al., 2023). Since many weeds can also be a host, adequate weed control is important (Aaltjesschema, 2019).

Growing Tagetes spp. (e.g. Tagetes patula) can reduce the population considerably (Evenhuis et al., 2004). The authors predicted that strawberries could be grown for about 7 successive years without economic damage due to the root lesion nematode. Pudasaini et al. (2006) showed that Tagetes can reduce P. penetrans exponentially in time under marigold. The effect of marigold was persistent as no increase in P. penetrans densities over the whole soil profile was noticed after two crop cycles of host plants.

Use of clean soil: The propagation material is kept either in containers of sterilized growing medium or in soil that has been tested and found free from various nematodes (e.g. EPPO 2022).

Soil fumigation: dependent on legislation. Preplant soil fumigation does not eradicate nematodes but dramatically reduces nematode numbers. The nematodes return to their original population density (or greater) within 2 or 3 years after planting, but the absence of nematode pressure during the initial years of establishment is critical for trees to develop strong, healthy root systems (Abawi & Mai, 2014). With the progressive phase-out of chemical nematicides such as Aldicarb, Carbofuran, and 1,3-Dichloropropene, the effectiveness and sustainability of current plant-parasitic nematode management strategies remain limited (Barbosa et al., 2022).

Healthy plants: To prevent the introduction of nematode problems, new orchards should be established with trees obtained from reputable nurseries that treat their soils for nematodes (Abawi & Mai, 2014).

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.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
Yes (new regulation proposal)

Proposed Tolerance levels:
 
Zero tolerance, based on inspection and testing

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
Yes

Proposed Risk management measure:
 
Non-Certified material (‘Conformitas Agraria Communitatis (CAC)’):
• Mother plants have been produced in a pest free place/site of production
AND
• Plants have been produced in soil/growing medium considered free from P. penetrans (e.g. tested soil, use of sterilized growing media or soil-free).

Justification (if necessary):
 
The risk of transmission of this nematode is restricted to materials with roots and soil. Generally, material obtained from mother plants (e.g. buds, cuttings...) doesn’t contain roots and soil. The critical point to avoid the spread of this pest is in the nurseries where certified and CAC seedlings are produced for marketing to growers or end users. Considering that detection by inspection is practically impossible when no symptoms are observed, that symptomology is non-specific (both above and below ground) and the complexity to perform laboratory testing, the fruit SEWG considered that PFA should not be proposed as an option. The Fruit SEWG also considered that an option requiring not growing hosts during > 5 years was not realistic considering how polyphagous the pest is.

REFERENCES:
  • Aaltjesschema (2019) Website on information and crop rotation for various crops. The website is s product of Wageningen UR, nematology PPO-AGV. Website is accessible until 31 March 2024, only information for perennial plants and fruit crops will still be available. https://www.aaltjesschema.nl/Home.aspx
  • Abawi GS & Mai WF (2014) Root lesion nematodes (revised by Halbrendt JM). In Compendium of apple and pear diseases and pests, second edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, USA: 113-114.
  • Allen MW (1949) Root-lesion nematodes: resistant rootstocks most promising method of control. California Agriculture, January: 13-14.
  • Anonymous (1999) Lesion nematodes. University of Illinois Extension. RPD, 1103. May 1999.
  • Bélair G, Coulombe J, Dauphinais N (2018) Management of Pratylenchus penetrans and Verticilllium symptoms in strawberry. Phytoprotection, 98(1), 1–3. https://doi.org/10.7202/1046783ar
  • Castillo P, Vovlas (2007) Biology and ecology of Pratylenchus. In “Pratylechus (Nematoda: Pratylenchidae): diagnosis, biology, pathogenicity and management”. Nematology Monographs & Perspective 6, 305-324.
  • De Los Santos B, Talavera M, Media JJ, Molina JM (2022) Plagas y enfermedades en frutos rojos. In “Cultivo, postcosecha, procesado y comercio de berris”. SPE3 s.l., Valencia (España).
  • EPPO (2022) PM 4/17 (3) Certification scheme for olive trees and rootstocks. EPPO Bulletin 52:590–60. DOI: 10.1111/epp.1288
  • Evenhuis A, Korthals G & Molendijk L (2004) Tagetes patula as an effective catch crop for long-term control of Pratylenchus penetrans. Nematology 6(6), 877-881. https://doi.org/10.1163/1568541044038632
  • Jackson-Ziems TA (2016) Root-Lesion Nematodes. Papers in Plant Pathology 523. http://digitalcommons.unl.edu/plantpathpapers/523
  • Lehman PS (1994) Dissemination of phytoparasitic nematodes. Nematology Circular, No 28. Fla. Dept. Agric.& Consumer Services. Division of Plant Industry.
  • López-Aranda JM (2008) El cultivo de la fresa en Huelva. In “La fresa de Huelva”. Junta de Andalucía. Consejería de Agricultura y Pesca. Servicio de Publicaciones y Divulgación.
  • MAPA (2019) Guía de Gestión Integrada de Plagas: fresa y fresón. Ministerio de Agricultura, Pesca y Alimentación. https://www.mapa.gob.es/es/agricultura/temas/sanidad-vegetal/productos-fitosanitarios/guias-gestion-plagas/horticolas/default.aspx
  • McKinley RT, Talboys PW (1979) Effects of Pratylenchus penetrans on development of strawberry wilt caused by Verticillium dahliae. Ann. Appl. Biol., 92: 347-357.
  • Moens M & Perry RN (2009) Migratory plant endoparasitic nematodes: a group rich in contrasts and divergence. Annual Review of Phytopathology 47, 313–32.
  • Montes F, Paéz JI, Guillén V, Miguel J (2006) Nematodos lesionadores de fresa: Pratylenchus penetrans. In “Fichas de Diagnóstico en Laboratorio de Organismos Nocivos de los Vegetales”. https://www.mapa.gob.es/app/observatorio-de-tecnologias-probadas/diagnostico/ficha.asp?fichaid=356
  • Pudasaini MP, Viaene N & Moens M (2006) Effect of marigold (Tagetes patula) on population dynamics of Pratylenchus penetrans in a field. Nematology 8, 477-84.
  • Quing Y (2008). Species of Pratylenchus (Nematoda: Pratylenchidae) in Canada: description, distribution, and identification. Canadian Journal of Plant Pathology 30 (3): 477-485. https://doi.org/10.1080/07060660809507545
  • Sandoval-Ruiz R, Gómez-Alpízar L, Humphreys-Pereira DA, Flores-Chaves L (2023) Molecular identification of root-lesion nematodes, Pratylenchus spp. in agricultural crops from Costa Rica. Agronomía Mesoamericana 34 (1): 49445. doi:10.15517/am.v34i1.49445
  • Schmitt DP, Sipes BS (2000) Plant-parasitic nematodes and their management. In “Plant Nutrient Management in Hawaii’s Soils, Approaches for Tropical and Subtropical Agriculture”. College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa.
  • Talavera M, Miranda L, Gómez-Mora JA, Vela MD, Verdejo-Lucas S. (2019). Nematode management in the strawberry fields of southern Spain. Agronomy 9, 252: doi:10.3390/agronomy9050252
  • Talavera MF (2021) Enfermedades causadas por nematodos en los frutos rojos de Huelva: etiología y control. Phytoma 331, 24-27.
  • Taning LM, Lippens L, Formesyn E, Wesemael W (2023) Impact of cover crops on population density of the root-lesion nematode Pratylenchus penetrans. Preprint DOI: https://doi.org/10.21203/rs.3.rs-3338686/v1

HOST PLANT N°4: 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?
 
No
 
Conclusion:
 
Evaluation continues

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:
 
Pratylenchus penetrans is cosmopolitan and has more than 350 hosts including woody plants (e.g., fruit trees, roses) and herbaceous plants (e.g., potato, vegetables) (Moens & Perry, 2009, CABI, 2021), e.g., Malus is a good host for Pratylenchus penetrans (aaltjesschema, 2019). Also Pyrus spp., Cydonia oblonga, Pistacia vera and many Prunus spp. can be hosts of P. penetrans (Hoekstra & Oostenbrink, 1962; Askary et al., 2012; Merrifield, 2000). Ficus carica is not mentioned as hosts and information of Pratylenchus penetrans on Pistacia vera is scarce (PlantwisePlus Knowledge Bank, 2023; Fatemy, 2009), this could be linked to P. penetrans being a nematode from mostly temperate climates and fig and pistachio being more Mediterranean crops. P. penetrans can complete its entire life cycle within the roots of plants.
Pratylenchus spp. are migratory endoparasites that enter the host root for feeding and reproduction and move freely within the tissue. Consequently, they spend much of their life cycle in roots and are found in soil when the host plants are senescing, stressed or diseased, or when their hosts have been ploughed up after harvest (Castillo and Vovlas, 2007).
P. penetrans occurs mostly on sandy and peaty soil. The transport of infected plants or those growing in infested soils is one of the principal means by which these nematodes are disseminated (Lehman, 1994; Anonymous, 1999). Bare-rooted plants are often contaminated by soil particles which may contain nematodes. Roots can host endoparasitic nematodes that are not removed by washing treatments (Lehman, 1994). In this context, it is essential that the plant propagation material be free of this pathogen (Allen, 1949). Because it can survive in soil, it can be dispersed by land vehicles etc.; within a field by cultivation, and can be introduced to non-infested sites by poorly sanitized farm equipment. However, measures (including hygiene) can limit the importance of such alternative pathways.
In responses to the questionnaire, DE, FR and NL supported deregulation in the EU because soilborne and widespread in production areas.
Considering the numerous bibliographic references that highlight the importance of plants for planting as an important pathway, and the existence of measures that can reduce the role of the others reported pathways, host plants for planting with roots, with or without soil or growing media, are considered as a main pathway.

5 - Economic impact:

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

Justification:
 
In pome fruits, 25 to 150 individuals/100 cm3 soil of Pratylenchus spp. are considered damaging but can vary depending on soil texture (Anonymous, 1998). Apple rootstocks seem to be a better host for Pratylenchus penetrans than pear and quince rootstocks, which showed a moderate resistance (Söğüt et al., 2013). The pathogenicity of Pratylenchus penetrans on stone and pome fruit trees has been amply demonstrated by experimental evidence and field observations (e.g. Mai and Parker, 1967; Townshed, 1990).

Malus is sensitive to Pratylenchus penetrans infection, and low levels of P. penetrans (33/100 gram soil) can already lead to damage (Hoestra & Oostenbrink, 1962). P. penetrans can also propagate well on Malus (aaltjesschema (2019). This species has been responsible for severe decline and for replanting failure in many apple orchards (Anonymous, 1999).

Some studies have indicated that certain apple rootstocks are less susceptible to root lesion nematode damage than are others, but nematode resistance has not been a high priority in most rootstock breeding programs. Root lesion nematode damage is a greater problem on dwarfing rootstocks than on more vigorous seedling rootstocks.

Apples tend to be more sensitive to root lesion nematode damage than are pears, but other factors are also involved, since, pears are e.g. more often planted on heavier soils than are apples, which provides some protection since root lesion nematodes are more damaging in lighter soils (Abawi & Mai , 2014).

In the responses to the questionnaire, FR supported deregulation in the EU, commenting that the pest had a 'low nuisance level on fruit plants'.

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 
Medium to 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?
 
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:
 
The economic impact of this pathogen on Malus is widely demonstrated, as well as the potential impacts on other hosts (Prunus, Pyrus).
The damage caused by Pratylenchus is usually most severe in light-textured soils that are low in nutrients (e.g. nitrogen, potassium, or calcium) and in organic matter (Anonymous, 1999).

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:
 
Crop rotation is difficult because of the wide host range of Pratylenchus penetrans, including weeds. Pratylenchus penetrans can propagate well on many crops, sometimes without causing damage (symptomless) (aaltjesschema). Recent research indicated that with proper choice of selected cultivars of cover crops, P. penetrans can be controlled but further breeding efforts are needed. Although some cover crops can reduce the population of Pratylenchus penetrans (Taning et al., 2023). Since many weeds can also be a host, adequate weed control is important (Aaltjesschema, 2019). Crop rotation is also a limited option since woody crops remain in soil for decades and the host-range of many of this of the plant parasitic nematodes is wide (Castillo y Vovlas, 2007).

Growing Tagetes spp. (e.g. Tagetes patula) can reduce the population considerably (Evenhuis et al., 2004). The authors predicted that strawberries could be grown for about 7 successive years without economic damage due to the root lesion nematode. Pudasaini et al. (2006) showed that Tagetes can reduce P. penetrans exponentially in time under marigold. The effect of marigold was persistent as no increase in P. penetrans densities over the whole soil profile was noticed after two crop cycles of host plants.

Use of clean soil: The propagation material is kept either in containers of sterilized growing medium or in soil that has been tested and found free from various nematodes (e.g. EPPO 2022).

Soil fumigation: dependent on legislation. Preplant soil fumigation does not eradicate nematodes but dramatically reduces nematode numbers. The nematodes return to their original population density (or greater) within 2 or 3 years after planting, but the absence of nematode pressure during the initial years of establishment is critical for trees to develop strong, healthy root systems (Abawi & Mai, 2014). With the progressive phase-out of chemical nematicides such as Aldicarb, Carbofuran, and 1,3-Dichloropropene, the effectiveness and sustainability of current plant-parasitic nematode management strategies remain limited (Barbosa et al., 2022).

Healthy plants: To prevent the introduction of nematode problems, new orchards should be established with trees obtained from reputable nurseries that treat their soils for nematodes (Abawi & Mai, 2014).

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.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
Yes

Proposed Risk management measure:
 
Non-Certified material (‘Conformitas Agraria Communitatis (CAC)’):
• Mother plants have been produced in a pest free place/site of production
or
• Material obtained from mother plants does not contain roots and soil

AND

• Plants have been produced in soil/growing medium considered free from P. penetrans (e.g. tested soil, use of sterilized growing media or soil-free).

Justification (if necessary):
 
The risk of transmission of this nematode is restricted to materials with roots and soil. Generally, material obtained from mother plants (e.g. buds, cuttings...) doesn’t contain roots and soil. The critical point to avoid the spread of this pest is in the nurseries where certified and CAC seedlings are produced for marketing to growers or end users. Considering that symptoms may not be visible, that symptomology is non-specific (both above and below ground) and the complexity to perform laboratory testing, the fruit SEWG considered that PFA should not be proposed as an option. The Fruit SEWG also considered that an option requiring not growing hosts during > 5 years was not realistic considering how polyphagous the pest is.
Hot water treatments with some time-temperature schedules have been shown to be effective against the pest (Anonymous, 1999; Lim et al., 2024). Further work would be needed to validate if these schedules are applicable to the different host species under practical circumstances.

[During consultation on draft recommendations, NL commented that it will be very difficult if not impossible to find production sites that are free, unless the plants are grown indoor in pots.] The Fruit SEWG considered that on one hand the pest has a very wide host range and is widespread in some countries (e.g. in NL); on the other hand, in other countries (e.g. in ES or other countries), soils are not so infested. But plant for planting is a significant pathway. It is an endoparasite, moving with plants for planting. It is difficult to see the symptoms since this involves uprooting the plant (only possible for Fragaria). The fruit SEWG considered that the decision should be taken later by risk managers on whether the measure is maintained to limit economic impact to end users or withdrawn to limit economic burden to the producer of plants for planting.

REFERENCES:
  • Aaltjesschema (2019). Website on information and crop rotation for various crops. The website is s product of Wageningen UR, nematology PPO-AGV. Website is accessible until 31 March 2024, only information for perennial plants and fruit crops will still be available. https://www.aaltjesschema.nl/Home.aspx
  • Abawi GS & Mai WF (2014) Root lesion nematodes (revised by Halbrendt JM). In Compendium of apple and pear diseases and pests, second edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, USA: 113-114.
  • Allen MW (1949). Root-lesion nematodes: resistant rootstocks most promising method of control. California Agriculture, January: 13-14.
  • Anonymous (1998) Pratylenchus on Oregon crops: Pratylenchus damage levels for Oregon crops: a literature survey. https://bpp.oregonstate.edu/pratylenchus-oregon-crops.
  • Anonymous (1999) Lesion nematodes. University of Illinois Extension. RPD, 1103. May 1999.
  • Askary TH, Banday SA, Iqbal U, Khan AA, Mir MM & Waliullah MIS (2012) Plant parasitic nematode diversity in pome, stone and nut fruits. In Agroecology and Strategies for Climate Change (ed Lichtfouse E). Springer Sicens+Business Media B.V. DOI 10.1007/978-94-007-1905-7_10. 237-268.
  • Barbosa P, Faria JMS, Figueiredo AC, Mota M & Vicente CSL (2022) Control of the root lesion Pratylenchus penetrans: the effect of nematicidal activity of plant-derived compounds. Revista de Ciencias Agrarias, 45 (4): 649-652. https://doi.org/10.19084/rca.28749
  • Bird GW & Melakeberhan H (1995) Root-Lesion Nematodes (Pratylenchus spp.). In Compendium of Stone Fruit Diseases (eds Ogawa JM, Zehr EI, Bird GW, Ritchie DF, Uriu K & Uyemoto JK)
  • Bucki P, Qing X, Castillo P, Gamliel A, Dobrinin S, Alon T, Miyara SB (2020) The genus Pratylenchus (Nematoda: Pratylenchidae) in Israel: from taxonomy to control practices. Plants 9, 1475; doi:10.3390/plants9111475.
  • Castillo P, Vovlas (2007) Biology and ecology of Pratylenchus. In “Pratylechus (Nematoda: Pratylenchidae): diagnosis, biology, pathogenicity and management”. Nematology Monographs & Perspective 6, 305-324.
  • Clavero-Camacho I, Archidona-Yuste A, Cantalapiedra-Navarrete C, Castillo P & Palomares-Rius JE (2024) Prevalence and ecological factors affecting the distribution of plant-parasitic nematodes in Prunus groves in Spain. Journal of Integrative Agriculture, 23(2): 585-589.
  • EPPO (2022) PM 4/17 (3) Certification scheme for olive trees and rootstocks. EPPO Bulletin 52, 590–60. DOI: 10.1111/epp.1288
  • Evenhuis A, Korthals G & Molendijk L. (2004). Tagetes patula as an effective catch crop for long-term control of Pratylenchus penetrans. Nematology, 6(6), 877-881. https://doi.org/10.1163/1568541044038632
  • Fatemy S (2009). Integrated management of pistachio nematodes. In Integrated Management of Fruit Crops and Forest Nematodes (eds Ciancio A & Mukerji KG). Springer Science+Business Media BV, 243-252.
  • Goodey JB, Franklin MT &Hooper DJ (1965) The nematode parasites of plants catalogued under their host. Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, England. Third Edition.
  • Hoestra H & Oostenbrink M (1962) Nematodes in relation to plant growth IV. Pratylenchus penetrans (Cobb) on orchard trees. Neth. J. agric. Sei., Vol. 10 (1962) No. 4 (November): 286-296
  • Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MGK, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WML & Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14 (9): 946-961.
  • Lehman PS (1994) Dissemination of phytoparasitic nematodes. Nematology Circular, No 28. Fla. Dept. Agric.& Consumer Services. Division of Plant Industry.
  • Lim G-E, Heo M-S & Park M-G (2024) Hot Water Treatment as a Quarantine Measure for Controlling Pratylenchus penetrans Cobb in Syngonium podophyllum Schott and Perilla frutescens Britton. Agriculture 14, 582. https://doi.org/10.3390/agriculture14040582.
  • Moens M & Perry RN (2009) Migratory plant endoparasitic nematodes: a group rich in contrasts and divergence. Annual Review of Phytopathology 47, 313–32.
  • NEMAPLEX (2024) Host Status of a Plant Genus and species to Nematodes. http://nemaplex.ucdavis.edu/ (accessed: 07/11/2024)
  • Nyczepir AP (1991) Nematode management strategies in stone fruits in the United States. Journal of Nematology 23(3), 334-341.
  • Mai WF & Abawi GS (1978) Determining the cause and extent of apple, cherry, and pear replant diseases under controlled conditions. Phytopathology 68, 1540-1544.
  • Merrifield K (2000) Plant-parasitic damage levels for Oregon nursery crops: A literature survey. Biology, host ranges, and damage levels of root-parasitic nematodes on Oregon nursery crops (Draft: 2000). https://bpp.oregonstate.edu/sites/agscid7/files/plant-parasitic-damage-levels-for-oregon-nursery-crops.pdf
  • Nyczepier A P & Halbrendt JM (1993) Nematode pests of deciduous fruit and nut trees. In Plant Parasitic Nematodes in Temperate Agriculture (eds Evans K, Trudgill DL & Webster JM). CAB International, Wallingford, England. pp. 381-425
  • PlantwisePlus Knowledge Bank (2023). Pratylenchus penetrans (nematode, northern root lesion). (accessed 26/Apr/2024). https://plantwiseplusknowledgebank.org/doi/full/10.1079/pwkb.species.43900
  • Pudasaini MP, Viaene N & Moens M (2006) Effect of marigold (Tagetes patula) on population dynamics of Pratylenchus penetrans in a field. Nematology 8, 477-84.
  • Schmitt DP & Sipes BS (2000) Plant-parasitic nematodes and their management. From “Plant Nutrient Management in Hawaii’s Soils, Approaches for Tropical and Subtropical Agriculture”. College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa.
  • Sharma GC, Thakur BS, Kashyap AS (2005) Impact of NPK on the nematode populations and yield of plum (Prunus salicina). SHS Acta Horticulturae, 696: VII International Symposium on Temperate Zone Fruits in the Tropics and Subtropics - Part Two. doi: 10.17660/ActaHortic.2005.696.77
  • Siddiqui IA, Sher SA & French AM (1973) Distribution of Plant Parasitic Nematodes in California. State of California Department of Food and Agriculture, Division of Plant Industry. 324p.
  • Söğüt MA, Devran Z, Arici ŞE, Şan B, Yildirim AN (2013) Host reactions of root lesion nematodes (Pratylenchus spp.) on the rootstocks of pome and stone. Turkish Journal of Entomology 37(2), 239-248.
  • Taning LM, Lippens L, Formesyn E, Wesemael W (2023) Impact of cover crops on population density of the root-lesion nematode Pratylenchus penetrans. Preprint DOI: https://doi.org/10.21203/rs.3.rs-3338686/v1
  • Townshend JL (1990) Growth of ‘Bartlett’ pear seedlings in response to number of root-lesions nematodes and temperature. HortSci, 25: 318-320
  • Yorston J M (1969). The interactions of Pratylenchus penetrans with host plants, Longidorus elongatus and Verticillium dahliae. PhD Thesis Oregon State University, 55 pp.

