| Legend |
|---|
| Justification for qualification based on EPPO PM 4 Standards |
| Justification for disqualification |
| Additional or non-conclusive information |
| Standard text |
NAME OF THE ORGANISM: Phytophthora cinnamomi (PHYTCN)
GENERAL INFORMATION ON THE PEST
Name as submitted in the project specification (if different):
Pest category:
Chromista
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: Forest reproductive material sector, 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: Forest reproductive material sector, 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 (1993); France (1994); France/Corse (1994); Germany (2018); Greece (2019); Ireland (1993); Italy (2014); Italy/Sicilia (1998); Italy/Sardegna (2009); Netherlands (1993); Portugal (2023); Portugal/Azores (1994); Spain (2017); Spain/Islas Canárias (2017)
Conclusion:
Candidate
Justification (if necessary):
Data of the presence of this pest on the EU territory are available in EPPO Global Database (https://gd.eppo.int/). The pest is also reported in other European countries e.g. Poland, Romania (CABI, 2021), and Sweden (Matsiakh & Menkis, 2023).
HOST PLANT N°1: Castanea sativa (CSNSA) for the Forest reproductive material sector.
Origin of the listing:
New proposal
Plants for planting:
Plants intended for planting, except seeds
3 - Is the pest already listed in a PM4 standard on the concerned host plant?
No
Conclusion:
Evaluation continues
Justification (if necessary):
This plant species has no EPPO PM4 Standards, and the pest is not mentioned in other PM4 standards
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:
Phytophthora cinnamomi has an exceptionally wide host range, and has been found infecting more than 5000 plant species around the world. Of all Phytophthora spp., P. cinnamomi has the widest host range (Hardham & Blackman, 2018). Currently, it is the most important Phytophthora pathogen of forest trees; besides chestnut, P. cinnamomi causes root diseases in eucalyptus, oaks, pines and members of the Ericaceae family, as well as several crops (Robin et al., 2012). It is also one of the few pathogens capable of causing mortality of Taxus.
Chestnut is a major host of Phytophthora cinnamomi, together with P. cambivora it is the causal agent of ink disease in European chestnut. Since ink disease was first recorded in Portugal in 1838, it has become widespread in Europe on sweet chestnut (Castanea sativa), and in the USA on American chestnut (C. dentata) and other chestnut species (Vettraino et al., 2001). The more aggressive P. cinnamomi is widely prevalent in Spain, Portugal and France, especially in areas characterized by limited frost events during the winter, while P. cambivora is the main cause of the disease in Italy and Greece (Vannini et al., 2010). In southern Europe, P. cinnamomi attacks native chestnut trees (Castanea sativa) in Portugal, Spain and France and is spreading to the chestnut areas of Italy (Jung et al., 2013, cited from CABI, 2021). In the context of climate change, it is predicted an expansion of P. cinnamomi towards cold areas favored by warming, where water is not a limiting factor (Brasier & Scott, 1994; Serrano et al., 2022).
Long-range spread is likely to have been on (cryptically) infected nursery plants representing an important source of Phytophthora cinnamomi inoculum that can be disseminated widely through local and global trading (e.g., Kenerley & Bruck, 1983; Benson & Campbell, 1985; Davison et al., 2006; Brasier 2008; Trinidade et al., 2019), and still occurs in this way (Jung et al., 2016; Bregant et al., 2021).
The major pathway for spread of P. cinnamomi is by movement of soil and gravel infested with chlamydospores, or in contaminated potting mix of nursery stock (e.g., Batini, 1973; Colquhoun and Petersen, 1994, Davison et al., 2006). Phytophthora cinnamomi survives in dead plant material (survival influenced by soil matric potential) and can survive for long periods in this substrate (Shea et al., 1980). This saprophytic phase can allow an increase in the population of the pathogen. P. cinnamomi may also survive in the soil as mycelium, sporangia, zoospore cysts, chlamydospores and oospores and survival can be extended in the presence of an organic substrate (Weste & Vithanage, 1979). Phytophthora cinnamomi is known to survive as chlamydospores for as long as 6 years if soil moisture exceeds 3% (Zentmyer and Mircetich, 1966). Tillage practices and vehicle movement along the rural road network (Vannini et al. 2005; Martins et al. 2007), or e.g. movement of contaminated road gravel, have been associated with disease spread and resulted in initiation of new epidemics in Australia (Weste, 1975).
The pathogen can also slowly spread through root-to-root contact and more rapidly with water movement by the spread of zoospores in drainage, seepage and irrigation water (Kinal et al., 1993; MacDonald et al., 1994, Robin et al., 2012). However, spread with water occurs over relatively short distances in comparison to the spread that may occur via movement of infected plants or contaminated soil.
P. cinnamomi can infect all aerial parts of plants (trunks, branches, leaves and fruits) (SEF, 2023). True seeds are not known to carry P. cinnamomi (CABI, 2021).
In Galicia, the main chestnut-growing region in Spain, the existence of temperatures below 0 ºC for a certain period greatly restricts the dispersal of this pathogen. In such circumstances, plants for planting, produced mainly in the warmer coastal regions where P. cinnamomi is widespread, is the main pathway (Fernández et al., 2014; C. Iglesias & B. Miguez pers. com. 2024). In responses to the questionnaire, FR also indicated that several areas remain not or poorly infested depending on host presence and climatic conditions. Despite the fact that P. cinnamomi has now been introduced into many parts of the world, plants for panting remain one of the major pathways (along with soil) for introduction into the wider (e.g. forestry) environment.
Plants for planting may also allow the introduction of new genotypes or the other mating type into new areas.
Chestnut is a major host of Phytophthora cinnamomi, together with P. cambivora it is the causal agent of ink disease in European chestnut. Since ink disease was first recorded in Portugal in 1838, it has become widespread in Europe on sweet chestnut (Castanea sativa), and in the USA on American chestnut (C. dentata) and other chestnut species (Vettraino et al., 2001). The more aggressive P. cinnamomi is widely prevalent in Spain, Portugal and France, especially in areas characterized by limited frost events during the winter, while P. cambivora is the main cause of the disease in Italy and Greece (Vannini et al., 2010). In southern Europe, P. cinnamomi attacks native chestnut trees (Castanea sativa) in Portugal, Spain and France and is spreading to the chestnut areas of Italy (Jung et al., 2013, cited from CABI, 2021). In the context of climate change, it is predicted an expansion of P. cinnamomi towards cold areas favored by warming, where water is not a limiting factor (Brasier & Scott, 1994; Serrano et al., 2022).
Long-range spread is likely to have been on (cryptically) infected nursery plants representing an important source of Phytophthora cinnamomi inoculum that can be disseminated widely through local and global trading (e.g., Kenerley & Bruck, 1983; Benson & Campbell, 1985; Davison et al., 2006; Brasier 2008; Trinidade et al., 2019), and still occurs in this way (Jung et al., 2016; Bregant et al., 2021).
The major pathway for spread of P. cinnamomi is by movement of soil and gravel infested with chlamydospores, or in contaminated potting mix of nursery stock (e.g., Batini, 1973; Colquhoun and Petersen, 1994, Davison et al., 2006). Phytophthora cinnamomi survives in dead plant material (survival influenced by soil matric potential) and can survive for long periods in this substrate (Shea et al., 1980). This saprophytic phase can allow an increase in the population of the pathogen. P. cinnamomi may also survive in the soil as mycelium, sporangia, zoospore cysts, chlamydospores and oospores and survival can be extended in the presence of an organic substrate (Weste & Vithanage, 1979). Phytophthora cinnamomi is known to survive as chlamydospores for as long as 6 years if soil moisture exceeds 3% (Zentmyer and Mircetich, 1966). Tillage practices and vehicle movement along the rural road network (Vannini et al. 2005; Martins et al. 2007), or e.g. movement of contaminated road gravel, have been associated with disease spread and resulted in initiation of new epidemics in Australia (Weste, 1975).
The pathogen can also slowly spread through root-to-root contact and more rapidly with water movement by the spread of zoospores in drainage, seepage and irrigation water (Kinal et al., 1993; MacDonald et al., 1994, Robin et al., 2012). However, spread with water occurs over relatively short distances in comparison to the spread that may occur via movement of infected plants or contaminated soil.