HOST PLANT N°5: Pistacia vera (PIAVE) 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

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:
 
Pratylenchus penetrans is cosmopolitan and has more than 350 hosts including woody plants (e.g., fruit trees, roses) and herbaceous plants (e.g., potato, vegetables) (Moens & Perry, 2009, CABI, 2021), e.g., Malus is a good host for Pratylenchus penetrans (aaltjesschema, 2019). Also Pyrus spp., Cydonia oblonga, Pistacia vera and many Prunus spp. can be hosts of P. penetrans (Hoekstra & Oostenbrink, 1962; Askary et al., 2012; Merrifield, 2000). Ficus carica is not mentioned as hosts and information of Pratylenchus penetrans on Pistacia vera is scarce (PlantwisePlus Knowledge Bank, 2023; Fatemy, 2009), this could be linked to P. penetrans being a nematode from mostly temperate climates and fig and pistachio being more Mediterranean crops. P. penetrans can complete its entire life cycle within the roots of plants.
Pratylenchus spp. are migratory endoparasites that enter the host root for feeding and reproduction and move freely within the tissue. Consequently, they spend much of their life cycle in roots and are found in soil when the host plants are senescing, stressed or diseased, or when their hosts have been ploughed up after harvest (Castillo and Vovlas, 2007).
P. penetrans occurs mostly on sandy and peaty soil. The transport of infected plants or those growing in infested soils is one of the principal means by which these nematodes are disseminated (Lehman, 1994; Anonymous, 1999). Bare-rooted plants are often contaminated by soil particles which may contain nematodes. Roots can host endoparasitic nematodes that are not removed by washing treatments (Lehman, 1994). In this context, it is essential that the plant propagation material be free of this pathogen (Allen, 1949). Because it can survive in soil, it can be dispersed by land vehicles etc.; within a field by cultivation, and can be introduced to non-infested sites by poorly sanitized farm equipment. However, measures (including hygiene) can limit the importance of such alternative pathways.
In responses to the questionnaire, DE, FR and NL supported deregulation in the EU because soilborne and widespread in production areas.
Considering the numerous bibliographic references that highlight the importance of plants for planting as an important pathway, and the existence of measures that can reduce the role of the others reported pathways, host plants for planting with roots, with or without soil or growing media, are considered as a main pathway.

5 - Economic impact:

Are there documented reports of any economic impact on the host?
 
No

Justification:
 
Although P. penetrans has been reported on Pistacia vera (Fatemy, 2009), details are not mentioned. Among the Pratylenchus species reported in the Mediterranean area causing damage on Pistacia vera, P. vulnus and P. penetrans are not included. Moreover, such records are restricted to Iran and Turkey (see references in Gusella et al., 2024). In Spain, there is no evidence of the regular presence of P. penetrans and P. vulnus in pistachio nurseries or plantations, and if they appear, their economic impact would be minimal (Martínez E. (IRIAF), pers. comm., 2024)
In the responses to the questionnaire, FR supported deregulation in the EU, commenting that the pest had a 'low nuisance level on fruit 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:
 
Not candidate

Justification:
 
The presence of this pest is not common under EU growing conditions. When reported, its impact on the crop is considered acceptable.

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:
 
Crop rotation is difficult because of the wide host range of Pratylenchus penetrans, including weeds. Pratylenchus penetrans can propagate well on many crops, sometimes without causing damage (symptomless) (aaltjesschema). Recent research indicated that with proper choice of selected cultivars of cover crops, P. penetrans can be controlled but further breeding efforts are needed. Although some cover crops can reduce the population of Pratylenchus penetrans (Taning et al., 2023). Since many weeds can also be a host, adequate weed control is important (Aaltjesschema, 2019). Crop rotation is also a limited option since woody crops remain in soil for decades and the host-range of many of this of the plant parasitic nematodes is wide (Castillo y Vovlas, 2007).

Growing Tagetes spp. (e.g. Tagetes patula) can reduce the population considerably (Evenhuis et al., 2004). The authors predicted that strawberries could be grown for about 7 successive years without economic damage due to the root lesion nematode. Pudasaini et al. (2006) showed that Tagetes can reduce P. penetrans exponentially in time under marigold. The effect of marigold was persistent as no increase in P. penetrans densities over the whole soil profile was noticed after two crop cycles of host plants.

Use of clean soil: The propagation material is kept either in containers of sterilized growing medium or in soil that has been tested and found free from various nematodes (e.g. EPPO 2022).

Soil fumigation: dependent on legislation. Preplant soil fumigation does not eradicate nematodes but dramatically reduces nematode numbers. The nematodes return to their original population density (or greater) within 2 or 3 years after planting, but the absence of nematode pressure during the initial years of establishment is critical for trees to develop strong, healthy root systems (Abawi & Mai, 2014). With the progressive phase-out of chemical nematicides such as Aldicarb, Carbofuran, and 1,3-Dichloropropene, the effectiveness and sustainability of current plant-parasitic nematode management strategies remain limited (Barbosa et al., 2022).

Healthy plants: To prevent the introduction of nematode problems, new orchards should be established with trees obtained from reputable nurseries that treat their soils for nematodes (Abawi & Mai, 2014).

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: the presence of this pest is not common under EU growing conditions. When reported, its impact on the crop is considered acceptable.


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:
  • Aaltjesschema (2019). Website on information and crop rotation for various crops. The website is s product of Wageningen UR, nematology PPO-AGV. Website is accessible until 31 March 2024, only information for perennial plants and fruit crops will still be available. https://www.aaltjesschema.nl/Home.aspx
  • Abawi GS & Mai WF (2014) Root lesion nematodes (revised by Halbrendt JM). In Compendium of apple and pear diseases and pests, second edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, USA: 113-114.
  • Allen MW (1949). Root-lesion nematodes: resistant rootstocks most promising method of control. California Agriculture, January: 13-14.
  • Anonymous (1998) Pratylenchus on Oregon crops: Pratylenchus damage levels for Oregon crops: a literature survey. https://bpp.oregonstate.edu/pratylenchus-oregon-crops.
  • Anonymous (1999) Lesion nematodes. University of Illinois Extension. RPD, 1103. May 1999.
  • Askary TH, Banday SA, Iqbal U, Khan AA, Mir MM & Waliullah MIS (2012) Plant parasitic nematode diversity in pome, stone and nut fruits. In Agroecology and Strategies for Climate Change (ed Lichtfouse E). Springer Sicens+Business Media B.V. DOI 10.1007/978-94-007-1905-7_10. 237-268.
  • Barbosa P, Faria JMS, Figueiredo AC, Mota M & Vicente CSL (2022) Control of the root lesion Pratylenchus penetrans: the effect of nematicidal activity of plant-derived compounds. Revista de Ciencias Agrarias, 45 (4): 649-652. https://doi.org/10.19084/rca.28749
  • Bird GW & Melakeberhan H (1995) Root-Lesion Nematodes (Pratylenchus spp.). In Compendium of Stone Fruit Diseases (eds Ogawa JM, Zehr EI, Bird GW, Ritchie DF, Uriu K & Uyemoto JK)
  • Bucki P, Qing X, Castillo P, Gamliel A, Dobrinin S, Alon T, Miyara SB (2020) The genus Pratylenchus (Nematoda: Pratylenchidae) in Israel: from taxonomy to control practices. Plants 9, 1475; doi:10.3390/plants9111475.
  • Castillo P, Vovlas (2007) Biology and ecology of Pratylenchus. In “Pratylechus (Nematoda: Pratylenchidae): diagnosis, biology, pathogenicity and management”. Nematology Monographs & Perspective 6, 305-324.
  • Clavero-Camacho I, Archidona-Yuste A, Cantalapiedra-Navarrete C, Castillo P & Palomares-Rius JE (2024) Prevalence and ecological factors affecting the distribution of plant-parasitic nematodes in Prunus groves in Spain. Journal of Integrative Agriculture, 23(2): 585-589.
  • EPPO (2022) PM 4/17 (3) Certification scheme for olive trees and rootstocks. EPPO Bulletin 52, 590–60. DOI: 10.1111/epp.1288
  • Evenhuis A, Korthals G & Molendijk L. (2004). Tagetes patula as an effective catch crop for long-term control of Pratylenchus penetrans. Nematology, 6(6), 877-881. https://doi.org/10.1163/1568541044038632
  • Fatemy S (2009). Integrated management of pistachio nematodes. In Integrated Management of Fruit Crops and Forest Nematodes (eds Ciancio A & Mukerji KG). Springer Science+Business Media BV, 243-252.
  • Goodey JB, Franklin MT &Hooper DJ (1965) The nematode parasites of plants catalogued under their host. Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, England. Third Edition.
  • Gusella G, López-Moral A, Antón-Domínguez BI, Trapero C, Polizzi G, Trapero A, Michailides TJ & Agustí-Brisach C (2024) Current status of pistachio diseases in countries of the Mediterranean Basin. Plant Pathology 00, 1–25. doi: 10.1111/ppa.13962.
  • Hoestra H & Oostenbrink M (1962) Nematodes in relation to plant growth IV. Pratylenchus penetrans (Cobb) on orchard trees. Neth. J. agric. Sei., Vol. 10 (1962) No. 4 (November): 286-296
  • Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MGK, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WML & Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14 (9): 946-961.
  • Lehman PS (1994) Dissemination of phytoparasitic nematodes. Nematology Circular, No 28. Fla. Dept. Agric.& Consumer Services. Division of Plant Industry.
  • Moens M & Perry RN (2009) Migratory plant endoparasitic nematodes: a group rich in contrasts and divergence. Annual Review of Phytopathology 47, 313–32.
  • NEMAPLEX (2024) Host Status of a Plant Genus and species to Nematodes. http://nemaplex.ucdavis.edu/ (accessed: 07/11/2024)
  • Nyczepir AP (1991) Nematode management strategies in stone fruits in the United States. Journal of Nematology 23(3), 334-341.
  • Mai WF & Abawi GS (1978) Determining the cause and extent of apple, cherry, and pear replant diseases under controlled conditions. Phytopathology 68, 1540-1544.
  • Merrifield K (2000) Plant-parasitic damage levels for Oregon nursery crops: A literature survey. Biology, host ranges, and damage levels of root-parasitic nematodes on Oregon nursery crops (Draft: 2000). https://bpp.oregonstate.edu/sites/agscid7/files/plant-parasitic-damage-levels-for-oregon-nursery-crops.pdf
  • Nyczepier A P & Halbrendt JM (1993) Nematode pests of deciduous fruit and nut trees. In Plant Parasitic Nematodes in Temperate Agriculture (eds Evans K, Trudgill DL & Webster JM). CAB International, Wallingford, England. pp. 381-425
  • PlantwisePlus Knowledge Bank (2023). Pratylenchus penetrans (nematode, northern root lesion). (accessed 26/Apr/2024). https://plantwiseplusknowledgebank.org/doi/full/10.1079/pwkb.species.43900
  • Pudasaini MP, Viaene N & Moens M (2006) Effect of marigold (Tagetes patula) on population dynamics of Pratylenchus penetrans in a field. Nematology 8, 477-84.
  • Schmitt DP & Sipes BS (2000) Plant-parasitic nematodes and their management. From “Plant Nutrient Management in Hawaii’s Soils, Approaches for Tropical and Subtropical Agriculture”. College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa.
  • Sharma GC, Thakur BS, Kashyap AS (2005) Impact of NPK on the nematode populations and yield of plum (Prunus salicina). SHS Acta Horticulturae, 696: VII International Symposium on Temperate Zone Fruits in the Tropics and Subtropics - Part Two. doi: 10.17660/ActaHortic.2005.696.77
  • Siddiqui IA, Sher SA & French AM (1973) Distribution of Plant Parasitic Nematodes in California. State of California Department of Food and Agriculture, Division of Plant Industry. 324p.
  • Söğüt MA, Devran Z, Arici ŞE, Şan B, Yildirim AN (2013) Host reactions of root lesion nematodes (Pratylenchus spp.) on the rootstocks of pome and stone. Turkish Journal of Entomology 37(2), 239-248.
  • Taning LM, Lippens L, Formesyn E, Wesemael W (2023) Impact of cover crops on population density of the root-lesion nematode Pratylenchus penetrans. Preprint DOI: https://doi.org/10.21203/rs.3.rs-3338686/v1
  • Townshend JL (1990) Growth of ‘Bartlett’ pear seedlings in response to number of root-lesions nematodes and temperature. HortSci, 25: 318-320
  • Yorston J M (1969). The interactions of Pratylenchus penetrans with host plants, Longidorus elongatus and Verticillium dahliae. PhD Thesis Oregon State University, 55 pp.

HOST PLANT N°6: Prunus armeniaca (PRNAR) 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):
 
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):
 
Yes
 
Conclusion:
 
Candidate

 
Justification:
 
Pratylenchus penetrans is cosmopolitan and has more than 350 hosts including woody plants (e.g., fruit trees, roses) and herbaceous plants (e.g., potato, vegetables) (Moens & Perry, 2009, CABI, 2021), e.g., Malus is a good host for Pratylenchus penetrans (aaltjesschema, 2019). Also Pyrus spp., Cydonia oblonga, Pistacia vera and many Prunus spp. can be hosts of P. penetrans (Hoekstra & Oostenbrink, 1962; Askary et al., 2012; Merrifield, 2000). Ficus carica is not mentioned as hosts and information of Pratylenchus penetrans on Pistacia vera is scarce (PlantwisePlus Knowledge Bank, 2023; Fatemy, 2009), this could be linked to P. penetrans being a nematode from mostly temperate climates and fig and pistachio being more Mediterranean crops. P. penetrans can complete its entire life cycle within the roots of plants.
Pratylenchus spp. are migratory endoparasites that enter the host root for feeding and reproduction and move freely within the tissue. Consequently, they spend much of their life cycle in roots and are found in soil when the host plants are senescing, stressed or diseased, or when their hosts have been ploughed up after harvest (Castillo and Vovlas, 2007).
P. penetrans occurs mostly on sandy and peaty soil. The transport of infected plants or those growing in infested soils is one of the principal means by which these nematodes are disseminated (Lehman, 1994; Anonymous, 1999). Bare-rooted plants are often contaminated by soil particles which may contain nematodes. Roots can host endoparasitic nematodes that are not removed by washing treatments (Lehman, 1994). In this context, it is essential that the plant propagation material be free of this pathogen (Allen, 1949). Because it can survive in soil, it can be dispersed by land vehicles etc.; within a field by cultivation, and can be introduced to non-infested sites by poorly sanitized farm equipment. However, measures (including hygiene) can limit the importance of such alternative pathways.
In responses to the questionnaire, DE, FR and NL supported deregulation in the EU because soilborne and widespread in production areas.
Considering the numerous bibliographic references that highlight the importance of plants for planting as an important pathway, and the existence of measures that can reduce the role of the others reported pathways, host plants for planting with roots, with or without soil or growing media, are a considered as a main pathway.

5 - Economic impact:

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

Justification:
 
Pratylenchus penetrans is well recognized as economically important pest of stone-fruits (Mai and Parker, 1967; Townshend, 1990; Clavero-Camacho et al., 2024).
Much of the damage caused by root-lesion nematodes in stone fruits (Prunus spp.) results from their ability to induce extensive root necrosis. Nematode invasion of young roots induces reddish brown, elongated lesions. Root lesions darken with age, necrosis often spreads to affect the entire root, growth ceases, and the root dies. Severe infection may destroy the fine roots. Heavy infections often result in small root systems and stunted trees. Symptoms are more common on young trees than on old trees (Bird & Melakeberhan, 1995).
Depending on the level of P. penetrans present in the soil, damage might occur :
- Prunus dulcis: in the NEMAPLEX (2024) database, Prunus dulcis is reported as susceptible (= high level of nematode reproduction) to Pratylenchus penetrans (Siddiqui et al., 1973).
- Prunus armeniaca & Prunus domestica: mentioned as host. In the NEMAPLEX (2024) database, Prunus armeniaca is reported as susceptible (= high level of nematode reproduction) to Pratylenchus penetrans (Siddiqui et al., 1973).
- Prunus avium & Prunus cerasus: Initial population of 80/100 g soil necessary for growth reduction (Nyczepir and Halbrendt 1993). In NE U.S., reduced yield and shortened productive life of Montmorency cherry on Mazard and Mahaleb rootstocks; parasitized trees were less winter hardy (Nyczepir and Halbrendt 1993). In pots, seedlings grown for 12 weeks in steam-fumigated orchard soil with a history of replant disease containing a mixed population of 7 P. penetrans and P. projectus/100 g weighed 46% more and were 64% taller than seedlings grown in non-treated soil (Mai and Abawi 1978), (Cited in Merrifield, 2000). Pratylenchus penetrans has been responsible for severe decline and for replating failure in many cherry orchards. Also, this nematode can lower the resistance of plants to other pathogens (Anonymous, 1999).
- Prunus cerasifera: Initial population of 320/100 g soil necessary for growth reduction (Nyczepir and Halbrendt 1993). (Cited in Merrifield, 2000)
- Prunus persica: 5/100 g soil (Barker et al. 1976). Root impairment results in loss of vigour and yields of mature trees, but P. penetrans’ role in orchard replant problems is probably more economically important (Nyczepir and Halbrendt 1993). Pratylenchus penetrans has been responsible for severe decline and for replating failure in many peach orchards. Also, this nematode can lower the resistance of plants to other pathogens (Anonymous, 1999). In pots, seedling height was significantly reduced 40% by 114/100 cm3, 60% by 228/100 cm3, and 75% by 457/100 cm3 (Cited in Merrifield, 2000).
- Prunus salicina: In a Prunus salicina (var. Santa Rosa) orchard located in India, Pratylenchus penetrans was the predominant plant-parasitic nematode, with populations of 150-380 nematodes per 200 cc soil (Sharma et al., 2005).
In the responses to the questionnaire, FR supported deregulation in the EU, commenting that the pest had a 'low nuisance level on fruit plants'.

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 
Medium to 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?
 
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:
 
Evidence of its economic impact is available in the literature and confirmed by Spanish experts.
The damage caused by Pratylenchus is usually most severe in light-textured soils that are low in nutrients (e.g. nitrogen, potassium, or calcium) and in organic matter (Anonymous, 1999). pH and soil texture were the most influential variables in Pratylenchus distribution and abundance during the study of Clavero-Camacho et al. (2024) on plant parasitic nematodes affecting Prunus species in Spain.

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:
 
Crop rotation is difficult because of the wide host range of Pratylenchus penetrans, including weeds. Pratylenchus penetrans can propagate well on many crops, sometimes without causing damage (symptomless) (aaltjesschema). Recent research indicated that with proper choice of selected cultivars of cover crops, P. penetrans can be controlled but further breeding efforts are needed. Although some cover crops can reduce the population of Pratylenchus penetrans (Taning et al., 2023). Since many weeds can also be a host, adequate weed control is important (Aaltjesschema, 2019). Crop rotation is also a limited option since woody crops remain in soil for decades and the host-range of many of this of the plant parasitic nematodes is wide (Castillo y Vovlas, 2007).

Growing Tagetes spp. (e.g. Tagetes patula) can reduce the population considerably (Evenhuis et al., 2004). The authors predicted that strawberries could be grown for about 7 successive years without economic damage due to the root lesion nematode. Pudasaini et al. (2006) showed that Tagetes can reduce P. penetrans exponentially in time under marigold. The effect of marigold was persistent as no increase in P. penetrans densities over the whole soil profile was noticed after two crop cycles of host plants.

Use of clean soil: The propagation material is kept either in containers of sterilized growing medium or in soil that has been tested and found free from various nematodes (e.g. EPPO 2022).