P. cinnamomi can infect all aerial parts of plants (trunks, branches, leaves and fruits) (SEF, 2023). True seeds are not known to carry P. cinnamomi (CABI, 2021).
In Galicia, the main chestnut-growing region in Spain, the existence of temperatures below 0 ºC for a certain period greatly restricts the dispersal of this pathogen. In such circumstances, plants for planting, produced mainly in the warmer coastal regions where P. cinnamomi is widespread, is the main pathway (Fernández et al., 2014; C. Iglesias & B. Miguez pers. com. 2024). In responses to the questionnaire, FR also indicated that several areas remain not or poorly infested depending on host presence and climatic conditions. Despite the fact that P. cinnamomi has now been introduced into many parts of the world, plants for panting remain one of the major pathways (along with soil) for introduction into the wider (e.g. forestry) environment.
Plants for planting may also allow the introduction of new genotypes or the other mating type into new areas.
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Yes
Justification:
Ink disease is one of the most destructive diseases affecting Castanea sativa. This pathogen is the main biological constraint to chestnut production in several European countries (Vanini and Vettraino, 2001). It causes root and collar rot of adult trees and of seedlings in nurseries, plantations and forests. Symptoms of the disease on adult trees include chlorotic leaves reduced in size, thinning of the crown, and immature husks remaining on the tree after leaf-fall. Flame shaped dark necroses are evident on the collar of the tree after debarking. It is the large roots that are mainly infected. They produce a black exudate that stains the surrounding soil, especially during spring and fall. On young trees with smooth bark, the necroses are visible without debarking as depressed, slightly cracked areas at the base of the stem. Infected seedlings in nurseries or plantations undergo a rapid or gradual wilting of the leaves. In the root system, there is extensive necrosis of the tap root that extends to the lateral roots and up the stem for some centimeters. P. cambivora and P. cinnamomi can kill adult trees in one to three years (Vannini & Vettraino, 2001).
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:
Impact clear.
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:
It is advisable to use of pathogen-free planting material.
Disease prevention is very important, especially in nurseries:
- Seedlings should be grown in pathogen-free soil and any residual roots remaining in the soil should be eliminated to prevent any carry-over of inoculum before new plants are grown in the same soil.
- Soil should be well drained and water stagnation prevented, because excess soil moisture favors the fungus.
- Seedlings should not be watered with river water originating from infected areas.
- When using potting mixes and containers, hygiene is critical.
Contrary to plants for fruit production, grafting on resistant rootstocks is not used for forestry purpose (too costly).
Although eradication is not considered possible in the wider environment (e.g. forests, plantations), it could be possible in nurseries.
Disease prevention is very important, especially in nurseries:
- Seedlings should be grown in pathogen-free soil and any residual roots remaining in the soil should be eliminated to prevent any carry-over of inoculum before new plants are grown in the same soil.
- Soil should be well drained and water stagnation prevented, because excess soil moisture favors the fungus.
- Seedlings should not be watered with river water originating from infected areas.
- When using potting mixes and containers, hygiene is critical.
Contrary to plants for fruit production, grafting on resistant rootstocks is not used for forestry purpose (too costly).
Although eradication is not considered possible in the wider environment (e.g. forests, plantations), it could be possible in nurseries.
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 the following measures.
Justification (if necessary):
Remark: The EU Forestry Marketing Directive (Council Directive 1999/105/EC) requires for basic ‘selected’ that ‘Trees in stands must in general be free from attacks by damaging organisms and show resistance to the adverse climatic and site conditions, except for damage by pollution, in the place where they are growing.’
9 - Risk management measures:
Is there a need to change the Risk management measure:
Yes
Proposed Risk management measure:
(A) Derived from mother plants which have been inspected, and found free from Phytophthora cinnamomi.
AND
(B) (a) Plants produced in areas known to be free from Phytophthora cinnamomi;
or
(b) Site of production found free from Phytophthora cinnamomi over the last complete growing season at appropriate times by inspection of the foliage;
or
(c)(i) Inspection of the site of production at appropriate times over the last complete growing season, and (ii) sampling of roots and soil at the basis of a representative number of plants in the site of production, and (iii) any plants found to be infected and plants in a surrounding zone of at least 1 m radius should be marked, excluded from marketing, and then destroyed (the distance may be increased depending on the growing system), and (iv) Pathogen-free soil should be used.
Additional measures e.g. for Basic material could include:
o Recording of cropping and soil borne disease history of fields;
o Rest period from host plants between findings of the pest and next planting;
AND
(B) (a) Plants produced in areas known to be free from Phytophthora cinnamomi;
or
(b) Site of production found free from Phytophthora cinnamomi over the last complete growing season at appropriate times by inspection of the foliage;
or
(c)(i) Inspection of the site of production at appropriate times over the last complete growing season, and (ii) sampling of roots and soil at the basis of a representative number of plants in the site of production, and (iii) any plants found to be infected and plants in a surrounding zone of at least 1 m radius should be marked, excluded from marketing, and then destroyed (the distance may be increased depending on the growing system), and (iv) Pathogen-free soil should be used.
Additional measures e.g. for Basic material could include:
o Recording of cropping and soil borne disease history of fields;
o Rest period from host plants between findings of the pest and next planting;
Justification (if necessary):
Trindade et al. (2019) stated that commonly plants in nurseries may not exhibit infection symptoms. However, systematic testing of the mother plants was not recommended based on a cost/benefit analysis.
Depending on how the plants are watered, the minimum buffer distance of 1m where plants are removed may need to be increased. This distance is to cover risk with water and root contacts.
Pathogen-free soil: soil may be tested, steaming can be used etc.
Testing should be performed according to EPPO Standard PM 7/26(1) Phytophthora cinnamomi
Depending on how the plants are watered, the minimum buffer distance of 1m where plants are removed may need to be increased. This distance is to cover risk with water and root contacts.
Pathogen-free soil: soil may be tested, steaming can be used etc.
Testing should be performed according to EPPO Standard PM 7/26(1) Phytophthora cinnamomi
REFERENCES:
- Batini F (1973) Jarrah dieback - a disease of the Jarrah Forest of Western Australia. Bulletin 84, Forests Department Perth, Western Australia.
- Benson DM & Campbell CL (1985) Spatial pattern of Phytophthora root rot and dieback of azalea in container-grown nursery stock. Plant Disease 69(12), 1049-1054.
- Brasier CM (2008) The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathology 57, 792-808. Doi: 10.1111/j.1365-3059.2008.01886.x
- Brasier CM & Scott JK (1994) European oak declines and global warming: a theoretical assessment with special reference to the activity of Phytophthora cinnamomi. EPPO Bulletin 24(1), 221-232. https://doi.org/10.1111/j.1365-2338.1994.tb01063.x
- Bregant C, Mulas AA, Rossetto G, Deidda A, Maddau L, Piras G & Linaldeddu BT (2021) Phytophthora mediterranea sp. nov., a new species closely related to Phytophthora cinnamomi from nursery plants of Myrtus communis in Italy. Forests 12, 682. https://doi.org/10.3390/f12060682
- Breisch H & Hennion B (2004) Chestnut rootstock: towards more resistance. Infos-Ctifl 198, 35-38.
- CABI (Davison E) (2021) Phytophthora cinnamomi (Phytophthora dieback) (last updated 3/May/2024; accessed 14/May/2024). https://www.cabidigitallibrary.org/doi/10.1079/cabicompendium.40957
- Colquhoun IJ & Petersen AE (1994) The impact of disease on mining. Journal of the Royal Society of Western Australia 77, 151-158.
- Davison EM, Drenth A, Kumar S, Mack S, Mackie AE & McKirdy S (2006) Pathogens associated with nursery plants imported into Western Australia. Australasian Plant Pathology 35(4), 473-475. http://www.publish.csiro.au/nid/39.htm
- Fernandes P, Amaral A, Colavolpe B, Balonas D, Serra M, Pereira A & Costa RL (2020) Propagation of new chestnut rootstocks with improved resistance to Phytophthora cinnamomi – New cast rootstocks. Silva Lusitana 28(1), 15-29.