Soil fumigation: dependent on legislation. Preplant soil fumigation does not eradicate nematodes but dramatically reduces nematode numbers. The nematodes return to their original population density (or greater) within 2 or 3 years after planting, but the absence of nematode pressure during the initial years of establishment is critical for trees to develop strong, healthy root systems (Abawi & Mai, 2014). With the progressive phase-out of chemical nematicides such as Aldicarb, Carbofuran, and 1,3-Dichloropropene, the effectiveness and sustainability of current plant-parasitic nematode management strategies remain limited (Barbosa et al., 2022).

Healthy plants: To prevent the introduction of nematode problems, new orchards should be established with trees obtained from reputable nurseries that treat their soils for nematodes (Abawi & Mai, 2014).

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.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
Yes

Proposed Risk management measure:
 
Non-Certified material (‘Conformitas Agraria Communitatis (CAC)’):
• Mother plants have been produced in a pest free place/site of production
or
• Material obtained from mother plants does not contain roots and soil

AND

• Plants have been produced in soil/growing medium considered free from P. penetrans (e.g. tested soil, use of sterilized growing media or soil-free).

Justification (if necessary):
 
The risk of transmission of this nematode is restricted to materials with roots and soil. Generally, material obtained from mother plants (e.g. buds, cuttings...) doesn’t contain roots and soil. The critical point to avoid the spread of this pest is in the nurseries where certified and CAC seedlings are produced for marketing to growers or end users. Considering that symptoms may not be visible, that symptomology is non-specific (both above and below ground) and the complexity to perform laboratory testing, the fruit SEWG considered that PFA should not be proposed as an option. The Fruit SEWG also considered that an option requiring not growing hosts during > 5 years was not realistic considering how polyphagous the pest is.
Hot water treatments with some time-temperature schedules have been shown to be effective against the pest (Anonymous, 1999; Lim et al., 2024). Further work would be needed to validate if these schedules are applicable to the different host species under practical circumstances.

[During consultation on draft recommendations, NL commented that it will be very difficult if not impossible to find production sites that are free, unless the plants are grown indoor in pots.] The Fruit SEWG considered that on one hand the pest has a very wide host range and is widespread in some countries (e.g. in NL); on the other hand, in other countries (e.g. in ES or other countries), soils are not so infested. But plant for planting is a significant pathway. It is an endoparasite, moving with plants for planting. It is difficult to see the symptoms since this involves uprooting the plant (only possible for Fragaria). The fruit SEWG considered that the decision should be taken later by risk managers on whether the measure is maintained to limit economic impact to end users or withdrawn to limit economic burden to the producer of plants for planting.

REFERENCES:
  • Aaltjesschema (2019). Website on information and crop rotation for various crops. The website is s product of Wageningen UR, nematology PPO-AGV. Website is accessible until 31 March 2024, only information for perennial plants and fruit crops will still be available. https://www.aaltjesschema.nl/Home.aspx
  • Abawi GS & Mai WF (2014) Root lesion nematodes (revised by Halbrendt JM). In Compendium of apple and pear diseases and pests, second edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, USA: 113-114.
  • Allen MW (1949). Root-lesion nematodes: resistant rootstocks most promising method of control. California Agriculture, January: 13-14.
  • Anonymous (1998) Pratylenchus on Oregon crops: Pratylenchus damage levels for Oregon crops: a literature survey. https://bpp.oregonstate.edu/pratylenchus-oregon-crops.
  • Anonymous (1999) Lesion nematodes. University of Illinois Extension. RPD, 1103. May 1999.
  • Askary TH, Banday SA, Iqbal U, Khan AA, Mir MM & Waliullah MIS (2012) Plant parasitic nematode diversity in pome, stone and nut fruits. In Agroecology and Strategies for Climate Change (ed Lichtfouse E). Springer Sicens+Business Media B.V. DOI 10.1007/978-94-007-1905-7_10. 237-268.
  • Barbosa P, Faria JMS, Figueiredo AC, Mota M & Vicente CSL (2022) Control of the root lesion Pratylenchus penetrans: the effect of nematicidal activity of plant-derived compounds. Revista de Ciencias Agrarias, 45 (4): 649-652. https://doi.org/10.19084/rca.28749
  • Bird GW & Melakeberhan H (1995) Root-Lesion Nematodes (Pratylenchus spp.). In Compendium of Stone Fruit Diseases (eds Ogawa JM, Zehr EI, Bird GW, Ritchie DF, Uriu K & Uyemoto JK)
  • Bucki P, Qing X, Castillo P, Gamliel A, Dobrinin S, Alon T, Miyara SB (2020) The genus Pratylenchus (Nematoda: Pratylenchidae) in Israel: from taxonomy to control practices. Plants 9, 1475; doi:10.3390/plants9111475.
  • Castillo P, Vovlas (2007) Biology and ecology of Pratylenchus. In “Pratylechus (Nematoda: Pratylenchidae): diagnosis, biology, pathogenicity and management”. Nematology Monographs & Perspective 6, 305-324.
  • Clavero-Camacho I, Archidona-Yuste A, Cantalapiedra-Navarrete C, Castillo P & Palomares-Rius JE (2024) Prevalence and ecological factors affecting the distribution of plant-parasitic nematodes in Prunus groves in Spain. Journal of Integrative Agriculture, 23(2): 585-589.
  • EPPO (2022) PM 4/17 (3) Certification scheme for olive trees and rootstocks. EPPO Bulletin 52, 590–60. DOI: 10.1111/epp.1288
  • Evenhuis A, Korthals G & Molendijk L. (2004). Tagetes patula as an effective catch crop for long-term control of Pratylenchus penetrans. Nematology, 6(6), 877-881. https://doi.org/10.1163/1568541044038632
  • Fatemy S (2009). Integrated management of pistachio nematodes. In Integrated Management of Fruit Crops and Forest Nematodes (eds Ciancio A & Mukerji KG). Springer Science+Business Media BV, 243-252.
  • Goodey JB, Franklin MT &Hooper DJ (1965) The nematode parasites of plants catalogued under their host. Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, England. Third Edition.
  • Hoestra H & Oostenbrink M (1962) Nematodes in relation to plant growth IV. Pratylenchus penetrans (Cobb) on orchard trees. Neth. J. agric. Sei., Vol. 10 (1962) No. 4 (November): 286-296
  • Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MGK, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WML & Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14 (9): 946-961.
  • Lehman PS (1994) Dissemination of phytoparasitic nematodes. Nematology Circular, No 28. Fla. Dept. Agric.& Consumer Services. Division of Plant Industry.
  • Lim G-E, Heo M-S & Park M-G (2024) Hot Water Treatment as a Quarantine Measure for Controlling Pratylenchus penetrans Cobb in Syngonium podophyllum Schott and Perilla frutescens Britton. Agriculture 14, 582. https://doi.org/10.3390/agriculture14040582.
  • Moens M & Perry RN (2009) Migratory plant endoparasitic nematodes: a group rich in contrasts and divergence. Annual Review of Phytopathology 47, 313–32.
  • NEMAPLEX (2024) Host Status of a Plant Genus and species to Nematodes. http://nemaplex.ucdavis.edu/ (accessed: 07/11/2024)
  • Nyczepir AP (1991) Nematode management strategies in stone fruits in the United States. Journal of Nematology 23(3), 334-341.
  • Mai WF & Abawi GS (1978) Determining the cause and extent of apple, cherry, and pear replant diseases under controlled conditions. Phytopathology 68, 1540-1544.
  • Merrifield K (2000) Plant-parasitic damage levels for Oregon nursery crops: A literature survey. Biology, host ranges, and damage levels of root-parasitic nematodes on Oregon nursery crops (Draft: 2000). https://bpp.oregonstate.edu/sites/agscid7/files/plant-parasitic-damage-levels-for-oregon-nursery-crops.pdf
  • Nyczepier A P & Halbrendt JM (1993) Nematode pests of deciduous fruit and nut trees. In Plant Parasitic Nematodes in Temperate Agriculture (eds Evans K, Trudgill DL & Webster JM). CAB International, Wallingford, England. pp. 381-425
  • PlantwisePlus Knowledge Bank (2023). Pratylenchus penetrans (nematode, northern root lesion). (accessed 26/Apr/2024). https://plantwiseplusknowledgebank.org/doi/full/10.1079/pwkb.species.43900
  • Pudasaini MP, Viaene N & Moens M (2006) Effect of marigold (Tagetes patula) on population dynamics of Pratylenchus penetrans in a field. Nematology 8, 477-84.
  • Schmitt DP & Sipes BS (2000) Plant-parasitic nematodes and their management. From “Plant Nutrient Management in Hawaii’s Soils, Approaches for Tropical and Subtropical Agriculture”. College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa.
  • Sharma GC, Thakur BS, Kashyap AS (2005) Impact of NPK on the nematode populations and yield of plum (Prunus salicina). SHS Acta Horticulturae, 696: VII International Symposium on Temperate Zone Fruits in the Tropics and Subtropics - Part Two. doi: 10.17660/ActaHortic.2005.696.77
  • Siddiqui IA, Sher SA & French AM (1973) Distribution of Plant Parasitic Nematodes in California. State of California Department of Food and Agriculture, Division of Plant Industry. 324p.
  • Söğüt MA, Devran Z, Arici ŞE, Şan B, Yildirim AN (2013) Host reactions of root lesion nematodes (Pratylenchus spp.) on the rootstocks of pome and stone. Turkish Journal of Entomology 37(2), 239-248.
  • Taning LM, Lippens L, Formesyn E, Wesemael W (2023) Impact of cover crops on population density of the root-lesion nematode Pratylenchus penetrans. Preprint DOI: https://doi.org/10.21203/rs.3.rs-3338686/v1
  • Townshend JL (1990) Growth of ‘Bartlett’ pear seedlings in response to number of root-lesions nematodes and temperature. HortSci, 25: 318-320
  • Yorston J M (1969). The interactions of Pratylenchus penetrans with host plants, Longidorus elongatus and Verticillium dahliae. PhD Thesis Oregon State University, 55 pp.

HOST PLANT N°7: Prunus avium (PRNAV) 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):
 
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):
 
Yes
 
Conclusion:
 
Candidate

 
Justification:
 
Pratylenchus penetrans is cosmopolitan and has more than 350 hosts including woody plants (e.g., fruit trees, roses) and herbaceous plants (e.g., potato, vegetables) (Moens & Perry, 2009, CABI, 2021), e.g., Malus is a good host for Pratylenchus penetrans (aaltjesschema, 2019). Also Pyrus spp., Cydonia oblonga, Pistacia vera and many Prunus spp. can be hosts of P. penetrans (Hoekstra & Oostenbrink, 1962; Askary et al., 2012; Merrifield, 2000). Ficus carica is not mentioned as hosts and information of Pratylenchus penetrans on Pistacia vera is scarce (PlantwisePlus Knowledge Bank, 2023; Fatemy, 2009), this could be linked to P. penetrans being a nematode from mostly temperate climates and fig and pistachio being more Mediterranean crops. P. penetrans can complete its entire life cycle within the roots of plants.
Pratylenchus spp. are migratory endoparasites that enter the host root for feeding and reproduction and move freely within the tissue. Consequently, they spend much of their life cycle in roots and are found in soil when the host plants are senescing, stressed or diseased, or when their hosts have been ploughed up after harvest (Castillo and Vovlas, 2007).
P. penetrans occurs mostly on sandy and peaty soil. The transport of infected plants or those growing in infested soils is one of the principal means by which these nematodes are disseminated (Lehman, 1994; Anonymous, 1999). Bare-rooted plants are often contaminated by soil particles which may contain nematodes. Roots can host endoparasitic nematodes that are not removed by washing treatments (Lehman, 1994). In this context, it is essential that the plant propagation material be free of this pathogen (Allen, 1949). Because it can survive in soil, it can be dispersed by land vehicles etc.; within a field by cultivation, and can be introduced to non-infested sites by poorly sanitized farm equipment. However, measures (including hygiene) can limit the importance of such alternative pathways.
In responses to the questionnaire, DE, FR and NL supported deregulation in the EU because soilborne and widespread in production areas.
Considering the numerous bibliographic references that highlight the importance of plants for planting as an important pathway, and the existence of measures that can reduce the role of the others reported pathways, host plants for planting with roots, with or without soil or growing media, are considered as a main pathway.

5 - Economic impact:

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

Justification:
 
Pratylenchus penetrans is well recognized as economically important pest of stone-fruits (Mai and Parker, 1967; Townshend, 1990; Clavero-Camacho et al., 2024).
Much of the damage caused by root-lesion nematodes in stone fruits (Prunus spp.) results from their ability to induce extensive root necrosis. Nematode invasion of young roots induces reddish brown, elongated lesions. Root lesions darken with age, necrosis often spreads to affect the entire root, growth ceases, and the root dies. Severe infection may destroy the fine roots. Heavy infections often result in small root systems and stunted trees. Symptoms are more common on young trees than on old trees (Bird & Melakeberhan, 1995).
Depending on the level of P. penetrans present in the soil, damage might occur :
- Prunus dulcis: in the NEMAPLEX (2024) database, Prunus dulcis is reported as susceptible (= high level of nematode reproduction) to Pratylenchus penetrans (Siddiqui et al., 1973).
- Prunus armeniaca & Prunus domestica: mentioned as host. In the NEMAPLEX (2024) database, Prunus armeniaca is reported as susceptible (= high level of nematode reproduction) to Pratylenchus penetrans (Siddiqui et al., 1973).
- Prunus avium & Prunus cerasus: Initial population of 80/100 g soil necessary for growth reduction (Nyczepir and Halbrendt 1993). In NE U.S., reduced yield and shortened productive life of Montmorency cherry on Mazard and Mahaleb rootstocks; parasitized trees were less winter hardy (Nyczepir and Halbrendt 1993). In pots, seedlings grown for 12 weeks in steam-fumigated orchard soil with a history of replant disease containing a mixed population of 7 P. penetrans and P. projectus/100 g weighed 46% more and were 64% taller than seedlings grown in non-treated soil (Mai and Abawi 1978), (Cited in Merrifield, 2000). Pratylenchus penetrans has been responsible for severe decline and for replating failure in many cherry orchards. Also, this nematode can lower the resistance of plants to other pathogens (Anonymous, 1999).
- Prunus cerasifera: Initial population of 320/100 g soil necessary for growth reduction (Nyczepir and Halbrendt 1993). (Cited in Merrifield, 2000)
- Prunus persica: 5/100 g soil (Barker et al. 1976). Root impairment results in loss of vigour and yields of mature trees, but P. penetrans’ role in orchard replant problems is probably more economically important (Nyczepir and Halbrendt 1993). Pratylenchus penetrans has been responsible for severe decline and for replating failure in many peach orchards. Also, this nematode can lower the resistance of plants to other pathogens (Anonymous, 1999). In pots, seedling height was significantly reduced 40% by 114/100 cm3, 60% by 228/100 cm3, and 75% by 457/100 cm3 (Cited in Merrifield, 2000).
- Prunus salicina: In a Prunus salicina (var. Santa Rosa) orchard located in India, Pratylenchus penetrans was the predominant plant-parasitic nematode, with populations of 150-380 nematodes per 200 cc soil (Sharma et al., 2005).
In the responses to the questionnaire, FR supported deregulation in the EU, commenting that the pest had a 'low nuisance level on fruit plants'.

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 
Medium to 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?
 
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:
 
Evidence of its economic impact is available in the literature and confirmed by Spanish experts.
The damage caused by Pratylenchus is usually most severe in light-textured soils that are low in nutrients (e.g. nitrogen, potassium, or calcium) and in organic matter (Anonymous, 1999). pH and soil texture were the most influential variables in Pratylenchus distribution and abundance during the study of Clavero-Camacho et al. (2024) on plant parasitic nematodes affecting Prunus species in Spain.

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:
 
Crop rotation is difficult because of the wide host range of Pratylenchus penetrans, including weeds. Pratylenchus penetrans can propagate well on many crops, sometimes without causing damage (symptomless) (aaltjesschema). Recent research indicated that with proper choice of selected cultivars of cover crops, P. penetrans can be controlled but further breeding efforts are needed. Although some cover crops can reduce the population of Pratylenchus penetrans (Taning et al., 2023). Since many weeds can also be a host, adequate weed control is important (Aaltjesschema, 2019). Crop rotation is also a limited option since woody crops remain in soil for decades and the host-range of many of this of the plant parasitic nematodes is wide (Castillo y Vovlas, 2007).

Growing Tagetes spp. (e.g. Tagetes patula) can reduce the population considerably (Evenhuis et al., 2004). The authors predicted that strawberries could be grown for about 7 successive years without economic damage due to the root lesion nematode. Pudasaini et al. (2006) showed that Tagetes can reduce P. penetrans exponentially in time under marigold. The effect of marigold was persistent as no increase in P. penetrans densities over the whole soil profile was noticed after two crop cycles of host plants.

Use of clean soil: The propagation material is kept either in containers of sterilized growing medium or in soil that has been tested and found free from various nematodes (e.g. EPPO 2022).

Soil fumigation: dependent on legislation. Preplant soil fumigation does not eradicate nematodes but dramatically reduces nematode numbers. The nematodes return to their original population density (or greater) within 2 or 3 years after planting, but the absence of nematode pressure during the initial years of establishment is critical for trees to develop strong, healthy root systems (Abawi & Mai, 2014). With the progressive phase-out of chemical nematicides such as Aldicarb, Carbofuran, and 1,3-Dichloropropene, the effectiveness and sustainability of current plant-parasitic nematode management strategies remain limited (Barbosa et al., 2022).

Healthy plants: To prevent the introduction of nematode problems, new orchards should be established with trees obtained from reputable nurseries that treat their soils for nematodes (Abawi & Mai, 2014).

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.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
Yes

Proposed Risk management measure:
 
Non-Certified material (‘Conformitas Agraria Communitatis (CAC)’):
• Mother plants have been produced in a pest free place/site of production
or
• Material obtained from mother plants does not contain roots and soil

AND

• Plants have been produced in soil/growing medium considered free from P. penetrans (e.g. tested soil, use of sterilized growing media or soil-free).

Justification (if necessary):
 
The risk of transmission of this nematode is restricted to materials with roots and soil. Generally, material obtained from mother plants (e.g. buds, cuttings...) doesn’t contain roots and soil. The critical point to avoid the spread of this pest is in the nurseries where certified and CAC seedlings are produced for marketing to growers or end users. Considering that detection by inspection is practically impossible when no symptoms are observed, that symptomology is non-specific (both above and below ground) and the complexity to perform laboratory testing, the fruit SEWG considered that PFA should not be proposed as an option. The Fruit SEWG also considered that an option requiring not growing hosts during > 5 years was not realistic considering how polyphagous the pest is.
Hot water treatments with some time-temperature schedules have been shown to be effective against the pest (Anonymous, 1999; Lim et al., 2024). Further work would be needed to validate if these schedules are applicable to the different host species under practical circumstances.

[During consultation on draft recommendations, NL commented that it will be very difficult if not impossible to find production sites that are free, unless the plants are grown indoor in pots.] The Fruit SEWG considered that on one hand the pest has a very wide host range and is widespread in some countries (e.g. in NL); on the other hand, in other countries (e.g. in ES or other countries), soils are not so infested. But plant for planting is a significant pathway. It is an endoparasite, moving with plants for planting. It is difficult to see the symptoms since this involves uprooting the plant (only possible for Fragaria). The fruit SEWG considered that the decision should be taken later by risk managers on whether the measure is maintained to limit economic impact to end users or withdrawn to limit economic burden to the producer of plants for planting.

REFERENCES:
  • Aaltjesschema (2019). Website on information and crop rotation for various crops. The website is s product of Wageningen UR, nematology PPO-AGV. Website is accessible until 31 March 2024, only information for perennial plants and fruit crops will still be available. https://www.aaltjesschema.nl/Home.aspx
  • Abawi GS & Mai WF (2014) Root lesion nematodes (revised by Halbrendt JM). In Compendium of apple and pear diseases and pests, second edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, USA: 113-114.
  • Allen MW (1949). Root-lesion nematodes: resistant rootstocks most promising method of control. California Agriculture, January: 13-14.
  • Anonymous (1998) Pratylenchus on Oregon crops: Pratylenchus damage levels for Oregon crops: a literature survey. https://bpp.oregonstate.edu/pratylenchus-oregon-crops.
  • Anonymous (1999) Lesion nematodes. University of Illinois Extension. RPD, 1103. May 1999.
  • Askary TH, Banday SA, Iqbal U, Khan AA, Mir MM & Waliullah MIS (2012) Plant parasitic nematode diversity in pome, stone and nut fruits. In Agroecology and Strategies for Climate Change (ed Lichtfouse E). Springer Sicens+Business Media B.V. DOI 10.1007/978-94-007-1905-7_10. 237-268.
  • Barbosa P, Faria JMS, Figueiredo AC, Mota M & Vicente CSL (2022) Control of the root lesion Pratylenchus penetrans: the effect of nematicidal activity of plant-derived compounds. Revista de Ciencias Agrarias, 45 (4): 649-652. https://doi.org/10.19084/rca.28749
  • Bird GW & Melakeberhan H (1995) Root-Lesion Nematodes (Pratylenchus spp.). In Compendium of Stone Fruit Diseases (eds Ogawa JM, Zehr EI, Bird GW, Ritchie DF, Uriu K & Uyemoto JK)
  • Bucki P, Qing X, Castillo P, Gamliel A, Dobrinin S, Alon T, Miyara SB (2020) The genus Pratylenchus (Nematoda: Pratylenchidae) in Israel: from taxonomy to control practices. Plants 9, 1475; doi:10.3390/plants9111475.
  • Castillo P, Vovlas (2007) Biology and ecology of Pratylenchus. In “Pratylechus (Nematoda: Pratylenchidae): diagnosis, biology, pathogenicity and management”. Nematology Monographs & Perspective 6, 305-324.
  • Clavero-Camacho I, Archidona-Yuste A, Cantalapiedra-Navarrete C, Castillo P & Palomares-Rius JE (2024) Prevalence and ecological factors affecting the distribution of plant-parasitic nematodes in Prunus groves in Spain. Journal of Integrative Agriculture, 23(2): 585-589.
  • EPPO (2022) PM 4/17 (3) Certification scheme for olive trees and rootstocks. EPPO Bulletin 52, 590–60. DOI: 10.1111/epp.1288
  • Evenhuis A, Korthals G & Molendijk L. (2004). Tagetes patula as an effective catch crop for long-term control of Pratylenchus penetrans. Nematology, 6(6), 877-881. https://doi.org/10.1163/1568541044038632
  • Fatemy S (2009). Integrated management of pistachio nematodes. In Integrated Management of Fruit Crops and Forest Nematodes (eds Ciancio A & Mukerji KG). Springer Science+Business Media BV, 243-252.
  • Goodey JB, Franklin MT &Hooper DJ (1965) The nematode parasites of plants catalogued under their host. Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, England. Third Edition.
  • Hoestra H & Oostenbrink M (1962) Nematodes in relation to plant growth IV. Pratylenchus penetrans (Cobb) on orchard trees. Neth. J. agric. Sei., Vol. 10 (1962) No. 4 (November): 286-296
  • Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MGK, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WML & Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14 (9): 946-961.
  • Lehman PS (1994) Dissemination of phytoparasitic nematodes. Nematology Circular, No 28. Fla. Dept. Agric.& Consumer Services. Division of Plant Industry.
  • Lim G-E, Heo M-S & Park M-G (2024) Hot Water Treatment as a Quarantine Measure for Controlling Pratylenchus penetrans Cobb in Syngonium podophyllum Schott and Perilla frutescens Britton. Agriculture 14, 582. https://doi.org/10.3390/agriculture14040582.
  • Moens M & Perry RN (2009) Migratory plant endoparasitic nematodes: a group rich in contrasts and divergence. Annual Review of Phytopathology 47, 313–32.
  • NEMAPLEX (2024) Host Status of a Plant Genus and species to Nematodes. http://nemaplex.ucdavis.edu/ (accessed: 07/11/2024)
  • Nyczepir AP (1991) Nematode management strategies in stone fruits in the United States. Journal of Nematology 23(3), 334-341.
  • Mai WF & Abawi GS (1978) Determining the cause and extent of apple, cherry, and pear replant diseases under controlled conditions. Phytopathology 68, 1540-1544.
  • Merrifield K (2000) Plant-parasitic damage levels for Oregon nursery crops: A literature survey. Biology, host ranges, and damage levels of root-parasitic nematodes on Oregon nursery crops (Draft: 2000). https://bpp.oregonstate.edu/sites/agscid7/files/plant-parasitic-damage-levels-for-oregon-nursery-crops.pdf
  • Nyczepier A P & Halbrendt JM (1993) Nematode pests of deciduous fruit and nut trees. In Plant Parasitic Nematodes in Temperate Agriculture (eds Evans K, Trudgill DL & Webster JM). CAB International, Wallingford, England. pp. 381-425
  • PlantwisePlus Knowledge Bank (2023). Pratylenchus penetrans (nematode, northern root lesion). (accessed 26/Apr/2024). https://plantwiseplusknowledgebank.org/doi/full/10.1079/pwkb.species.43900
  • Pudasaini MP, Viaene N & Moens M (2006) Effect of marigold (Tagetes patula) on population dynamics of Pratylenchus penetrans in a field. Nematology 8, 477-84.
  • Schmitt DP & Sipes BS (2000) Plant-parasitic nematodes and their management. From “Plant Nutrient Management in Hawaii’s Soils, Approaches for Tropical and Subtropical Agriculture”. College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa.
  • Sharma GC, Thakur BS, Kashyap AS (2005) Impact of NPK on the nematode populations and yield of plum (Prunus salicina). SHS Acta Horticulturae, 696: VII International Symposium on Temperate Zone Fruits in the Tropics and Subtropics - Part Two. doi: 10.17660/ActaHortic.2005.696.77
  • Siddiqui IA, Sher SA & French AM (1973) Distribution of Plant Parasitic Nematodes in California. State of California Department of Food and Agriculture, Division of Plant Industry. 324p.
  • Söğüt MA, Devran Z, Arici ŞE, Şan B, Yildirim AN (2013) Host reactions of root lesion nematodes (Pratylenchus spp.) on the rootstocks of pome and stone. Turkish Journal of Entomology 37(2), 239-248.
  • Taning LM, Lippens L, Formesyn E, Wesemael W (2023) Impact of cover crops on population density of the root-lesion nematode Pratylenchus penetrans. Preprint DOI: https://doi.org/10.21203/rs.3.rs-3338686/v1
  • Townshend JL (1990) Growth of ‘Bartlett’ pear seedlings in response to number of root-lesions nematodes and temperature. HortSci, 25: 318-320
  • Yorston J M (1969). The interactions of Pratylenchus penetrans with host plants, Longidorus elongatus and Verticillium dahliae. PhD Thesis Oregon State University, 55 pp.

HOST PLANT N°8: Prunus cerasus (PRNCE) 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):
 
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):
 
Yes
 
Conclusion:
 
Candidate

 
Justification:
 
Pratylenchus penetrans is cosmopolitan and has more than 350 hosts including woody plants (e.g., fruit trees, roses) and herbaceous plants (e.g., potato, vegetables) (Moens & Perry, 2009, CABI, 2021), e.g., Malus is a good host for Pratylenchus penetrans (aaltjesschema, 2019). Also Pyrus spp., Cydonia oblonga, Pistacia vera and many Prunus spp. can be hosts of P. penetrans (Hoekstra & Oostenbrink, 1962; Askary et al., 2012; Merrifield, 2000). Ficus carica is not mentioned as hosts and information of Pratylenchus penetrans on Pistacia vera is scarce (PlantwisePlus Knowledge Bank, 2023; Fatemy, 2009), this could be linked to P. penetrans being a nematode from mostly temperate climates and fig and pistachio being more Mediterranean crops. P. penetrans can complete its entire life cycle within the roots of plants.
Pratylenchus spp. are migratory endoparasites that enter the host root for feeding and reproduction and move freely within the tissue. Consequently, they spend much of their life cycle in roots and are found in soil when the host plants are senescing, stressed or diseased, or when their hosts have been ploughed up after harvest (Castillo and Vovlas, 2007).
P. penetrans occurs mostly on sandy and peaty soil. The transport of infected plants or those growing in infested soils is one of the principal means by which these nematodes are disseminated (Lehman, 1994; Anonymous, 1999). Bare-rooted plants are often contaminated by soil particles which may contain nematodes. Roots can host endoparasitic nematodes that are not removed by washing treatments (Lehman, 1994). In this context, it is essential that the plant propagation material be free of this pathogen (Allen, 1949). Because it can survive in soil, it can be dispersed by land vehicles etc.; within a field by cultivation, and can be introduced to non-infested sites by poorly sanitized farm equipment. However, measures (including hygiene) can limit the importance of such alternative pathways.
In responses to the questionnaire, DE, FR and NL supported deregulation in the EU because soilborne and widespread in production areas.
Considering the numerous bibliographic references that highlight the importance of plants for planting as an important pathway, and the existence of measures that can reduce the role of the others reported pathways, host plants for planting with roots, with or without soil or growing media, are considered as a main pathway.

5 - Economic impact:

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

Justification:
 
Pratylenchus penetrans is well recognized as economically important pest of stone-fruits (Mai and Parker, 1967; Townshend, 1990; Clavero-Camacho et al., 2024).
Much of the damage caused by root-lesion nematodes in stone fruits (Prunus spp.) results from their ability to induce extensive root necrosis. Nematode invasion of young roots induces reddish brown, elongated lesions. Root lesions darken with age, necrosis often spreads to affect the entire root, growth ceases, and the root dies. Severe infection may destroy the fine roots. Heavy infections often result in small root systems and stunted trees. Symptoms are more common on young trees than on old trees (Bird & Melakeberhan, 1995).
Depending on the level of P. penetrans present in the soil, damage might occur :
- Prunus dulcis: in the NEMAPLEX (2024) database, Prunus dulcis is reported as susceptible (= high level of nematode reproduction) to Pratylenchus penetrans (Siddiqui et al., 1973).
- Prunus armeniaca & Prunus domestica: mentioned as host. In the NEMAPLEX (2024) database, Prunus armeniaca is reported as susceptible (= high level of nematode reproduction) to Pratylenchus penetrans (Siddiqui et al., 1973).
- Prunus avium & Prunus cerasus: Initial population of 80/100 g soil necessary for growth reduction (Nyczepir and Halbrendt 1993). In NE U.S., reduced yield and shortened productive life of Montmorency cherry on Mazard and Mahaleb rootstocks; parasitized trees were less winter hardy (Nyczepir and Halbrendt 1993). In pots, seedlings grown for 12 weeks in steam-fumigated orchard soil with a history of replant disease containing a mixed population of 7 P. penetrans and P. projectus/100 g weighed 46% more and were 64% taller than seedlings grown in non-treated soil (Mai and Abawi 1978), (Cited in Merrifield, 2000). Pratylenchus penetrans has been responsible for severe decline and for replating failure in many cherry orchards. Also, this nematode can lower the resistance of plants to other pathogens (Anonymous, 1999).
- Prunus cerasifera: Initial population of 320/100 g soil necessary for growth reduction (Nyczepir and Halbrendt 1993). (Cited in Merrifield, 2000)
- Prunus persica: 5/100 g soil (Barker et al. 1976). Root impairment results in loss of vigour and yields of mature trees, but P. penetrans’ role in orchard replant problems is probably more economically important (Nyczepir and Halbrendt 1993). Pratylenchus penetrans has been responsible for severe decline and for replating failure in many peach orchards. Also, this nematode can lower the resistance of plants to other pathogens (Anonymous, 1999). In pots, seedling height was significantly reduced 40% by 114/100 cm3, 60% by 228/100 cm3, and 75% by 457/100 cm3 (Cited in Merrifield, 2000).
- Prunus salicina: In a Prunus salicina (var. Santa Rosa) orchard located in India, Pratylenchus penetrans was the predominant plant-parasitic nematode, with populations of 150-380 nematodes per 200 cc soil (Sharma et al., 2005).
In the responses to the questionnaire, FR supported deregulation in the EU, commenting that the pest had a 'low nuisance level on fruit plants'.

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 
Medium to 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?
 
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:
 
Evidence of its economic impact is available in the literature and confirmed by Spanish experts.
The damage caused by Pratylenchus is usually most severe in light-textured soils that are low in nutrients (e.g. nitrogen, potassium, or calcium) and in organic matter (Anonymous, 1999). pH and soil texture were the most influential variables in Pratylenchus distribution and abundance during the study of Clavero-Camacho et al. (2024) on plant parasitic nematodes affecting Prunus species in Spain.

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:
 
Crop rotation is difficult because of the wide host range of Pratylenchus penetrans, including weeds. Pratylenchus penetrans can propagate well on many crops, sometimes without causing damage (symptomless) (aaltjesschema). Recent research indicated that with proper choice of selected cultivars of cover crops, P. penetrans can be controlled but further breeding efforts are needed. Although some cover crops can reduce the population of Pratylenchus penetrans (Taning et al., 2023). Since many weeds can also be a host, adequate weed control is important (Aaltjesschema, 2019). Crop rotation is also a limited option since woody crops remain in soil for decades and the host-range of many of this of the plant parasitic nematodes is wide (Castillo y Vovlas, 2007).

Growing Tagetes spp. (e.g. Tagetes patula) can reduce the population considerably (Evenhuis et al., 2004). The authors predicted that strawberries could be grown for about 7 successive years without economic damage due to the root lesion nematode. Pudasaini et al. (2006) showed that Tagetes can reduce P. penetrans exponentially in time under marigold. The effect of marigold was persistent as no increase in P. penetrans densities over the whole soil profile was noticed after two crop cycles of host plants.

Use of clean soil: The propagation material is kept either in containers of sterilized growing medium or in soil that has been tested and found free from various nematodes (e.g. EPPO 2022).

Soil fumigation: dependent on legislation. Preplant soil fumigation does not eradicate nematodes but dramatically reduces nematode numbers. The nematodes return to their original population density (or greater) within 2 or 3 years after planting, but the absence of nematode pressure during the initial years of establishment is critical for trees to develop strong, healthy root systems (Abawi & Mai, 2014). With the progressive phase-out of chemical nematicides such as Aldicarb, Carbofuran, and 1,3-Dichloropropene, the effectiveness and sustainability of current plant-parasitic nematode management strategies remain limited (Barbosa et al., 2022).

Healthy plants: To prevent the introduction of nematode problems, new orchards should be established with trees obtained from reputable nurseries that treat their soils for nematodes (Abawi & Mai, 2014).

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.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
Yes

Proposed Risk management measure:
 
Non-Certified material (‘Conformitas Agraria Communitatis (CAC)’):
• Mother plants have been produced in a pest free place/site of production
or
• Material obtained from mother plants does not contain roots and soil

AND

• Plants have been produced in soil/growing medium considered free from P. penetrans (e.g. tested soil, use of sterilized growing media or soil-free).

Justification (if necessary):
 
The risk of transmission of this nematode is restricted to materials with roots and soil. Generally, material obtained from mother plants (e.g. buds, cuttings...) doesn’t contain roots and soil. The critical point to avoid the spread of this pest is in the nurseries where certified and CAC seedlings are produced for marketing to growers or end users. Considering that detection by inspection is practically impossible when no symptoms are observed, that symptomology is non-specific (both above and below ground) and the complexity to perform laboratory testing, the fruit SEWG considered that PFA should not be proposed as an option. The Fruit SEWG also considered that an option requiring not growing hosts during > 5 years was not realistic considering how polyphagous the pest is.
Hot water treatments with some time-temperature schedules have been shown to be effective against the pest (Anonymous, 1999; Lim et al., 2024). Further work would be needed to validate if these schedules are applicable to the different host species under practical circumstances.

[During consultation on draft recommendations, NL commented that it will be very difficult if not impossible to find production sites that are free, unless the plants are grown indoor in pots.] The Fruit SEWG considered that on one hand the pest has a very wide host range and is widespread in some countries (e.g. in NL); on the other hand, in other countries (e.g. in ES or other countries), soils are not so infested. But plant for planting is a significant pathway. It is an endoparasite, moving with plants for planting. It is difficult to see the symptoms since this involves uprooting the plant (only possible for Fragaria). The fruit SEWG considered that the decision should be taken later by risk managers on whether the measure is maintained to limit economic impact to end users or withdrawn to limit economic burden to the producer of plants for planting.

REFERENCES:
  • Aaltjesschema (2019). Website on information and crop rotation for various crops. The website is s product of Wageningen UR, nematology PPO-AGV. Website is accessible until 31 March 2024, only information for perennial plants and fruit crops will still be available. https://www.aaltjesschema.nl/Home.aspx
  • Abawi GS & Mai WF (2014) Root lesion nematodes (revised by Halbrendt JM). In Compendium of apple and pear diseases and pests, second edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, USA: 113-114.
  • Allen MW (1949). Root-lesion nematodes: resistant rootstocks most promising method of control. California Agriculture, January: 13-14.
  • Anonymous (1998) Pratylenchus on Oregon crops: Pratylenchus damage levels for Oregon crops: a literature survey. https://bpp.oregonstate.edu/pratylenchus-oregon-crops.
  • Anonymous (1999) Lesion nematodes. University of Illinois Extension. RPD, 1103. May 1999.
  • Askary TH, Banday SA, Iqbal U, Khan AA, Mir MM & Waliullah MIS (2012) Plant parasitic nematode diversity in pome, stone and nut fruits. In Agroecology and Strategies for Climate Change (ed Lichtfouse E). Springer Sicens+Business Media B.V. DOI 10.1007/978-94-007-1905-7_10. 237-268.
  • Barbosa P, Faria JMS, Figueiredo AC, Mota M & Vicente CSL (2022) Control of the root lesion Pratylenchus penetrans: the effect of nematicidal activity of plant-derived compounds. Revista de Ciencias Agrarias, 45 (4): 649-652. https://doi.org/10.19084/rca.28749
  • Bird GW & Melakeberhan H (1995) Root-Lesion Nematodes (Pratylenchus spp.). In Compendium of Stone Fruit Diseases (eds Ogawa JM, Zehr EI, Bird GW, Ritchie DF, Uriu K & Uyemoto JK)
  • Bucki P, Qing X, Castillo P, Gamliel A, Dobrinin S, Alon T, Miyara SB (2020) The genus Pratylenchus (Nematoda: Pratylenchidae) in Israel: from taxonomy to control practices. Plants 9, 1475; doi:10.3390/plants9111475.
  • Castillo P, Vovlas (2007) Biology and ecology of Pratylenchus. In “Pratylechus (Nematoda: Pratylenchidae): diagnosis, biology, pathogenicity and management”. Nematology Monographs & Perspective 6, 305-324.
  • Clavero-Camacho I, Archidona-Yuste A, Cantalapiedra-Navarrete C, Castillo P & Palomares-Rius JE (2024) Prevalence and ecological factors affecting the distribution of plant-parasitic nematodes in Prunus groves in Spain. Journal of Integrative Agriculture, 23(2): 585-589.
  • EPPO (2022) PM 4/17 (3) Certification scheme for olive trees and rootstocks. EPPO Bulletin 52:590–60. DOI: 10.1111/epp.1288
  • Evenhuis A, Korthals G & Molendijk L. (2004). Tagetes patula as an effective catch crop for long-term control of Pratylenchus penetrans. Nematology, 6(6), 877-881. https://doi.org/10.1163/1568541044038632
  • Fatemy S (2009). Integrated management of pistachio nematodes. In Integrated Management of Fruit Crops and Forest Nematodes (eds Ciancio A & Mukerji KG). Springer Science+Business Media BV, 243-252.
  • Goodey JB, Franklin MT &Hooper DJ (1965) The nematode parasites of plants catalogued under their host. Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, England. Third Edition.
  • Hoestra H & Oostenbrink M (1962) Nematodes in relation to plant growth IV. Pratylenchus penetrans (Cobb) on orchard trees. Neth. J. agric. Sei., Vol. 10 (1962) No. 4 (November): 286-296
  • Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MGK, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WML & Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14 (9): 946-961.
  • Lehman PS (1994) Dissemination of phytoparasitic nematodes. Nematology Circular, No 28. Fla. Dept. Agric.& Consumer Services. Division of Plant Industry.
  • Lim G-E, Heo M-S & Park M-G (2024) Hot Water Treatment as a Quarantine Measure for Controlling Pratylenchus penetrans Cobb in Syngonium podophyllum Schott and Perilla frutescens Britton. Agriculture 14, 582. https://doi.org/10.3390/agriculture14040582.
  • Moens M & Perry RN (2009) Migratory plant endoparasitic nematodes: a group rich in contrasts and divergence. Annual Review of Phytopathology 47, 313–32.
  • NEMAPLEX (2024) Host Status of a Plant Genus and species to Nematodes. http://nemaplex.ucdavis.edu/ (accessed: 07/11/2024)
  • Nyczepir AP (1991) Nematode management strategies in stone fruits in the United States. Journal of Nematology 23(3), 334-341.
  • Mai WF & Abawi GS (1978) Determining the cause and extent of apple, cherry, and pear replant diseases under controlled conditions. Phytopathology 68, 1540-1544.
  • Merrifield K (2000) Plant-parasitic damage levels for Oregon nursery crops: A literature survey. Biology, host ranges, and damage levels of root-parasitic nematodes on Oregon nursery crops (Draft: 2000). https://bpp.oregonstate.edu/sites/agscid7/files/plant-parasitic-damage-levels-for-oregon-nursery-crops.pdf
  • Nyczepier A P & Halbrendt JM (1993) Nematode pests of deciduous fruit and nut trees. In Plant Parasitic Nematodes in Temperate Agriculture (eds Evans K, Trudgill DL & Webster JM). CAB International, Wallingford, England. pp. 381-425
  • PlantwisePlus Knowledge Bank (2023). Pratylenchus penetrans (nematode, northern root lesion). (accessed 26/Apr/2024). https://plantwiseplusknowledgebank.org/doi/full/10.1079/pwkb.species.43900
  • Pudasaini MP, Viaene N & Moens M (2006) Effect of marigold (Tagetes patula) on population dynamics of Pratylenchus penetrans in a field. Nematology 8, 477-84.
  • Schmitt DP & Sipes BS (2000) Plant-parasitic nematodes and their management. From “Plant Nutrient Management in Hawaii’s Soils, Approaches for Tropical and Subtropical Agriculture”. College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa.
  • Sharma GC, Thakur BS, Kashyap AS (2005) Impact of NPK on the nematode populations and yield of plum (Prunus salicina). SHS Acta Horticulturae, 696: VII International Symposium on Temperate Zone Fruits in the Tropics and Subtropics - Part Two. doi: 10.17660/ActaHortic.2005.696.77
  • Siddiqui IA, Sher SA & French AM (1973) Distribution of Plant Parasitic Nematodes in California. State of California Department of Food and Agriculture, Division of Plant Industry. 324p.
  • Söğüt MA, Devran Z, Arici ŞE, Şan B, Yildirim AN (2013) Host reactions of root lesion nematodes (Pratylenchus spp.) on the rootstocks of pome and stone. Turkish Journal of Entomology 37(2), 239-248.
  • Taning LM, Lippens L, Formesyn E, Wesemael W (2023) Impact of cover crops on population density of the root-lesion nematode Pratylenchus penetrans. Preprint DOI: https://doi.org/10.21203/rs.3.rs-3338686/v1
  • Townshend JL (1990) Growth of ‘Bartlett’ pear seedlings in response to number of root-lesions nematodes and temperature. HortSci, 25: 318-320
  • Yorston J M (1969). The interactions of Pratylenchus penetrans with host plants, Longidorus elongatus and Verticillium dahliae. PhD Thesis Oregon State University, 55 pp.