- Hardham R & Blackman LM (2018) Pathogen Profile Update: Phytophthora cinnamomi. Molecular plant pathology 19(2), 260-285. https://doi.org/10.1111/mpp.12568
- Harshani HS, Tsakalos JL, Mansfield, TM, McComb J, Burgess TI, St. J. Hardy GE (2023) Impact of Phytophthora cinnamomi on the taxonomic and functional diversity of forest plants in a mediterranean-type biodiversity hotspot. Journal of Vegetation Science 34, e13218, 13 pp. https://doi.org/10.1111/jvs.13218
- Jung T, Vettraino AM, Cech T & Vannini A (2013) The impact of invasive Phytophthora species on European forests. In Phytophthora: a global perspective (ed Lamour, K). Wallingford, UK: CABI, 146-158.
- Jung T, Orlikowski L, Henricot B, Abad-Campos P, Aday AG, Aguín Casal O, Bakonyi J, Cacciola SO, Cech T, Chavarriaga D, Corcobado T, Cravador A, Decourcelle T, Denton G, Diamandis S, Doğmuş-Lehtijärvi HT, Franceschini A, Ginetti B, Green S, Glavendekíc M, Hantula J, Hartmann G, Herrero M, Ivic D, Horta Jung M, Lilja A, Keca N, Kramarets V, Lyubenova A, Machado H, Magnano di San Lio G, Mansilla Vázquez PJ, Marçais B, Matsiakh I, Milenkovic I, Moricca S, Nagy ZA, Nechwatal J., Olsson C, Oszako T, Pane A, Paplomatas EJ, Pintos Varela C, Prospero S, Rial Martínez C, Rigling D, Robin C, Rytkönen A, Sánchez ME, Sanz Ros AV, Scanu B, Schlenzig A, Schumacher J, Slavov S, Solla A, Sousa E, Stenlid J, Talgø V, Tomic Z, Tsopelas P, Vannini A, Vettraino AM, Wenneker M, Woodward S & Peréz-Sierra A (2016) Widespread Phytophthora infestations in European nurseries put forest, semi‐natural and horticultural ecosystems at high risk of Phytophthora diseases. Forest Pathology, 46(2), 134-16. https://doi.org/10.1111/efp.12239.
- Jung T, Jung MH, Cacciola SO, Cech T, Bakonyi J, Seress D, ... & Scanu B (2017) Multiple new cryptic pathogenic Phytophthora species from Fagaceae forests in Austria, Italy and Portugal. IMA fungus, 8, 219-244.
- Jung T, Pérez-Sierra A, Durán A, Jung MH, Balci Y & Scanu B (2018) Canker and decline diseases caused by soil- and airborne Phytophthora species in forests and woodlands. Persoonia - Molecular Phylogeny and Evolution of Fungi, Volume 40, pp. 182-220(39)
- Kenerley CM & Bruck RI (1983) Overwintering and survival of Phytophthora cinnamomi in Fraser fir and cover cropped nursery beds in North Carolina. Phytopathology. 73 (12), 1643-1647. DOI:10.1094/Phyto-73-1643
- Kinal J, Shearer BL & Fairman RG (1993) Dispersal of Phytophthora cinnamomi through lateritic soil by laterally flowing subsurface water. Plant Disease 77(11), 1085-1090.
- MacDonald JD, Ali-Shtayeh MS, Kabashima J & Stites J (1994) Occurrence of Phytophthora species in recirculated nursery irrigation effluents. Plant Disease 78(6), 607-611.
- Martins L, Castro J, Macedo W, Marques C, Abreu C (2007) Assessment of the spread of chestnut ink disease using remote sensing and geostatistical methods. European Journal of Plant Pathology 119, 159-164. DOI 10.1007/s10658-007-9155-3
- Matsiakh I & Menkis A (2023) An Overview of Phytophthora Species on Woody Plants in Sweden and Other Nordic Countries. Microorganisms 11(5), 1309. https://doi.org/10.3390/microorganisms11051309
- Robin C, Smith I & Hansen EM (2012) Phythophthora cinnamomi. Forest Phytophthoras. doi: 10.5399/osu/fp.2.1.3041.