HOST PLANT N°9: Prunus domestica (PRNDO) 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):
 
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):
 
Yes
 
Conclusion:
 
Candidate

 
Justification:
 
Pratylenchus penetrans is cosmopolitan and has more than 350 hosts including woody plants (e.g., fruit trees, roses) and herbaceous plants (e.g., potato, vegetables) (Moens & Perry, 2009, CABI, 2021), e.g., Malus is a good host for Pratylenchus penetrans (aaltjesschema, 2019). Also Pyrus spp., Cydonia oblonga, Pistacia vera and many Prunus spp. can be hosts of P. penetrans (Hoekstra & Oostenbrink, 1962; Askary et al., 2012; Merrifield, 2000). Ficus carica is not mentioned as hosts and information of Pratylenchus penetrans on Pistacia vera is scarce (PlantwisePlus Knowledge Bank, 2023; Fatemy, 2009), this could be linked to P. penetrans being a nematode from mostly temperate climates and fig and pistachio being more Mediterranean crops. P. penetrans can complete its entire life cycle within the roots of plants.
Pratylenchus spp. are migratory endoparasites that enter the host root for feeding and reproduction and move freely within the tissue. Consequently, they spend much of their life cycle in roots and are found in soil when the host plants are senescing, stressed or diseased, or when their hosts have been ploughed up after harvest (Castillo and Vovlas, 2007).
P. penetrans occurs mostly on sandy and peaty soil. The transport of infected plants or those growing in infested soils is one of the principal means by which these nematodes are disseminated (Lehman, 1994; Anonymous, 1999). Bare-rooted plants are often contaminated by soil particles which may contain nematodes. Roots can host endoparasitic nematodes that are not removed by washing treatments (Lehman, 1994). In this context, it is essential that the plant propagation material be free of this pathogen (Allen, 1949). Because it can survive in soil, it can be dispersed by land vehicles etc.; within a field by cultivation, and can be introduced to non-infested sites by poorly sanitized farm equipment. However, measures (including hygiene) can limit the importance of such alternative pathways.
In responses to the questionnaire, DE, FR and NL supported deregulation in the EU because soilborne and widespread in production areas.
Considering the numerous bibliographic references that highlight the importance of plants for planting as an important pathway, and the existence of measures that can reduce the role of the others reported pathways, host plants for planting with roots, with or without soil or growing media, are a considered as a main pathway.

5 - Economic impact:

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

Justification:
 
Pratylenchus penetrans is well recognized as economically important pest of stone-fruits (Mai and Parker, 1967; Townshend, 1990; Clavero-Camacho et al., 2024).
Much of the damage caused by root-lesion nematodes in stone fruits (Prunus spp.) results from their ability to induce extensive root necrosis. Nematode invasion of young roots induces reddish brown, elongated lesions. Root lesions darken with age, necrosis often spreads to affect the entire root, growth ceases, and the root dies. Severe infection may destroy the fine roots. Heavy infections often result in small root systems and stunted trees. Symptoms are more common on young trees than on old trees (Bird & Melakeberhan, 1995).
Depending on the level of P. penetrans present in the soil, damage might occur :
- Prunus dulcis: in the NEMAPLEX (2024) database, Prunus dulcis is reported as susceptible (= high level of nematode reproduction) to Pratylenchus penetrans (Siddiqui et al., 1973).
- Prunus armeniaca & Prunus domestica: mentioned as host. In the NEMAPLEX (2024) database, Prunus armeniaca is reported as susceptible (= high level of nematode reproduction) to Pratylenchus penetrans (Siddiqui et al., 1973).
- Prunus avium & Prunus cerasus: Initial population of 80/100 g soil necessary for growth reduction (Nyczepir and Halbrendt 1993). In NE U.S., reduced yield and shortened productive life of Montmorency cherry on Mazard and Mahaleb rootstocks; parasitized trees were less winter hardy (Nyczepir and Halbrendt 1993). In pots, seedlings grown for 12 weeks in steam-fumigated orchard soil with a history of replant disease containing a mixed population of 7 P. penetrans and P. projectus/100 g weighed 46% more and were 64% taller than seedlings grown in non-treated soil (Mai and Abawi 1978), (Cited in Merrifield, 2000). Pratylenchus penetrans has been responsible for severe decline and for replating failure in many cherry orchards. Also, this nematode can lower the resistance of plants to other pathogens (Anonymous, 1999).
- Prunus cerasifera: Initial population of 320/100 g soil necessary for growth reduction (Nyczepir and Halbrendt 1993). (Cited in Merrifield, 2000)
- Prunus persica: 5/100 g soil (Barker et al. 1976). Root impairment results in loss of vigour and yields of mature trees, but P. penetrans’ role in orchard replant problems is probably more economically important (Nyczepir and Halbrendt 1993). Pratylenchus penetrans has been responsible for severe decline and for replating failure in many peach orchards. Also, this nematode can lower the resistance of plants to other pathogens (Anonymous, 1999). In pots, seedling height was significantly reduced 40% by 114/100 cm3, 60% by 228/100 cm3, and 75% by 457/100 cm3 (Cited in Merrifield, 2000).
- Prunus salicina: In a Prunus salicina (var. Santa Rosa) orchard located in India, Pratylenchus penetrans was the predominant plant-parasitic nematode, with populations of 150-380 nematodes per 200 cc soil (Sharma et al., 2005).
In the responses to the questionnaire, FR supported deregulation in the EU, commenting that the pest had a 'low nuisance level on fruit plants'.

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 
Medium to 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?
 
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:
 
Evidence of its economic impact is available in the literature and confirmed by Spanish experts.
The damage caused by Pratylenchus is usually most severe in light-textured soils that are low in nutrients (e.g. nitrogen, potassium, or calcium) and in organic matter (Anonymous, 1999). pH and soil texture were the most influential variables in Pratylenchus distribution and abundance during the study of Clavero-Camacho et al. (2024) on plant parasitic nematodes affecting Prunus species in Spain.

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:
 
Crop rotation is difficult because of the wide host range of Pratylenchus penetrans, including weeds. Pratylenchus penetrans can propagate well on many crops, sometimes without causing damage (symptomless) (aaltjesschema). Recent research indicated that with proper choice of selected cultivars of cover crops, P. penetrans can be controlled but further breeding efforts are needed. Although some cover crops can reduce the population of Pratylenchus penetrans (Taning et al., 2023). Since many weeds can also be a host, adequate weed control is important (Aaltjesschema, 2019). Crop rotation is also a limited option since woody crops remain in soil for decades and the host-range of many of this of the plant parasitic nematodes is wide (Castillo y Vovlas, 2007).

Growing Tagetes spp. (e.g. Tagetes patula) can reduce the population considerably (Evenhuis et al., 2004). The authors predicted that strawberries could be grown for about 7 successive years without economic damage due to the root lesion nematode. Pudasaini et al. (2006) showed that Tagetes can reduce P. penetrans exponentially in time under marigold. The effect of marigold was persistent as no increase in P. penetrans densities over the whole soil profile was noticed after two crop cycles of host plants.

Use of clean soil: The propagation material is kept either in containers of sterilized growing medium or in soil that has been tested and found free from various nematodes (e.g. EPPO 2022).

Soil fumigation: dependent on legislation. Preplant soil fumigation does not eradicate nematodes but dramatically reduces nematode numbers. The nematodes return to their original population density (or greater) within 2 or 3 years after planting, but the absence of nematode pressure during the initial years of establishment is critical for trees to develop strong, healthy root systems (Abawi & Mai, 2014). With the progressive phase-out of chemical nematicides such as Aldicarb, Carbofuran, and 1,3-Dichloropropene, the effectiveness and sustainability of current plant-parasitic nematode management strategies remain limited (Barbosa et al., 2022).

Healthy plants: To prevent the introduction of nematode problems, new orchards should be established with trees obtained from reputable nurseries that treat their soils for nematodes (Abawi & Mai, 2014).

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.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
Yes

Proposed Risk management measure:
 
Non-Certified material (‘Conformitas Agraria Communitatis (CAC)’):
• Mother plants have been produced in a pest free place/site of production
or
• Material obtained from mother plants does not contain roots and soil

AND

• Plants have been produced in soil/growing medium considered free from P. penetrans (e.g. tested soil, use of sterilized growing media or soil-free).

Justification (if necessary):
 
The risk of transmission of this nematode is restricted to materials with roots and soil. Generally, material obtained from mother plants (e.g. buds, cuttings...) doesn’t contain roots and soil. The critical point to avoid the spread of this pest is in the nurseries where certified and CAC seedlings are produced for marketing to growers or end users. Considering that symptoms may not be visible, that symptomology is non-specific (both above and below ground) and the complexity to perform laboratory testing, the fruit SEWG considered that PFA should not be proposed as an option. The Fruit SEWG also considered that an option requiring not growing hosts during > 5 years was not realistic considering how polyphagous the pest is.
Hot water treatments with some time-temperature schedules have been shown to be effective against the pest (Anonymous, 1999; Lim et al., 2024). Further work would be needed to validate if these schedules are applicable to the different host species under practical circumstances.

[During consultation on draft recommendations, NL commented that it will be very difficult if not impossible to find production sites that are free, unless the plants are grown indoor in pots.] The Fruit SEWG considered that on one hand the pest has a very wide host range and is widespread in some countries (e.g. in NL); on the other hand, in other countries (e.g. in ES or other countries), soils are not so infested. But plant for planting is a significant pathway. It is an endoparasite, moving with plants for planting. It is difficult to see the symptoms since this involves uprooting the plant (only possible for Fragaria). The fruit SEWG considered that the decision should be taken later by risk managers on whether the measure is maintained to limit economic impact to end users or withdrawn to limit economic burden to the producer of plants for planting.

REFERENCES:
  • Aaltjesschema (2019). Website on information and crop rotation for various crops. The website is s product of Wageningen UR, nematology PPO-AGV. Website is accessible until 31 March 2024, only information for perennial plants and fruit crops will still be available. https://www.aaltjesschema.nl/Home.aspx
  • Abawi GS & Mai WF (2014) Root lesion nematodes (revised by Halbrendt JM). In Compendium of apple and pear diseases and pests, second edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, USA: 113-114.
  • Allen MW (1949). Root-lesion nematodes: resistant rootstocks most promising method of control. California Agriculture, January: 13-14.
  • Anonymous (1998) Pratylenchus on Oregon crops: Pratylenchus damage levels for Oregon crops: a literature survey. https://bpp.oregonstate.edu/pratylenchus-oregon-crops.
  • Anonymous (1999) Lesion nematodes. University of Illinois Extension. RPD, 1103. May 1999.
  • Askary TH, Banday SA, Iqbal U, Khan AA, Mir MM & Waliullah MIS (2012) Plant parasitic nematode diversity in pome, stone and nut fruits. In Agroecology and Strategies for Climate Change (ed Lichtfouse E). Springer Sicens+Business Media B.V. DOI 10.1007/978-94-007-1905-7_10. 237-268.
  • Barbosa P, Faria JMS, Figueiredo AC, Mota M & Vicente CSL (2022) Control of the root lesion Pratylenchus penetrans: the effect of nematicidal activity of plant-derived compounds. Revista de Ciencias Agrarias, 45 (4): 649-652. https://doi.org/10.19084/rca.28749
  • Bird GW & Melakeberhan H (1995) Root-Lesion Nematodes (Pratylenchus spp.). In Compendium of Stone Fruit Diseases (eds Ogawa JM, Zehr EI, Bird GW, Ritchie DF, Uriu K & Uyemoto JK)
  • Bucki P, Qing X, Castillo P, Gamliel A, Dobrinin S, Alon T, Miyara SB (2020) The genus Pratylenchus (Nematoda: Pratylenchidae) in Israel: from taxonomy to control practices. Plants 9, 1475; doi:10.3390/plants9111475.
  • Castillo P, Vovlas (2007) Biology and ecology of Pratylenchus. In “Pratylechus (Nematoda: Pratylenchidae): diagnosis, biology, pathogenicity and management”. Nematology Monographs & Perspective 6, 305-324.
  • Clavero-Camacho I, Archidona-Yuste A, Cantalapiedra-Navarrete C, Castillo P & Palomares-Rius JE (2024) Prevalence and ecological factors affecting the distribution of plant-parasitic nematodes in Prunus groves in Spain. Journal of Integrative Agriculture, 23(2): 585-589.
  • EPPO (2022) PM 4/17 (3) Certification scheme for olive trees and rootstocks. EPPO Bulletin 52, 590–60. DOI: 10.1111/epp.1288
  • Evenhuis A, Korthals G & Molendijk L. (2004). Tagetes patula as an effective catch crop for long-term control of Pratylenchus penetrans. Nematology, 6(6), 877-881. https://doi.org/10.1163/1568541044038632
  • Fatemy S (2009). Integrated management of pistachio nematodes. In Integrated Management of Fruit Crops and Forest Nematodes (eds Ciancio A & Mukerji KG). Springer Science+Business Media BV, 243-252.
  • Goodey JB, Franklin MT &Hooper DJ (1965) The nematode parasites of plants catalogued under their host. Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, England. Third Edition.
  • Hoestra H & Oostenbrink M (1962) Nematodes in relation to plant growth IV. Pratylenchus penetrans (Cobb) on orchard trees. Neth. J. agric. Sei., Vol. 10 (1962) No. 4 (November): 286-296
  • Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MGK, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WML & Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14 (9): 946-961.
  • Lehman PS (1994) Dissemination of phytoparasitic nematodes. Nematology Circular, No 28. Fla. Dept. Agric.& Consumer Services. Division of Plant Industry.
  • Lim G-E, Heo M-S & Park M-G (2024) Hot Water Treatment as a Quarantine Measure for Controlling Pratylenchus penetrans Cobb in Syngonium podophyllum Schott and Perilla frutescens Britton. Agriculture 14, 582. https://doi.org/10.3390/agriculture14040582.
  • Moens M & Perry RN (2009) Migratory plant endoparasitic nematodes: a group rich in contrasts and divergence. Annual Review of Phytopathology 47, 313–32.
  • NEMAPLEX (2024) Host Status of a Plant Genus and species to Nematodes. http://nemaplex.ucdavis.edu/ (accessed: 07/11/2024)
  • Nyczepir AP (1991) Nematode management strategies in stone fruits in the United States. Journal of Nematology 23(3), 334-341.
  • Mai WF & Abawi GS (1978) Determining the cause and extent of apple, cherry, and pear replant diseases under controlled conditions. Phytopathology 68, 1540-1544.
  • Merrifield K (2000) Plant-parasitic damage levels for Oregon nursery crops: A literature survey. Biology, host ranges, and damage levels of root-parasitic nematodes on Oregon nursery crops (Draft: 2000). https://bpp.oregonstate.edu/sites/agscid7/files/plant-parasitic-damage-levels-for-oregon-nursery-crops.pdf
  • Nyczepier A P & Halbrendt JM (1993) Nematode pests of deciduous fruit and nut trees. In Plant Parasitic Nematodes in Temperate Agriculture (eds Evans K, Trudgill DL & Webster JM). CAB International, Wallingford, England. pp. 381-425
  • PlantwisePlus Knowledge Bank (2023). Pratylenchus penetrans (nematode, northern root lesion). (accessed 26/Apr/2024). https://plantwiseplusknowledgebank.org/doi/full/10.1079/pwkb.species.43900
  • Pudasaini MP, Viaene N & Moens M (2006) Effect of marigold (Tagetes patula) on population dynamics of Pratylenchus penetrans in a field. Nematology 8, 477-84.
  • Schmitt DP & Sipes BS (2000) Plant-parasitic nematodes and their management. From “Plant Nutrient Management in Hawaii’s Soils, Approaches for Tropical and Subtropical Agriculture”. College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa.
  • Sharma GC, Thakur BS, Kashyap AS (2005) Impact of NPK on the nematode populations and yield of plum (Prunus salicina). SHS Acta Horticulturae, 696: VII International Symposium on Temperate Zone Fruits in the Tropics and Subtropics - Part Two. doi: 10.17660/ActaHortic.2005.696.77
  • Siddiqui IA, Sher SA & French AM (1973) Distribution of Plant Parasitic Nematodes in California. State of California Department of Food and Agriculture, Division of Plant Industry. 324p.
  • Söğüt MA, Devran Z, Arici ŞE, Şan B, Yildirim AN (2013) Host reactions of root lesion nematodes (Pratylenchus spp.) on the rootstocks of pome and stone. Turkish Journal of Entomology 37(2), 239-248.
  • Taning LM, Lippens L, Formesyn E, Wesemael W (2023) Impact of cover crops on population density of the root-lesion nematode Pratylenchus penetrans. Preprint DOI: https://doi.org/10.21203/rs.3.rs-3338686/v1
  • Townshend JL (1990) Growth of ‘Bartlett’ pear seedlings in response to number of root-lesions nematodes and temperature. HortSci, 25: 318-320
  • Yorston J M (1969). The interactions of Pratylenchus penetrans with host plants, Longidorus elongatus and Verticillium dahliae. PhD Thesis Oregon State University, 55 pp.

HOST PLANT N°10: Prunus dulcis (PRNDU) 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):
 
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):
 
Yes
 
Conclusion:
 
Candidate

 
Justification:
 
Pratylenchus penetrans is cosmopolitan and has more than 350 hosts including woody plants (e.g., fruit trees, roses) and herbaceous plants (e.g., potato, vegetables) (Moens & Perry, 2009, CABI, 2021), e.g., Malus is a good host for Pratylenchus penetrans (aaltjesschema, 2019). Also Pyrus spp., Cydonia oblonga, Pistacia vera and many Prunus spp. can be hosts of P. penetrans (Hoekstra & Oostenbrink, 1962; Askary et al., 2012; Merrifield, 2000). Ficus carica is not mentioned as hosts and information of Pratylenchus penetrans on Pistacia vera is scarce (PlantwisePlus Knowledge Bank, 2023; Fatemy, 2009), this could be linked to P. penetrans being a nematode from mostly temperate climates and fig and pistachio being more Mediterranean crops. P. penetrans can complete its entire life cycle within the roots of plants.
Pratylenchus spp. are migratory endoparasites that enter the host root for feeding and reproduction and move freely within the tissue. Consequently, they spend much of their life cycle in roots and are found in soil when the host plants are senescing, stressed or diseased, or when their hosts have been ploughed up after harvest (Castillo and Vovlas, 2007).
P. penetrans occurs mostly on sandy and peaty soil. The transport of infected plants or those growing in infested soils is one of the principal means by which these nematodes are disseminated (Lehman, 1994; Anonymous, 1999). Bare-rooted plants are often contaminated by soil particles which may contain nematodes. Roots can host endoparasitic nematodes that are not removed by washing treatments (Lehman, 1994). In this context, it is essential that the plant propagation material be free of this pathogen (Allen, 1949). Because it can survive in soil, it can be dispersed by land vehicles etc.; within a field by cultivation, and can be introduced to non-infested sites by poorly sanitized farm equipment. However, measures (including hygiene) can limit the importance of such alternative pathways.
In responses to the questionnaire, DE, FR and NL supported deregulation in the EU because soilborne and widespread in production areas.
Considering the numerous bibliographic references that highlight the importance of plants for planting as an important pathway, and the existence of measures that can reduce the role of the others reported pathways, host plants for planting with roots, with or without soil or growing media, are a considered as a main pathway.

5 - Economic impact:

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

Justification:
 
Pratylenchus penetrans is well recognized as economically important pest of stone-fruits (Mai and Parker, 1967; Townshend, 1990; Clavero-Camacho et al., 2024).
Much of the damage caused by root-lesion nematodes in stone fruits (Prunus spp.) results from their ability to induce extensive root necrosis. Nematode invasion of young roots induces reddish brown, elongated lesions. Root lesions darken with age, necrosis often spreads to affect the entire root, growth ceases, and the root dies. Severe infection may destroy the fine roots. Heavy infections often result in small root systems and stunted trees. Symptoms are more common on young trees than on old trees (Bird & Melakeberhan, 1995).
Depending on the level of P. penetrans present in the soil, damage might occur :
- Prunus dulcis: in the NEMAPLEX (2024) database, Prunus dulcis is reported as susceptible (= high level of nematode reproduction) to Pratylenchus penetrans (Siddiqui et al., 1973).
- Prunus armeniaca & Prunus domestica: mentioned as host. In the NEMAPLEX (2024) database, Prunus armeniaca is reported as susceptible (= high level of nematode reproduction) to Pratylenchus penetrans (Siddiqui et al., 1973).
- Prunus avium & Prunus cerasus: Initial population of 80/100 g soil necessary for growth reduction (Nyczepir and Halbrendt 1993). In NE U.S., reduced yield and shortened productive life of Montmorency cherry on Mazard and Mahaleb rootstocks; parasitized trees were less winter hardy (Nyczepir and Halbrendt 1993). In pots, seedlings grown for 12 weeks in steam-fumigated orchard soil with a history of replant disease containing a mixed population of 7 P. penetrans and P. projectus/100 g weighed 46% more and were 64% taller than seedlings grown in non-treated soil (Mai and Abawi 1978), (Cited in Merrifield, 2000). Pratylenchus penetrans has been responsible for severe decline and for replanting failure in many cherry orchards. Also, this nematode can lower the resistance of plants to other pathogens (Anonymous, 1999).
- Prunus cerasifera: Initial population of 320/100 g soil necessary for growth reduction (Nyczepir and Halbrendt 1993). (Cited in Merrifield, 2000)
- Prunus persica: 5/100 g soil (Barker et al. 1976). Root impairment results in loss of vigour and yields of mature trees, but P. penetrans’ role in orchard replant problems is probably more economically important (Nyczepir and Halbrendt 1993). Pratylenchus penetrans has been responsible for severe decline and for replating failure in many peach orchards. Also, this nematode can lower the resistance of plants to other pathogens (Anonymous, 1999). In pots, seedling height was significantly reduced 40% by 114/100 cm3, 60% by 228/100 cm3, and 75% by 457/100 cm3 (Cited in Merrifield, 2000).
- Prunus salicina: In a Prunus salicina (var. Santa Rosa) orchard located in India, Pratylenchus penetrans was the predominant plant-parasitic nematode, with populations of 150-380 nematodes per 200 cc soil (Sharma et al., 2005).
In the responses to the questionnaire, FR supported deregulation in the EU, commenting that the pest had a 'low nuisance level on fruit plants'.

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 
Medium to 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?
 
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:
 
Evidence of its economic impact is available in the literature and confirmed by Spanish experts.
The damage caused by Pratylenchus is usually most severe in light-textured soils that are low in nutrients (e.g. nitrogen, potassium, or calcium) and in organic matter (Anonymous, 1999). pH and soil texture were the most influential variables in Pratylenchus distribution and abundance during the study of Clavero-Camacho et al. (2024) on plant parasitic nematodes affecting Prunus species in Spain.

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:
 
Crop rotation is difficult because of the wide host range of Pratylenchus penetrans, including weeds. Pratylenchus penetrans can propagate well on many crops, sometimes without causing damage (symptomless) (aaltjesschema). Recent research indicated that with proper choice of selected cultivars of cover crops, P. penetrans can be controlled but further breeding efforts are needed. Although some cover crops can reduce the population of Pratylenchus penetrans (Taning et al., 2023). Since many weeds can also be a host, adequate weed control is important (Aaltjesschema, 2019). Crop rotation is also a limited option since woody crops remain in soil for decades and the host-range of many of this of the plant parasitic nematodes is wide (Castillo y Vovlas, 2007).

Growing Tagetes spp. (e.g. Tagetes patula) can reduce the population considerably (Evenhuis et al., 2004). The authors predicted that strawberries could be grown for about 7 successive years without economic damage due to the root lesion nematode. Pudasaini et al. (2006) showed that Tagetes can reduce P. penetrans exponentially in time under marigold. The effect of marigold was persistent as no increase in P. penetrans densities over the whole soil profile was noticed after two crop cycles of host plants.

Use of clean soil: The propagation material is kept either in containers of sterilized growing medium or in soil that has been tested and found free from various nematodes (e.g. EPPO 2022).

Soil fumigation: dependent on legislation. Preplant soil fumigation does not eradicate nematodes but dramatically reduces nematode numbers. The nematodes return to their original population density (or greater) within 2 or 3 years after planting, but the absence of nematode pressure during the initial years of establishment is critical for trees to develop strong, healthy root systems (Abawi & Mai, 2014). With the progressive phase-out of chemical nematicides such as Aldicarb, Carbofuran, and 1,3-Dichloropropene, the effectiveness and sustainability of current plant-parasitic nematode management strategies remain limited (Barbosa et al., 2022).

Healthy plants: To prevent the introduction of nematode problems, new orchards should be established with trees obtained from reputable nurseries that treat their soils for nematodes (Abawi & Mai, 2014).

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.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
Yes

Proposed Risk management measure:
 
Non-Certified material (‘Conformitas Agraria Communitatis (CAC)’):
• Mother plants have been produced in a pest free place/site of production
or
• Material obtained from mother plants does not contain roots and soil

AND

• Plants have been produced in soil/growing medium considered free from P. penetrans (e.g. tested soil, use of sterilized growing media or soil-free).

Justification (if necessary):
 
The risk of transmission of this nematode is restricted to materials with roots and soil. Generally, material obtained from mother plants (e.g. buds, cuttings...) doesn’t contain roots and soil. The critical point to avoid the spread of this pest is in the nurseries where certified and CAC seedlings are produced for marketing to growers or end users. Considering that symptoms may not be visible, that symptomology is non-specific (both above and below ground) and the complexity to perform laboratory testing, the fruit SEWG considered that PFA should not be proposed as an option. The Fruit SEWG also considered that an option requiring not growing hosts during > 5 years was not realistic considering how polyphagous the pest is.
Hot water treatments with some time-temperature schedules have been shown to be effective against the pest (Anonymous, 1999; Lim et al., 2024). Further work would be needed to validate if these schedules are applicable to the different host species under practical circumstances.

[During consultation on draft recommendations, NL commented that it will be very difficult if not impossible to find production sites that are free, unless the plants are grown indoor in pots.] The Fruit SEWG considered that on one hand the pest has a very wide host range and is widespread in some countries (e.g. in NL); on the other hand, in other countries (e.g. in ES or other countries), soils are not so infested. But plant for planting is a significant pathway. It is an endoparasite, moving with plants for planting. It is difficult to see the symptoms since this involves uprooting the plant (only possible for Fragaria). The fruit SEWG considered that the decision should be taken later by risk managers on whether the measure is maintained to limit economic impact to end users or withdrawn to limit economic burden to the producer of plants for planting.

REFERENCES:
  • Aaltjesschema (2019). Website on information and crop rotation for various crops. The website is s product of Wageningen UR, nematology PPO-AGV. Website is accessible until 31 March 2024, only information for perennial plants and fruit crops will still be available. https://www.aaltjesschema.nl/Home.aspx
  • Abawi GS & Mai WF (2014) Root lesion nematodes (revised by Halbrendt JM). In Compendium of apple and pear diseases and pests, second edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, USA: 113-114.
  • Allen MW (1949). Root-lesion nematodes: resistant rootstocks most promising method of control. California Agriculture, January: 13-14.
  • Anonymous (1998) Pratylenchus on Oregon crops: Pratylenchus damage levels for Oregon crops: a literature survey. https://bpp.oregonstate.edu/pratylenchus-oregon-crops.
  • Anonymous (1999) Lesion nematodes. University of Illinois Extension. RPD, 1103. May 1999.
  • Askary TH, Banday SA, Iqbal U, Khan AA, Mir MM & Waliullah MIS (2012) Plant parasitic nematode diversity in pome, stone and nut fruits. In Agroecology and Strategies for Climate Change (ed Lichtfouse E). Springer Sicens+Business Media B.V. DOI 10.1007/978-94-007-1905-7_10. 237-268.
  • Barbosa P, Faria JMS, Figueiredo AC, Mota M & Vicente CSL (2022) Control of the root lesion Pratylenchus penetrans: the effect of nematicidal activity of plant-derived compounds. Revista de Ciencias Agrarias, 45 (4): 649-652. https://doi.org/10.19084/rca.28749
  • Bird GW & Melakeberhan H (1995) Root-Lesion Nematodes (Pratylenchus spp.). In Compendium of Stone Fruit Diseases (eds Ogawa JM, Zehr EI, Bird GW, Ritchie DF, Uriu K & Uyemoto JK)
  • Bucki P, Qing X, Castillo P, Gamliel A, Dobrinin S, Alon T, Miyara SB (2020) The genus Pratylenchus (Nematoda: Pratylenchidae) in Israel: from taxonomy to control practices. Plants 9, 1475; doi:10.3390/plants9111475.
  • Castillo P, Vovlas (2007) Biology and ecology of Pratylenchus. In “Pratylechus (Nematoda: Pratylenchidae): diagnosis, biology, pathogenicity and management”. Nematology Monographs & Perspective 6, 305-324.
  • Clavero-Camacho I, Archidona-Yuste A, Cantalapiedra-Navarrete C, Castillo P & Palomares-Rius JE (2024) Prevalence and ecological factors affecting the distribution of plant-parasitic nematodes in Prunus groves in Spain. Journal of Integrative Agriculture, 23(2): 585-589.
  • EPPO (2022) PM 4/17 (3) Certification scheme for olive trees and rootstocks. EPPO Bulletin 52, 590–60. DOI: 10.1111/epp.1288
  • Evenhuis A, Korthals G & Molendijk L. (2004). Tagetes patula as an effective catch crop for long-term control of Pratylenchus penetrans. Nematology, 6(6), 877-881. https://doi.org/10.1163/1568541044038632
  • Fatemy S (2009). Integrated management of pistachio nematodes. In Integrated Management of Fruit Crops and Forest Nematodes (eds Ciancio A & Mukerji KG). Springer Science+Business Media BV, 243-252.
  • Goodey JB, Franklin MT &Hooper DJ (1965) The nematode parasites of plants catalogued under their host. Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, England. Third Edition.
  • Hoestra H & Oostenbrink M (1962) Nematodes in relation to plant growth IV. Pratylenchus penetrans (Cobb) on orchard trees. Neth. J. agric. Sei., Vol. 10 (1962) No. 4 (November): 286-296
  • Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MGK, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WML & Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14 (9): 946-961.
  • Lehman PS (1994) Dissemination of phytoparasitic nematodes. Nematology Circular, No 28. Fla. Dept. Agric.& Consumer Services. Division of Plant Industry.
  • Lim G-E, Heo M-S & Park M-G (2024) Hot Water Treatment as a Quarantine Measure for Controlling Pratylenchus penetrans Cobb in Syngonium podophyllum Schott and Perilla frutescens Britton. Agriculture 14, 582. https://doi.org/10.3390/agriculture14040582.
  • Moens M & Perry RN (2009) Migratory plant endoparasitic nematodes: a group rich in contrasts and divergence. Annual Review of Phytopathology 47, 313–32.
  • NEMAPLEX (2024) Host Status of a Plant Genus and species to Nematodes. http://nemaplex.ucdavis.edu/ (accessed: 07/11/2024)
  • Nyczepir AP (1991) Nematode management strategies in stone fruits in the United States. Journal of Nematology 23(3), 334-341.
  • Mai WF & Abawi GS (1978) Determining the cause and extent of apple, cherry, and pear replant diseases under controlled conditions. Phytopathology 68, 1540-1544.
  • Merrifield K (2000) Plant-parasitic damage levels for Oregon nursery crops: A literature survey. Biology, host ranges, and damage levels of root-parasitic nematodes on Oregon nursery crops (Draft: 2000). https://bpp.oregonstate.edu/sites/agscid7/files/plant-parasitic-damage-levels-for-oregon-nursery-crops.pdf
  • Nyczepier A P & Halbrendt JM (1993) Nematode pests of deciduous fruit and nut trees. In Plant Parasitic Nematodes in Temperate Agriculture (eds Evans K, Trudgill DL & Webster JM). CAB International, Wallingford, England. pp. 381-425
  • PlantwisePlus Knowledge Bank (2023). Pratylenchus penetrans (nematode, northern root lesion). (accessed 26/Apr/2024). https://plantwiseplusknowledgebank.org/doi/full/10.1079/pwkb.species.43900
  • Pudasaini MP, Viaene N & Moens M (2006) Effect of marigold (Tagetes patula) on population dynamics of Pratylenchus penetrans in a field. Nematology 8, 477-84.
  • Schmitt DP & Sipes BS (2000) Plant-parasitic nematodes and their management. From “Plant Nutrient Management in Hawaii’s Soils, Approaches for Tropical and Subtropical Agriculture”. College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa.
  • Sharma GC, Thakur BS, Kashyap AS (2005) Impact of NPK on the nematode populations and yield of plum (Prunus salicina). SHS Acta Horticulturae, 696: VII International Symposium on Temperate Zone Fruits in the Tropics and Subtropics - Part Two. doi: 10.17660/ActaHortic.2005.696.77
  • Siddiqui IA, Sher SA & French AM (1973) Distribution of Plant Parasitic Nematodes in California. State of California Department of Food and Agriculture, Division of Plant Industry. 324p.
  • Söğüt MA, Devran Z, Arici ŞE, Şan B, Yildirim AN (2013) Host reactions of root lesion nematodes (Pratylenchus spp.) on the rootstocks of pome and stone. Turkish Journal of Entomology 37(2), 239-248.
  • Taning LM, Lippens L, Formesyn E, Wesemael W (2023) Impact of cover crops on population density of the root-lesion nematode Pratylenchus penetrans. Preprint DOI: https://doi.org/10.21203/rs.3.rs-3338686/v1
  • Townshend JL (1990) Growth of ‘Bartlett’ pear seedlings in response to number of root-lesions nematodes and temperature. HortSci, 25: 318-320
  • Yorston J M (1969). The interactions of Pratylenchus penetrans with host plants, Longidorus elongatus and Verticillium dahliae. PhD Thesis Oregon State University, 55 pp.

HOST PLANT N°11: Prunus persica (PRNPS) 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):
 
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):
 
Yes
 
Conclusion:
 
Candidate

 
Justification:
 
Pratylenchus penetrans is cosmopolitan and has more than 350 hosts including woody plants (e.g., fruit trees, roses) and herbaceous plants (e.g., potato, vegetables) (Moens & Perry, 2009, CABI, 2021), e.g., Malus is a good host for Pratylenchus penetrans (aaltjesschema, 2019). Also Pyrus spp., Cydonia oblonga, Pistacia vera and many Prunus spp. can be hosts of P. penetrans (Hoekstra & Oostenbrink, 1962; Askary et al., 2012; Merrifield, 2000). Ficus carica is not mentioned as hosts and information of Pratylenchus penetrans on Pistacia vera is scarce (PlantwisePlus Knowledge Bank, 2023; Fatemy, 2009), this could be linked to P. penetrans being a nematode from mostly temperate climates and fig and pistachio being more Mediterranean crops. P. penetrans can complete its entire life cycle within the roots of plants.
Pratylenchus spp. are migratory endoparasites that enter the host root for feeding and reproduction and move freely within the tissue. Consequently, they spend much of their life cycle in roots and are found in soil when the host plants are senescing, stressed or diseased, or when their hosts have been ploughed up after harvest (Castillo and Vovlas, 2007).
P. penetrans occurs mostly on sandy and peaty soil. The transport of infected plants or those growing in infested soils is one of the principal means by which these nematodes are disseminated (Lehman, 1994; Anonymous, 1999). Bare-rooted plants are often contaminated by soil particles which may contain nematodes. Roots can host endoparasitic nematodes that are not removed by washing treatments (Lehman, 1994). In this context, it is essential that the plant propagation material be free of this pathogen (Allen, 1949). Because it can survive in soil, it can be dispersed by land vehicles etc.; within a field by cultivation, and can be introduced to non-infested sites by poorly sanitized farm equipment. However, measures (including hygiene) can limit the importance of such alternative pathways.
In responses to the questionnaire, DE, FR and NL supported deregulation in the EU because soilborne and widespread in production areas.
Considering the numerous bibliographic references that highlight the importance of plants for planting as an important pathway, and the existence of measures that can reduce the role of the others reported pathways, host plants for planting with roots, with or without soil or growing media, are considered as a main pathway.

5 - Economic impact:

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

Justification:
 
Pratylenchus penetrans is well recognized as economically important pest of stone-fruits (Mai and Parker, 1967; Townshend, 1990; Clavero-Camacho et al., 2024).
Much of the damage caused by root-lesion nematodes in stone fruits (Prunus spp.) results from their ability to induce extensive root necrosis. Nematode invasion of young roots induces reddish brown, elongated lesions. Root lesions darken with age, necrosis often spreads to affect the entire root, growth ceases, and the root dies. Severe infection may destroy the fine roots. Heavy infections often result in small root systems and stunted trees. Symptoms are more common on young trees than on old trees (Bird & Melakeberhan, 1995).
Depending on the level of P. penetrans present in the soil, damage might occur :
- Prunus dulcis: in the NEMAPLEX (2024) database, Prunus dulcis is reported as susceptible (= high level of nematode reproduction) to Pratylenchus penetrans (Siddiqui et al., 1973).
- Prunus armeniaca & Prunus domestica: mentioned as host. In the NEMAPLEX (2024) database, Prunus armeniaca is reported as susceptible (= high level of nematode reproduction) to Pratylenchus penetrans (Siddiqui et al., 1973).
- Prunus avium & Prunus cerasus: Initial population of 80/100 g soil necessary for growth reduction (Nyczepir and Halbrendt 1993). In NE U.S., reduced yield and shortened productive life of Montmorency cherry on Mazard and Mahaleb rootstocks; parasitized trees were less winter hardy (Nyczepir and Halbrendt 1993). In pots, seedlings grown for 12 weeks in steam-fumigated orchard soil with a history of replant disease containing a mixed population of 7 P. penetrans and P. projectus/100 g weighed 46% more and were 64% taller than seedlings grown in non-treated soil (Mai and Abawi 1978), (Cited in Merrifield, 2000). Pratylenchus penetrans has been responsible for severe decline and for replating failure in many cherry orchards. Also, this nematode can lower the resistance of plants to other pathogens (Anonymous, 1999).
- Prunus cerasifera: Initial population of 320/100 g soil necessary for growth reduction (Nyczepir and Halbrendt 1993). (Cited in Merrifield, 2000)
- Prunus persica: 5/100 g soil (Barker et al. 1976). Root impairment results in loss of vigour and yields of mature trees, but P. penetrans’ role in orchard replant problems is probably more economically important (Nyczepir and Halbrendt 1993). Pratylenchus penetrans has been responsible for severe decline and for replating failure in many peach orchards. Also, this nematode can lower the resistance of plants to other pathogens (Anonymous, 1999). In pots, seedling height was significantly reduced 40% by 114/100 cm3, 60% by 228/100 cm3, and 75% by 457/100 cm3 (Cited in Merrifield, 2000).
- Prunus salicina: In a Prunus salicina (var. Santa Rosa) orchard located in India, Pratylenchus penetrans was the predominant plant-parasitic nematode, with populations of 150-380 nematodes per 200 cc soil (Sharma et al., 2005).
In the responses to the questionnaire, FR supported deregulation in the EU, commenting that the pest had a 'low nuisance level on fruit plants'.

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 
Medium to 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?
 
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:
 
Evidence of its economic impact is available in the literature and confirmed by Spanish experts.
The damage caused by Pratylenchus is usually most severe in light-textured soils that are low in nutrients (e.g. nitrogen, potassium, or calcium) and in organic matter (Anonymous, 1999). pH and soil texture were the most influential variables in Pratylenchus distribution and abundance during the study of Clavero-Camacho et al. (2024) on plant parasitic nematodes affecting Prunus species in Spain.

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:
 
Crop rotation is difficult because of the wide host range of Pratylenchus penetrans, including weeds. Pratylenchus penetrans can propagate well on many crops, sometimes without causing damage (symptomless) (aaltjesschema). Recent research indicated that with proper choice of selected cultivars of cover crops, P. penetrans can be controlled but further breeding efforts are needed. Although some cover crops can reduce the population of Pratylenchus penetrans (Taning et al., 2023). Since many weeds can also be a host, adequate weed control is important (Aaltjesschema, 2019). Crop rotation is also a limited option since woody crops remain in soil for decades and the host-range of many of this of the plant parasitic nematodes is wide (Castillo y Vovlas, 2007).

Growing Tagetes spp. (e.g. Tagetes patula) can reduce the population considerably (Evenhuis et al., 2004). The authors predicted that strawberries could be grown for about 7 successive years without economic damage due to the root lesion nematode. Pudasaini et al. (2006) showed that Tagetes can reduce P. penetrans exponentially in time under marigold. The effect of marigold was persistent as no increase in P. penetrans densities over the whole soil profile was noticed after two crop cycles of host plants.