- Santos C, Machado H, Correia I, Gomes F, Gomes-Laranjo J & Costa R (2014) Phenotyping Castanea hybrids for Phytophthora cinnamomic resistance. Plant Pathology 64, 901–910 Doi: 10.1111/ppa.12313
- Sena K, Crocker E, Vincelli P & Barton C (2018) Phytophthora cinnamomi as a driver of forest change: Implications for conservation and management. Forest Ecology and Management 409, 799-807. https://doi.org/10.1016/j.foreco.2017.12.022;
- Serrano MS, Romero MA, Homet P & Gomez-Aparicio L (2022) Climate change impact on the population dynamics of exotic pathogens: The case of the worldwide pathogen Phytophthora cinnamomi. Agricultural and Forest Meteorology 322, 109002. Available at https://doi.org/10.1016/j.agrformet.2022.109002.
- Shea SR, Gillen KJ & Leppard WI (1980) Seasonal variation in population levels of Phytophthora cinnamomi Rands in soil in diseased, freely-drained Eucalyptus marginata sites in the northern Jarrah forest of South-Western Australia. Protection Ecology 2(2), 135-156.
- Smith PM (1988) Phytophthora cinnamomi. In European Handbook of Plant Diseases (eds Smith IM, Dunez J, Lelliott RA, Phillips DH &Archer SA). Oxford, UK: Blackwell Scientific Publications, 213-215.
- Trindade M, Costa e Silva F, Moreira AC, Gonçalves MdC, David TS, Cardillo E, Rodríguez-Molina MC, Silva CS, Ribeiro, Dina D & Santos G (2019) Prevenção e Gestão de Fitóftora em Viveiros Florestais. Ed: INIAV. Available at https://www.iniav.pt/images/publicacoes/livros-manuais/fitoftora_viveiros.pdf.
- Vannini A & Vettraino AM (2001) Ink disease in chestnuts: impact on the European chestnut. Forest Snow Landscape Research 76(3), 345–350.
- Vannini A, Vettraino AM, Fabi A, Montaghi A, Valentini R & Belli C (2005) Monitoring Ink disease of chestnut with the airborne multispectral system A.S.P.I.S. Acta Horticulturae 693, 529–533.
- Vettraino AM, Morel O, Perlerou C, Robin C, Diamandis S & Vannini A (2005) Occurrence and distribution of Phytophthora species in European chestnut stands, and their association with Ink Disease and crown decline. European Journal of Plant Pathology 111, 169-180.
- Weste G (1975) The distribution of Phytophthora cinnamomi within the National Park, Wilson's Promontory, Victoria. Australian Journal of Botany 23(1), 67-76
- Zentmyer GA & Mircetich SM (1966) Saprophytism and persistence in soil by Phytophthora cinnamomi. Phytopathology 56, 710-712.
HOST PLANT N°2: Castanea sativa (CSNSA) 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, except seeds
3 - Is the pest already listed in a PM4 standard on the concerned host plant?
No
Conclusion:
Evaluation continues
Justification (if necessary):
This plant species has no EPPO PM4 Standards, and the pest is not mentioned in other PM4 standards
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:
Phytophthora cinnamomi has an exceptionally wide host range, and has been found infecting more than 5000 plant species around the world. Of all Phytophthora spp., P. cinnamomi has the widest host range (Hardham & Blackman, 2018). Currently, it is the most important Phytophthora pathogen of forest trees; besides chestnut, P. cinnamomi causes root diseases in eucalyptus, oaks, pines and members of the Ericaceae family, as well as several crops (Robin et al., 2012). It is also one of the few pathogens capable of causing mortality of Taxus.
Chestnut is a major host of Phytophthora cinnamomi, together with P. cambivora it is the causal agent of ink disease in European chestnut. Since ink disease was first recorded in Portugal in 1838, it has become widespread in Europe on sweet chestnut (Castanea sativa), and in the USA on American chestnut (C. dentata) and other chestnut species (Vettraino et al., 2001). The more aggressive P. cinnamomi is widely prevalent in Spain, Portugal and France, especially in areas characterized by limited frost events during the winter, while P. cambivora is the main cause of the disease in Italy and Greece (Vannini et al., 2010). In southern Europe, P. cinnamomi attacks native chestnut trees (Castanea sativa) in Portugal, Spain and France and is spreading to the chestnut areas of Italy (Jung et al., 2013, cited from CABI, 2021). In the context of climate change, it is predicted an expansion of P. cinnamomi towards cold areas favored by warming, where water is not a limiting factor (Brasier & Scott, 1994; Serrano et al., 2022).