Use of clean soil: The propagation material is kept either in containers of sterilized growing medium or in soil that has been tested and found free from various nematodes (e.g. EPPO 2022).

Soil fumigation: dependent on legislation. Preplant soil fumigation does not eradicate nematodes but dramatically reduces nematode numbers. The nematodes return to their original population density (or greater) within 2 or 3 years after planting, but the absence of nematode pressure during the initial years of establishment is critical for trees to develop strong, healthy root systems (Abawi & Mai, 2014). With the progressive phase-out of chemical nematicides such as Aldicarb, Carbofuran, and 1,3-Dichloropropene, the effectiveness and sustainability of current plant-parasitic nematode management strategies remain limited (Barbosa et al., 2022).

Healthy plants: To prevent the introduction of nematode problems, new orchards should be established with trees obtained from reputable nurseries that treat their soils for nematodes (Abawi & Mai, 2014).

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.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
Yes

Proposed Risk management measure:
 
Non-Certified material (‘Conformitas Agraria Communitatis (CAC)’):
• Mother plants have been produced in a pest free place/site of production
or
• Material obtained from mother plants does not contain roots and soil

AND

• Plants have been produced in soil/growing medium considered free from P. penetrans (e.g. tested soil, use of sterilized growing media or soil-free).

Justification (if necessary):
 
The risk of transmission of this nematode is restricted to materials with roots and soil. Generally, material obtained from mother plants (e.g. buds, cuttings...) doesn’t contain roots and soil. The critical point to avoid the spread of this pest is in the nurseries where certified and CAC seedlings are produced for marketing to growers or end users. Considering that detection by inspection is practically impossible when no symptoms are observed, that symptomology is non-specific (both above and below ground) and the complexity to perform laboratory testing, the fruit SEWG considered that PFA should not be proposed as an option. The Fruit SEWG also considered that an option requiring not growing hosts during > 5 years was not realistic considering how polyphagous the pest is.
Hot water treatments with some time-temperature schedules have been shown to be effective against the pest (Anonymous, 1999; Lim et al., 2024). Further work would be needed to validate if these schedules are applicable to the different host species under practical circumstances.

[During consultation on draft recommendations, NL commented that it will be very difficult if not impossible to find production sites that are free, unless the plants are grown indoor in pots.] The Fruit SEWG considered that on one hand the pest has a very wide host range and is widespread in some countries (e.g. in NL); on the other hand, in other countries (e.g. in ES or other countries), soils are not so infested. But plant for planting is a significant pathway. It is an endoparasite, moving with plants for planting. It is difficult to see the symptoms since this involves uprooting the plant (only possible for Fragaria). The fruit SEWG considered that the decision should be taken later by risk managers on whether the measure is maintained to limit economic impact to end users or withdrawn to limit economic burden to the producer of plants for planting.

REFERENCES:
  • Aaltjesschema (2019). Website on information and crop rotation for various crops. The website is s product of Wageningen UR, nematology PPO-AGV. Website is accessible until 31 March 2024, only information for perennial plants and fruit crops will still be available. https://www.aaltjesschema.nl/Home.aspx
  • Abawi GS & Mai WF (2014) Root lesion nematodes (revised by Halbrendt JM). In Compendium of apple and pear diseases and pests, second edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, USA: 113-114.
  • Allen MW (1949). Root-lesion nematodes: resistant rootstocks most promising method of control. California Agriculture, January: 13-14.
  • Anonymous (1998) Pratylenchus on Oregon crops: Pratylenchus damage levels for Oregon crops: a literature survey. https://bpp.oregonstate.edu/pratylenchus-oregon-crops.
  • Anonymous (1999) Lesion nematodes. University of Illinois Extension. RPD, 1103. May 1999.
  • Askary TH, Banday SA, Iqbal U, Khan AA, Mir MM & Waliullah MIS (2012) Plant parasitic nematode diversity in pome, stone and nut fruits. In Agroecology and Strategies for Climate Change (ed Lichtfouse E). Springer Sicens+Business Media B.V. DOI 10.1007/978-94-007-1905-7_10. 237-268.
  • Barbosa P, Faria JMS, Figueiredo AC, Mota M & Vicente CSL (2022) Control of the root lesion Pratylenchus penetrans: the effect of nematicidal activity of plant-derived compounds. Revista de Ciencias Agrarias, 45 (4): 649-652. https://doi.org/10.19084/rca.28749
  • Bird GW & Melakeberhan H (1995) Root-Lesion Nematodes (Pratylenchus spp.). In Compendium of Stone Fruit Diseases (eds Ogawa JM, Zehr EI, Bird GW, Ritchie DF, Uriu K & Uyemoto JK)
  • Bucki P, Qing X, Castillo P, Gamliel A, Dobrinin S, Alon T, Miyara SB (2020) The genus Pratylenchus (Nematoda: Pratylenchidae) in Israel: from taxonomy to control practices. Plants 9, 1475; doi:10.3390/plants9111475.
  • Castillo P, Vovlas (2007) Biology and ecology of Pratylenchus. In “Pratylechus (Nematoda: Pratylenchidae): diagnosis, biology, pathogenicity and management”. Nematology Monographs & Perspective 6, 305-324.
  • Clavero-Camacho I, Archidona-Yuste A, Cantalapiedra-Navarrete C, Castillo P & Palomares-Rius JE (2024) Prevalence and ecological factors affecting the distribution of plant-parasitic nematodes in Prunus groves in Spain. Journal of Integrative Agriculture, 23(2): 585-589.
  • EPPO (2022) PM 4/17 (3) Certification scheme for olive trees and rootstocks. EPPO Bulletin 52, 590–60. DOI: 10.1111/epp.1288
  • Evenhuis A, Korthals G & Molendijk L. (2004). Tagetes patula as an effective catch crop for long-term control of Pratylenchus penetrans. Nematology, 6(6), 877-881. https://doi.org/10.1163/1568541044038632
  • Fatemy S (2009). Integrated management of pistachio nematodes. In Integrated Management of Fruit Crops and Forest Nematodes (eds Ciancio A & Mukerji KG). Springer Science+Business Media BV, 243-252.
  • Goodey JB, Franklin MT &Hooper DJ (1965) The nematode parasites of plants catalogued under their host. Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, England. Third Edition.
  • Hoestra H & Oostenbrink M (1962) Nematodes in relation to plant growth IV. Pratylenchus penetrans (Cobb) on orchard trees. Neth. J. agric. Sei., Vol. 10 (1962) No. 4 (November): 286-296
  • Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MGK, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WML & Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14 (9): 946-961.
  • Lehman PS (1994) Dissemination of phytoparasitic nematodes. Nematology Circular, No 28. Fla. Dept. Agric.& Consumer Services. Division of Plant Industry.
  • Lim G-E, Heo M-S & Park M-G (2024) Hot Water Treatment as a Quarantine Measure for Controlling Pratylenchus penetrans Cobb in Syngonium podophyllum Schott and Perilla frutescens Britton. Agriculture 14, 582. https://doi.org/10.3390/agriculture14040582.
  • Moens M & Perry RN (2009) Migratory plant endoparasitic nematodes: a group rich in contrasts and divergence. Annual Review of Phytopathology 47, 313–32.
  • NEMAPLEX (2024) Host Status of a Plant Genus and species to Nematodes. http://nemaplex.ucdavis.edu/ (accessed: 07/11/2024)
  • Nyczepir AP (1991) Nematode management strategies in stone fruits in the United States. Journal of Nematology 23(3), 334-341.
  • Mai WF & Abawi GS (1978) Determining the cause and extent of apple, cherry, and pear replant diseases under controlled conditions. Phytopathology 68, 1540-1544.
  • Merrifield K (2000) Plant-parasitic damage levels for Oregon nursery crops: A literature survey. Biology, host ranges, and damage levels of root-parasitic nematodes on Oregon nursery crops (Draft: 2000). https://bpp.oregonstate.edu/sites/agscid7/files/plant-parasitic-damage-levels-for-oregon-nursery-crops.pdf
  • Nyczepier A P & Halbrendt JM (1993) Nematode pests of deciduous fruit and nut trees. In Plant Parasitic Nematodes in Temperate Agriculture (eds Evans K, Trudgill DL & Webster JM). CAB International, Wallingford, England. pp. 381-425
  • PlantwisePlus Knowledge Bank (2023). Pratylenchus penetrans (nematode, northern root lesion). (accessed 26/Apr/2024). https://plantwiseplusknowledgebank.org/doi/full/10.1079/pwkb.species.43900
  • Pudasaini MP, Viaene N & Moens M (2006) Effect of marigold (Tagetes patula) on population dynamics of Pratylenchus penetrans in a field. Nematology 8, 477-84.
  • Schmitt DP & Sipes BS (2000) Plant-parasitic nematodes and their management. From “Plant Nutrient Management in Hawaii’s Soils, Approaches for Tropical and Subtropical Agriculture”. College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa.
  • Sharma GC, Thakur BS, Kashyap AS (2005) Impact of NPK on the nematode populations and yield of plum (Prunus salicina). SHS Acta Horticulturae, 696: VII International Symposium on Temperate Zone Fruits in the Tropics and Subtropics - Part Two. doi: 10.17660/ActaHortic.2005.696.77
  • Siddiqui IA, Sher SA & French AM (1973) Distribution of Plant Parasitic Nematodes in California. State of California Department of Food and Agriculture, Division of Plant Industry. 324p.
  • Söğüt MA, Devran Z, Arici ŞE, Şan B, Yildirim AN (2013) Host reactions of root lesion nematodes (Pratylenchus spp.) on the rootstocks of pome and stone. Turkish Journal of Entomology 37(2), 239-248.
  • Taning LM, Lippens L, Formesyn E, Wesemael W (2023) Impact of cover crops on population density of the root-lesion nematode Pratylenchus penetrans. Preprint DOI: https://doi.org/10.21203/rs.3.rs-3338686/v1
  • Townshend JL (1990) Growth of ‘Bartlett’ pear seedlings in response to number of root-lesions nematodes and temperature. HortSci, 25: 318-320
  • Yorston J M (1969). The interactions of Pratylenchus penetrans with host plants, Longidorus elongatus and Verticillium dahliae. PhD Thesis Oregon State University, 55 pp.

HOST PLANT N°12: Prunus salicina (PRNSC) 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):
 
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):
 
Yes
 
Conclusion:
 
Candidate

 
Justification:
 
Pratylenchus penetrans is cosmopolitan and has more than 350 hosts including woody plants (e.g., fruit trees, roses) and herbaceous plants (e.g., potato, vegetables) (Moens & Perry, 2009, CABI, 2021), e.g., Malus is a good host for Pratylenchus penetrans (aaltjesschema, 2019). Also Pyrus spp., Cydonia oblonga, Pistacia vera and many Prunus spp. can be hosts of P. penetrans (Hoekstra & Oostenbrink, 1962; Askary et al., 2012; Merrifield, 2000). Ficus carica is not mentioned as hosts and information of Pratylenchus penetrans on Pistacia vera is scarce (PlantwisePlus Knowledge Bank, 2023; Fatemy, 2009), this could be linked to P. penetrans being a nematode from mostly temperate climates and fig and pistachio being more Mediterranean crops. P. penetrans can complete its entire life cycle within the roots of plants.
Pratylenchus spp. are migratory endoparasites that enter the host root for feeding and reproduction and move freely within the tissue. Consequently, they spend much of their life cycle in roots and are found in soil when the host plants are senescing, stressed or diseased, or when their hosts have been ploughed up after harvest (Castillo and Vovlas, 2007).
P. penetrans occurs mostly on sandy and peaty soil. The transport of infected plants or those growing in infested soils is one of the principal means by which these nematodes are disseminated (Lehman, 1994; Anonymous, 1999). Bare-rooted plants are often contaminated by soil particles which may contain nematodes. Roots can host endoparasitic nematodes that are not removed by washing treatments (Lehman, 1994). In this context, it is essential that the plant propagation material be free of this pathogen (Allen, 1949). Because it can survive in soil, it can be dispersed by land vehicles etc.; within a field by cultivation, and can be introduced to non-infested sites by poorly sanitized farm equipment. However, measures (including hygiene) can limit the importance of such alternative pathways.
In responses to the questionnaire, DE, FR and NL supported deregulation in the EU because soilborne and widespread in production areas.
Considering the numerous bibliographic references that highlight the importance of plants for planting as an important pathway, and the existence of measures that can reduce the role of the others reported pathways, host plants for planting with roots, with or without soil or growing media, are considered as a main pathway.

5 - Economic impact:

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

Justification:
 
Pratylenchus penetrans is well recognized as economically important pest of stone-fruits (Mai and Parker, 1967; Townshend, 1990; Clavero-Camacho et al., 2024).
Much of the damage caused by root-lesion nematodes in stone fruits (Prunus spp.) results from their ability to induce extensive root necrosis. Nematode invasion of young roots induces reddish brown, elongated lesions. Root lesions darken with age, necrosis often spreads to affect the entire root, growth ceases, and the root dies. Severe infection may destroy the fine roots. Heavy infections often result in small root systems and stunted trees. Symptoms are more common on young trees than on old trees (Bird & Melakeberhan, 1995).
Depending on the level of P. penetrans present in the soil, damage might occur :
- Prunus dulcis: in the NEMAPLEX (2024) database, Prunus dulcis is reported as susceptible (= high level of nematode reproduction) to Pratylenchus penetrans (Siddiqui et al., 1973).
- Prunus armeniaca & Prunus domestica: mentioned as host. In the NEMAPLEX (2024) database, Prunus armeniaca is reported as susceptible (= high level of nematode reproduction) to Pratylenchus penetrans (Siddiqui et al., 1973).
- Prunus avium & Prunus cerasus: Initial population of 80/100 g soil necessary for growth reduction (Nyczepir and Halbrendt 1993). In NE U.S., reduced yield and shortened productive life of Montmorency cherry on Mazard and Mahaleb rootstocks; parasitized trees were less winter hardy (Nyczepir and Halbrendt 1993). In pots, seedlings grown for 12 weeks in steam-fumigated orchard soil with a history of replant disease containing a mixed population of 7 P. penetrans and P. projectus/100 g weighed 46% more and were 64% taller than seedlings grown in non-treated soil (Mai and Abawi 1978), (Cited in Merrifield, 2000). Pratylenchus penetrans has been responsible for severe decline and for replating failure in many cherry orchards. Also, this nematode can lower the resistance of plants to other pathogens (Anonymous, 1999).
- Prunus cerasifera: Initial population of 320/100 g soil necessary for growth reduction (Nyczepir and Halbrendt 1993). (Cited in Merrifield, 2000)
- Prunus persica: 5/100 g soil (Barker et al. 1976). Root impairment results in loss of vigour and yields of mature trees, but P. penetrans’ role in orchard replant problems is probably more economically important (Nyczepir and Halbrendt 1993). Pratylenchus penetrans has been responsible for severe decline and for replating failure in many peach orchards. Also, this nematode can lower the resistance of plants to other pathogens (Anonymous, 1999). In pots, seedling height was significantly reduced 40% by 114/100 cm3, 60% by 228/100 cm3, and 75% by 457/100 cm3 (Cited in Merrifield, 2000).
- Prunus salicina: In a Prunus salicina (var. Santa Rosa) orchard located in India, Pratylenchus penetrans was the predominant plant-parasitic nematode, with populations of 150-380 nematodes per 200 cc soil (Sharma et al., 2005).
In the responses to the questionnaire, FR supported deregulation in the EU, commenting that the pest had a 'low nuisance level on fruit plants'.

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 
Medium to 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?
 
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:
 
Evidence of its economic impact is available in the literature and confirmed by Spanish experts.
The damage caused by Pratylenchus is usually most severe in light-textured soils that are low in nutrients (e.g. nitrogen, potassium, or calcium) and in organic matter (Anonymous, 1999). pH and soil texture were the most influential variables in Pratylenchus distribution and abundance during the study of Clavero-Camacho et al. (2024) on plant parasitic nematodes affecting Prunus species in Spain.

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:
 
Crop rotation is difficult because of the wide host range of Pratylenchus penetrans, including weeds. Pratylenchus penetrans can propagate well on many crops, sometimes without causing damage (symptomless) (aaltjesschema). Recent research indicated that with proper choice of selected cultivars of cover crops, P. penetrans can be controlled but further breeding efforts are needed. Although some cover crops can reduce the population of Pratylenchus penetrans (Taning et al., 2023). Since many weeds can also be a host, adequate weed control is important (Aaltjesschema, 2019). Crop rotation is also a limited option since woody crops remain in soil for decades and the host-range of many of this of the plant parasitic nematodes is wide (Castillo y Vovlas, 2007).

Growing Tagetes spp. (e.g. Tagetes patula) can reduce the population considerably (Evenhuis et al., 2004). The authors predicted that strawberries could be grown for about 7 successive years without economic damage due to the root lesion nematode. Pudasaini et al. (2006) showed that Tagetes can reduce P. penetrans exponentially in time under marigold. The effect of marigold was persistent as no increase in P. penetrans densities over the whole soil profile was noticed after two crop cycles of host plants.

Use of clean soil: The propagation material is kept either in containers of sterilized growing medium or in soil that has been tested and found free from various nematodes (e.g. EPPO 2022).

Soil fumigation: dependent on legislation. Preplant soil fumigation does not eradicate nematodes but dramatically reduces nematode numbers. The nematodes return to their original population density (or greater) within 2 or 3 years after planting, but the absence of nematode pressure during the initial years of establishment is critical for trees to develop strong, healthy root systems (Abawi & Mai, 2014). With the progressive phase-out of chemical nematicides such as Aldicarb, Carbofuran, and 1,3-Dichloropropene, the effectiveness and sustainability of current plant-parasitic nematode management strategies remain limited (Barbosa et al., 2022).

Healthy plants: To prevent the introduction of nematode problems, new orchards should be established with trees obtained from reputable nurseries that treat their soils for nematodes (Abawi & Mai, 2014).

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.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
Yes

Proposed Risk management measure:
 
Non-Certified material (‘Conformitas Agraria Communitatis (CAC)’):
• Mother plants have been produced in a pest free place/site of production
or
• Material obtained from mother plants does not contain roots and soil

AND

• Plants have been produced in soil/growing medium considered free from P. penetrans (e.g. tested soil, use of sterilized growing media or soil-free).

Justification (if necessary):
 
The risk of transmission of this nematode is restricted to materials with roots and soil. Generally, material obtained from mother plants (e.g. buds, cuttings...) doesn’t contain roots and soil. The critical point to avoid the spread of this pest is in the nurseries where certified and CAC seedlings are produced for marketing to growers or end users. Considering that detection by inspection is practically impossible when no symptoms are observed, that symptomology is non-specific (both above and below ground) and the complexity to perform laboratory testing, the fruit SEWG considered that PFA should not be proposed as an option. The Fruit SEWG also considered that an option requiring not growing hosts during > 5 years was not realistic considering how polyphagous the pest is.
Hot water treatments with some time-temperature schedules have been shown to be effective against the pest (Anonymous, 1999; Lim et al., 2024). Further work would be needed to validate if these schedules are applicable to the different host species under practical circumstances.

[During consultation on draft recommendations, NL commented that it will be very difficult if not impossible to find production sites that are free, unless the plants are grown indoor in pots.] The Fruit SEWG considered that on one hand the pest has a very wide host range and is widespread in some countries (e.g. in NL); on the other hand, in other countries (e.g. in ES or other countries), soils are not so infested. But plant for planting is a significant pathway. It is an endoparasite, moving with plants for planting. It is difficult to see the symptoms since this involves uprooting the plant (only possible for Fragaria). The fruit SEWG considered that the decision should be taken later by risk managers on whether the measure is maintained to limit economic impact to end users or withdrawn to limit economic burden to the producer of plants for planting.

REFERENCES:
  • Aaltjesschema (2019). Website on information and crop rotation for various crops. The website is s product of Wageningen UR, nematology PPO-AGV. Website is accessible until 31 March 2024, only information for perennial plants and fruit crops will still be available. https://www.aaltjesschema.nl/Home.aspx
  • Abawi GS & Mai WF (2014) Root lesion nematodes (revised by Halbrendt JM). In Compendium of apple and pear diseases and pests, second edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, USA: 113-114.
  • Allen MW (1949). Root-lesion nematodes: resistant rootstocks most promising method of control. California Agriculture, January: 13-14.
  • Anonymous (1998) Pratylenchus on Oregon crops: Pratylenchus damage levels for Oregon crops: a literature survey. https://bpp.oregonstate.edu/pratylenchus-oregon-crops.
  • Anonymous (1999) Lesion nematodes. University of Illinois Extension. RPD, 1103. May 1999.
  • Askary TH, Banday SA, Iqbal U, Khan AA, Mir MM & Waliullah MIS (2012) Plant parasitic nematode diversity in pome, stone and nut fruits. In Agroecology and Strategies for Climate Change (ed Lichtfouse E). Springer Sicens+Business Media B.V. DOI 10.1007/978-94-007-1905-7_10. 237-268.
  • Barbosa P, Faria JMS, Figueiredo AC, Mota M & Vicente CSL (2022) Control of the root lesion Pratylenchus penetrans: the effect of nematicidal activity of plant-derived compounds. Revista de Ciencias Agrarias, 45 (4): 649-652. https://doi.org/10.19084/rca.28749
  • Bird GW & Melakeberhan H (1995) Root-Lesion Nematodes (Pratylenchus spp.). In Compendium of Stone Fruit Diseases (eds Ogawa JM, Zehr EI, Bird GW, Ritchie DF, Uriu K & Uyemoto JK)
  • Bucki P, Qing X, Castillo P, Gamliel A, Dobrinin S, Alon T, Miyara SB (2020) The genus Pratylenchus (Nematoda: Pratylenchidae) in Israel: from taxonomy to control practices. Plants 9, 1475; doi:10.3390/plants9111475.
  • Castillo P, Vovlas (2007) Biology and ecology of Pratylenchus. In “Pratylechus (Nematoda: Pratylenchidae): diagnosis, biology, pathogenicity and management”. Nematology Monographs & Perspective 6, 305-324.
  • Clavero-Camacho I, Archidona-Yuste A, Cantalapiedra-Navarrete C, Castillo P & Palomares-Rius JE (2024) Prevalence and ecological factors affecting the distribution of plant-parasitic nematodes in Prunus groves in Spain. Journal of Integrative Agriculture, 23(2): 585-589.
  • EPPO (2022) PM 4/17 (3) Certification scheme for olive trees and rootstocks. EPPO Bulletin 52, 590–60. DOI: 10.1111/epp.1288
  • Evenhuis A, Korthals G & Molendijk L. (2004). Tagetes patula as an effective catch crop for long-term control of Pratylenchus penetrans. Nematology, 6(6), 877-881. https://doi.org/10.1163/1568541044038632
  • Fatemy S (2009). Integrated management of pistachio nematodes. In Integrated Management of Fruit Crops and Forest Nematodes (eds Ciancio A & Mukerji KG). Springer Science+Business Media BV, 243-252.
  • Goodey JB, Franklin MT &Hooper DJ (1965) The nematode parasites of plants catalogued under their host. Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, England. Third Edition.
  • Hoestra H & Oostenbrink M (1962) Nematodes in relation to plant growth IV. Pratylenchus penetrans (Cobb) on orchard trees. Neth. J. agric. Sei., Vol. 10 (1962) No. 4 (November): 286-296
  • Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MGK, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WML & Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14 (9): 946-961.
  • Lehman PS (1994) Dissemination of phytoparasitic nematodes. Nematology Circular, No 28. Fla. Dept. Agric.& Consumer Services. Division of Plant Industry.
  • Lim G-E, Heo M-S & Park M-G (2024) Hot Water Treatment as a Quarantine Measure for Controlling Pratylenchus penetrans Cobb in Syngonium podophyllum Schott and Perilla frutescens Britton. Agriculture 14, 582. https://doi.org/10.3390/agriculture14040582.
  • Moens M & Perry RN (2009) Migratory plant endoparasitic nematodes: a group rich in contrasts and divergence. Annual Review of Phytopathology 47, 313–32.
  • NEMAPLEX (2024) Host Status of a Plant Genus and species to Nematodes. http://nemaplex.ucdavis.edu/ (accessed: 07/11/2024)
  • Nyczepir AP (1991) Nematode management strategies in stone fruits in the United States. Journal of Nematology 23(3), 334-341.
  • Mai WF & Abawi GS (1978) Determining the cause and extent of apple, cherry, and pear replant diseases under controlled conditions. Phytopathology 68, 1540-1544.
  • Merrifield K (2000) Plant-parasitic damage levels for Oregon nursery crops: A literature survey. Biology, host ranges, and damage levels of root-parasitic nematodes on Oregon nursery crops (Draft: 2000). https://bpp.oregonstate.edu/sites/agscid7/files/plant-parasitic-damage-levels-for-oregon-nursery-crops.pdf
  • Nyczepier A P & Halbrendt JM (1993) Nematode pests of deciduous fruit and nut trees. In Plant Parasitic Nematodes in Temperate Agriculture (eds Evans K, Trudgill DL & Webster JM). CAB International, Wallingford, England. pp. 381-425
  • PlantwisePlus Knowledge Bank (2023). Pratylenchus penetrans (nematode, northern root lesion). (accessed 26/Apr/2024). https://plantwiseplusknowledgebank.org/doi/full/10.1079/pwkb.species.43900
  • Pudasaini MP, Viaene N & Moens M (2006) Effect of marigold (Tagetes patula) on population dynamics of Pratylenchus penetrans in a field. Nematology 8, 477-84.
  • Schmitt DP & Sipes BS (2000) Plant-parasitic nematodes and their management. From “Plant Nutrient Management in Hawaii’s Soils, Approaches for Tropical and Subtropical Agriculture”. College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa.
  • Sharma GC, Thakur BS, Kashyap AS (2005) Impact of NPK on the nematode populations and yield of plum (Prunus salicina). SHS Acta Horticulturae, 696: VII International Symposium on Temperate Zone Fruits in the Tropics and Subtropics - Part Two. doi: 10.17660/ActaHortic.2005.696.77
  • Siddiqui IA, Sher SA & French AM (1973) Distribution of Plant Parasitic Nematodes in California. State of California Department of Food and Agriculture, Division of Plant Industry. 324p.
  • Söğüt MA, Devran Z, Arici ŞE, Şan B, Yildirim AN (2013) Host reactions of root lesion nematodes (Pratylenchus spp.) on the rootstocks of pome and stone. Turkish Journal of Entomology 37(2), 239-248.
  • Taning LM, Lippens L, Formesyn E, Wesemael W (2023) Impact of cover crops on population density of the root-lesion nematode Pratylenchus penetrans. Preprint DOI: https://doi.org/10.21203/rs.3.rs-3338686/v1
  • Townshend JL (1990) Growth of ‘Bartlett’ pear seedlings in response to number of root-lesions nematodes and temperature. HortSci, 25: 318-320
  • Yorston J M (1969). The interactions of Pratylenchus penetrans with host plants, Longidorus elongatus and Verticillium dahliae. PhD Thesis Oregon State University, 55 pp.

HOST PLANT N°13: 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?
 
No
 
Conclusion:
 
Evaluation continues

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:
 
Pratylenchus penetrans is cosmopolitan and has more than 350 hosts including woody plants (e.g., fruit trees, roses) and herbaceous plants (e.g., potato, vegetables) (Moens & Perry, 2009, CABI, 2021), e.g., Malus is a good host for Pratylenchus penetrans (aaltjesschema, 2019). Also Pyrus spp., Cydonia oblonga, Pistacia vera and many Prunus spp. can be hosts of P. penetrans (Hoekstra & Oostenbrink, 1962; Askary et al., 2012; Merrifield, 2000). Ficus carica is not mentioned as hosts and information of Pratylenchus penetrans on Pistacia vera is scarce (PlantwisePlus Knowledge Bank, 2023; Fatemy, 2009), this could be linked to P. penetrans being a nematode from mostly temperate climates and fig and pistachio being more Mediterranean crops. P. penetrans can complete its entire life cycle within the roots of plants.
Pratylenchus spp. are migratory endoparasites that enter the host root for feeding and reproduction and move freely within the tissue. Consequently, they spend much of their life cycle in roots and are found in soil when the host plants are senescing, stressed or diseased, or when their hosts have been ploughed up after harvest (Castillo and Vovlas, 2007).
P. penetrans occurs mostly on sandy and peaty soil. The transport of infected plants or those growing in infested soils is one of the principal means by which these nematodes are disseminated (Lehman, 1994; Anonymous, 1999). Bare-rooted plants are often contaminated by soil particles which may contain nematodes. Roots can host endoparasitic nematodes that are not removed by washing treatments (Lehman, 1994). In this context, it is essential that the plant propagation material be free of this pathogen (Allen, 1949). Because it can survive in soil, it can be dispersed by land vehicles etc.; within a field by cultivation, and can be introduced to non-infested sites by poorly sanitized farm equipment. However, measures (including hygiene) can limit the importance of such alternative pathways.
In responses to the questionnaire, DE, FR and NL supported deregulation in the EU because soilborne and widespread in production areas.
Considering the numerous bibliographic references that highlight the importance of plants for planting as an important pathway, and the existence of measures that can reduce the role of the others reported pathways, host plants for planting with roots, with or without soil or growing media, are considered as a main pathway.

5 - Economic impact:

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

Justification:
 
In pome fruits, 25 to 150 individuals/100 cm3 soil of Pratylenchus spp. are considered damaging but can vary depending on soil texture (Anonymous, 1998). Apple rootstocks seem to be a better host for Pratylenchus penetrans than pear and quince rootstocks, which showed a moderate resistance (Söğüt et al., 2013). Cydonia oblonga mentioned as one of the main hosts (Plantwise). The pathogenicity of Pratylenchus penetrans on stone and pome fruit trees has been amply demonstrated by experimental evidence and field observations (e.g. Mai and Parker, 1967; Townshed, 1990).

In Pyrus, an initial population of 30/100 g soil is necessary for growth reduction; and P. penetrans is involved in pear replant problems in the USA and Canada (Nyczepir and Halbrendt 1993). In pots, seedlings grown for 12 weeks in steam-fumigated orchard soil with a history of replant disease containing a mixed population of 50 P. penetrans and P. projectus/100 g did not weight significantly more and were not significantly taller than seedlings grown in non-treated soil (Mai and Abawi 1978; from Merrifield, 2000).

Apples tend to be more sensitive to root lesion nematode damage than are pears, but other factors are also involved, since, pears are e.g. more often planted on heavier soils than are apples, which provides some protection since root lesion nematodes are more damaging in lighter soils (Abawi & Mai , 2014).

In the responses to the questionnaire, FR supported deregulation in the EU, commenting that the pest had a 'low nuisance level on fruit plants'.

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 
Medium to 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?
 
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:
 
The economic impact of this pathogen on Pyrus is widely demonstrated, as well as the potential impacts on other hosts (Prunus, Malus).
The damage caused by Pratylenchus is usually most severe in light-textured soils that are low in nutrients (e.g. nitrogen, potassium, or calcium) and in organic matter (Anonymous, 1999).

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:
 
Crop rotation is difficult because of the wide host range of Pratylenchus penetrans, including weeds. Pratylenchus penetrans can propagate well on many crops, sometimes without causing damage (symptomless) (aaltjesschema). Recent research indicated that with proper choice of selected cultivars of cover crops, P. penetrans can be controlled but further breeding efforts are needed. Although some cover crops can reduce the population of Pratylenchus penetrans (Taning et al., 2023). Since many weeds can also be a host, adequate weed control is important (Aaltjesschema, 2019). Crop rotation is also a limited option since woody crops remain in soil for decades and the host-range of many of this of the plant parasitic nematodes is wide (Castillo y Vovlas, 2007).

Growing Tagetes spp. (e.g. Tagetes patula) can reduce the population considerably (Evenhuis et al., 2004). The authors predicted that strawberries could be grown for about 7 successive years without economic damage due to the root lesion nematode. Pudasaini et al. (2006) showed that Tagetes can reduce P. penetrans exponentially in time under marigold. The effect of marigold was persistent as no increase in P. penetrans densities over the whole soil profile was noticed after two crop cycles of host plants.

Use of clean soil: The propagation material is kept either in containers of sterilized growing medium or in soil that has been tested and found free from various nematodes (e.g. EPPO 2022).

Soil fumigation: dependent on legislation. Preplant soil fumigation does not eradicate nematodes but dramatically reduces nematode numbers. The nematodes return to their original population density (or greater) within 2 or 3 years after planting, but the absence of nematode pressure during the initial years of establishment is critical for trees to develop strong, healthy root systems (Abawi & Mai, 2014). With the progressive phase-out of chemical nematicides such as Aldicarb, Carbofuran, and 1,3-Dichloropropene, the effectiveness and sustainability of current plant-parasitic nematode management strategies remain limited (Barbosa et al., 2022).

Healthy plants: To prevent the introduction of nematode problems, new orchards should be established with trees obtained from reputable nurseries that treat their soils for nematodes (Abawi & Mai, 2014).

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.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
Yes

Proposed Risk management measure:
 
Non-Certified material (‘Conformitas Agraria Communitatis (CAC)’):
• Mother plants have been produced in a pest free place/site of production
or
• Material obtained from mother plants does not contain roots and soil

AND

• Plants have been produced in soil/growing medium considered free from P. penetrans (e.g. tested soil, use of sterilized growing media or soil-free).

Justification (if necessary):
 
The risk of transmission of this nematode is restricted to materials with roots and soil. Generally, material obtained from mother plants (e.g. buds, cuttings...) doesn’t contain roots and soil. The critical point to avoid the spread of this pest is in the nurseries where certified and CAC seedlings are produced for marketing to growers or end users. Considering that symptoms may not be visible, that symptomology is non-specific (both above and below ground) and the complexity to perform laboratory testing, the fruit SEWG considered that PFA should not be proposed as an option. The Fruit SEWG also considered that an option requiring not growing hosts during > 5 years was not realistic considering how polyphagous the pest is.
Hot water treatments with some time-temperature schedules have been shown to be effective against the pest (Anonymous, 1999; Lim et al., 2024). Further work would be needed to validate if these schedules are applicable to the different host species under practical circumstances.

[During consultation on draft recommendations, NL commented that it will be very difficult if not impossible to find production sites that are free, unless the plants are grown indoor in pots.] The Fruit SEWG considered that on one hand the pest has a very wide host range and is widespread in some countries (e.g. in NL); on the other hand, in other countries (e.g. in ES or other countries), soils are not so infested. But plant for planting is a significant pathway. It is an endoparasite, moving with plants for planting. It is difficult to see the symptoms since this involves uprooting the plant (only possible for Fragaria). The fruit SEWG considered that the decision should be taken later by risk managers on whether the measure is maintained to limit economic impact to end users or withdrawn to limit economic burden to the producer of plants for planting.

REFERENCES:
  • Aaltjesschema (2019). Website on information and crop rotation for various crops. The website is s product of Wageningen UR, nematology PPO-AGV. Website is accessible until 31 March 2024, only information for perennial plants and fruit crops will still be available. https://www.aaltjesschema.nl/Home.aspx
  • Abawi GS & Mai WF (2014) Root lesion nematodes (revised by Halbrendt JM). In Compendium of apple and pear diseases and pests, second edition (eds Sutton TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, USA: 113-114.
  • Allen MW (1949). Root-lesion nematodes: resistant rootstocks most promising method of control. California Agriculture, January: 13-14.
  • Anonymous (1998) Pratylenchus on Oregon crops: Pratylenchus damage levels for Oregon crops: a literature survey. https://bpp.oregonstate.edu/pratylenchus-oregon-crops.
  • Anonymous (1999) Lesion nematodes. University of Illinois Extension. RPD, 1103. May 1999.
  • Askary TH, Banday SA, Iqbal U, Khan AA, Mir MM & Waliullah MIS (2012) Plant parasitic nematode diversity in pome, stone and nut fruits. In Agroecology and Strategies for Climate Change (ed Lichtfouse E). Springer Sicens+Business Media B.V. DOI 10.1007/978-94-007-1905-7_10. 237-268.
  • Barbosa P, Faria JMS, Figueiredo AC, Mota M & Vicente CSL (2022) Control of the root lesion Pratylenchus penetrans: the effect of nematicidal activity of plant-derived compounds. Revista de Ciencias Agrarias, 45 (4): 649-652. https://doi.org/10.19084/rca.28749
  • Bird GW & Melakeberhan H (1995) Root-Lesion Nematodes (Pratylenchus spp.). In Compendium of Stone Fruit Diseases (eds Ogawa JM, Zehr EI, Bird GW, Ritchie DF, Uriu K & Uyemoto JK)
  • Bucki P, Qing X, Castillo P, Gamliel A, Dobrinin S, Alon T, Miyara SB (2020) The genus Pratylenchus (Nematoda: Pratylenchidae) in Israel: from taxonomy to control practices. Plants 9, 1475; doi:10.3390/plants9111475.
  • Castillo P, Vovlas (2007) Biology and ecology of Pratylenchus. In “Pratylechus (Nematoda: Pratylenchidae): diagnosis, biology, pathogenicity and management”. Nematology Monographs & Perspective 6, 305-324.
  • Clavero-Camacho I, Archidona-Yuste A, Cantalapiedra-Navarrete C, Castillo P & Palomares-Rius JE (2024) Prevalence and ecological factors affecting the distribution of plant-parasitic nematodes in Prunus groves in Spain. Journal of Integrative Agriculture, 23(2): 585-589.
  • EPPO (2022) PM 4/17 (3) Certification scheme for olive trees and rootstocks. EPPO Bulletin 52, 590–60. DOI: 10.1111/epp.1288
  • Evenhuis A, Korthals G & Molendijk L. (2004). Tagetes patula as an effective catch crop for long-term control of Pratylenchus penetrans. Nematology, 6(6), 877-881. https://doi.org/10.1163/1568541044038632
  • Fatemy S (2009). Integrated management of pistachio nematodes. In Integrated Management of Fruit Crops and Forest Nematodes (eds Ciancio A & Mukerji KG). Springer Science+Business Media BV, 243-252.
  • Goodey JB, Franklin MT &Hooper DJ (1965) The nematode parasites of plants catalogued under their host. Commonwealth Agricultural Bureaux, Farnham Royal, Bucks, England. Third Edition.
  • Hoestra H & Oostenbrink M (1962) Nematodes in relation to plant growth IV. Pratylenchus penetrans (Cobb) on orchard trees. Neth. J. agric. Sei., Vol. 10 (1962) No. 4 (November): 286-296
  • Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MGK, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WML & Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14 (9): 946-961.
  • Lehman PS (1994) Dissemination of phytoparasitic nematodes. Nematology Circular, No 28. Fla. Dept. Agric.& Consumer Services. Division of Plant Industry.
  • Lim G-E, Heo M-S & Park M-G (2024) Hot Water Treatment as a Quarantine Measure for Controlling Pratylenchus penetrans Cobb in Syngonium podophyllum Schott and Perilla frutescens Britton. Agriculture 14, 582. https://doi.org/10.3390/agriculture14040582.
  • Moens M & Perry RN (2009) Migratory plant endoparasitic nematodes: a group rich in contrasts and divergence. Annual Review of Phytopathology 47, 313–32.
  • NEMAPLEX (2024) Host Status of a Plant Genus and species to Nematodes. http://nemaplex.ucdavis.edu/ (accessed: 07/11/2024)
  • Nyczepir AP (1991) Nematode management strategies in stone fruits in the United States. Journal of Nematology 23(3), 334-341.
  • Mai WF & Abawi GS (1978) Determining the cause and extent of apple, cherry, and pear replant diseases under controlled conditions. Phytopathology 68, 1540-1544.
  • Merrifield K (2000) Plant-parasitic damage levels for Oregon nursery crops: A literature survey. Biology, host ranges, and damage levels of root-parasitic nematodes on Oregon nursery crops (Draft: 2000). https://bpp.oregonstate.edu/sites/agscid7/files/plant-parasitic-damage-levels-for-oregon-nursery-crops.pdf
  • Nyczepier A P & Halbrendt JM (1993) Nematode pests of deciduous fruit and nut trees. In Plant Parasitic Nematodes in Temperate Agriculture (eds Evans K, Trudgill DL & Webster JM). CAB International, Wallingford, England. pp. 381-425
  • PlantwisePlus Knowledge Bank (2023). Pratylenchus penetrans (nematode, northern root lesion). (accessed 26/Apr/2024). https://plantwiseplusknowledgebank.org/doi/full/10.1079/pwkb.species.43900
  • Pudasaini MP, Viaene N & Moens M (2006) Effect of marigold (Tagetes patula) on population dynamics of Pratylenchus penetrans in a field. Nematology 8, 477-84.
  • Schmitt DP & Sipes BS (2000) Plant-parasitic nematodes and their management. From “Plant Nutrient Management in Hawaii’s Soils, Approaches for Tropical and Subtropical Agriculture”. College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa.
  • Sharma GC, Thakur BS, Kashyap AS (2005) Impact of NPK on the nematode populations and yield of plum (Prunus salicina). SHS Acta Horticulturae, 696: VII International Symposium on Temperate Zone Fruits in the Tropics and Subtropics - Part Two. doi: 10.17660/ActaHortic.2005.696.77
  • Siddiqui IA, Sher SA & French AM (1973) Distribution of Plant Parasitic Nematodes in California. State of California Department of Food and Agriculture, Division of Plant Industry. 324p.
  • Söğüt MA, Devran Z, Arici ŞE, Şan B, Yildirim AN (2013) Host reactions of root lesion nematodes (Pratylenchus spp.) on the rootstocks of pome and stone. Turkish Journal of Entomology 37(2), 239-248.
  • Taning LM, Lippens L, Formesyn E, Wesemael W (2023) Impact of cover crops on population density of the root-lesion nematode Pratylenchus penetrans. Preprint DOI: https://doi.org/10.21203/rs.3.rs-3338686/v1
  • Townshend JL (1990) Growth of ‘Bartlett’ pear seedlings in response to number of root-lesions nematodes and temperature. HortSci, 25: 318-320
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