Long-range spread is likely to have been on (cryptically) infected nursery plants representing an important source of Phytophthora cinnamomi inoculum that can be disseminated widely through local and global trading (e.g., Kenerley & Bruck, 1983; Benson & Campbell, 1985; Davison et al., 2006; Brasier 2008; Trinidade et al., 2019), and still occurs in this way (Jung et al., 2016; Bregant et al., 2021).
The major pathway for spread of P. cinnamomi is by movement of soil and gravel infested with chlamydospores, or in contaminated potting mix of nursery stock (e.g., Batini, 1973; Colquhoun and Petersen, 1994, Davison et al., 2006). Phytophthora cinnamomi survives in dead plant material (survival influenced by soil matric potential) and can survive for long periods in this substrate (Shea et al., 1980). This saprophytic phase can allow an increase in the population of the pathogen. P. cinnamomi may also survive in the soil as mycelium, sporangia, zoospore cysts, chlamydospores and oospores and survival can be extended in the presence of an organic substrate (Weste & Vithanage, 1979). Phytophthora cinnamomi is known to survive as chlamydospores for as long as 6 years if soil moisture exceeds 3% (Zentmyer and Mircetich, 1966). Tillage practices and vehicle movement along the rural road network (Vannini et al. 2005; Martins et al. 2007), or e.g. movement of contaminated road gravel, have been associated with disease spread and resulted in initiation of new epidemics in Australia (Weste, 1975).
The pathogen can also slowly spread through root-to-root contact and more rapidly with water movement by the spread of zoospores in drainage, seepage and irrigation water (Kinal et al., 1993; MacDonald et al., 1994, Robin et al., 2012). However, spread with water occurs over relatively short distances in comparison to the spread that may occur via movement of infected plants or contaminated soil.
P. cinnamomi can infect all aerial parts of plants (trunks, branches, leaves and fruits) (SEF, 2023). True seeds are not known to carry P. cinnamomi (CABI, 2021).
In Galicia, the main chestnut-growing region in Spain, the existence of temperatures below 0 ºC for a certain period greatly restricts the dispersal of this pathogen. In such circumstances, plants for planting, produced mainly in the warmer coastal regions where P. cinnamomi is widespread, is the main pathway (Fernández et al., 2014; C. Iglesias & B. Miguez pers. com. 2024). In responses to the questionnaire, FR also indicated that several areas remain not or poorly infested depending on host presence and climatic conditions.
Plants for planting may also allow the introduction of new genotypes or the other mating type into new areas.
Chestnut is a major host of Phytophthora cinnamomi, together with P. cambivora it is the causal agent of ink disease in European chestnut. Since ink disease was first recorded in Portugal in 1838, it has become widespread in Europe on sweet chestnut (Castanea sativa), and in the USA on American chestnut (C. dentata) and other chestnut species (Vettraino et al., 2001). The more aggressive P. cinnamomi is widely prevalent in Spain, Portugal and France, especially in areas characterized by limited frost events during the winter, while P. cambivora is the main cause of the disease in Italy and Greece (Vannini et al., 2010). In southern Europe, P. cinnamomi attacks native chestnut trees (Castanea sativa) in Portugal, Spain and France and is spreading to the chestnut areas of Italy (Jung et al., 2013, cited from CABI, 2021). In the context of climate change, it is predicted an expansion of P. cinnamomi towards cold areas favored by warming, where water is not a limiting factor (Brasier & Scott, 1994; Serrano et al., 2022).
Long-range spread is likely to have been on (cryptically) infected nursery plants representing an important source of Phytophthora cinnamomi inoculum that can be disseminated widely through local and global trading (e.g., Kenerley & Bruck, 1983; Benson & Campbell, 1985; Davison et al., 2006; Brasier 2008; Trinidade et al., 2019), and still occurs in this way (Jung et al., 2016; Bregant et al., 2021).
The major pathway for spread of P. cinnamomi is by movement of soil and gravel infested with chlamydospores, or in contaminated potting mix of nursery stock (e.g., Batini, 1973; Colquhoun and Petersen, 1994, Davison et al., 2006). Phytophthora cinnamomi survives in dead plant material (survival influenced by soil matric potential) and can survive for long periods in this substrate (Shea et al., 1980). This saprophytic phase can allow an increase in the population of the pathogen. P. cinnamomi may also survive in the soil as mycelium, sporangia, zoospore cysts, chlamydospores and oospores and survival can be extended in the presence of an organic substrate (Weste & Vithanage, 1979). Phytophthora cinnamomi is known to survive as chlamydospores for as long as 6 years if soil moisture exceeds 3% (Zentmyer and Mircetich, 1966). Tillage practices and vehicle movement along the rural road network (Vannini et al. 2005; Martins et al. 2007), or e.g. movement of contaminated road gravel, have been associated with disease spread and resulted in initiation of new epidemics in Australia (Weste, 1975).
The pathogen can also slowly spread through root-to-root contact and more rapidly with water movement by the spread of zoospores in drainage, seepage and irrigation water (Kinal et al., 1993; MacDonald et al., 1994, Robin et al., 2012). However, spread with water occurs over relatively short distances in comparison to the spread that may occur via movement of infected plants or contaminated soil.
P. cinnamomi can infect all aerial parts of plants (trunks, branches, leaves and fruits) (SEF, 2023). True seeds are not known to carry P. cinnamomi (CABI, 2021).
In Galicia, the main chestnut-growing region in Spain, the existence of temperatures below 0 ºC for a certain period greatly restricts the dispersal of this pathogen. In such circumstances, plants for planting, produced mainly in the warmer coastal regions where P. cinnamomi is widespread, is the main pathway (Fernández et al., 2014; C. Iglesias & B. Miguez pers. com. 2024). In responses to the questionnaire, FR also indicated that several areas remain not or poorly infested depending on host presence and climatic conditions.
Plants for planting may also allow the introduction of new genotypes or the other mating type into new areas.
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Yes
Justification:
Ink disease is one of the most destructive diseases affecting Castanea sativa. This pathogen is the main biological constraint to chestnut production in several European countries (Vanini and Vettraino, 2001). It causes root and collar rot of adult trees and of seedlings in nurseries, plantations and forests. Symptoms of the disease on adult trees include chlorotic leaves reduced in size, thinning of the crown, and immature husks remaining on the tree after leaf-fall. Flame shaped dark necroses are evident on the collar of the tree after debarking. It is the large roots that are mainly infected. They produce a black exudate that stains the surrounding soil, especially during spring and fall. On young trees with smooth bark, the necroses are visible without debarking as depressed, slightly cracked areas at the base of the stem. Infected seedlings in nurseries or plantations undergo a rapid or gradual wilting of the leaves. In the root system, there is extensive necrosis of the tap root that extends to the lateral roots and up the stem for some centimeters. P. cambivora and P. cinnamomic can kill adult trees in one to three years (Vannini & Vettraino, 2001).
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:
Impact clear.
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:
The main prevention measures are the planting of resistant chestnut trees obtained by controlled hybridisation of Castanea sativa with Castanea mollissima and Castanea crenata (MAPA, 2018) and, in cold climate regions, the use of pathogen-free propagating plant material (C. Iglesias & B. Miguez pers. com. 2024):
- Disease prevention is very important, especially in nurseries. Seedlings should be grown in pathogen-free soil and any residual roots remaining in the soil should be eliminated to prevent any carry-over of inoculum before new plants are grown in the same soil. Soil should be well drained and water stagnation prevented, because excess soil moisture favors the fungus. Seedlings should not be watered with river water originating from infected areas. It is advisable to use of pathogen-free planting material, potting mixes and containers.
- Resistant rootstocks: In chestnut, high levels of resistance have been reported for Asiatic chestnut (Castanea crenata) and the hybrids C. sativa x C. crenata. Studies on the resistance of these hybrids to P. cambivora and Phytophthora cinnamomi are continuing and some offer interesting perspectives with regard to their graft compatibility with cultivated varieties and to productivity (Santos et al., 2014, Fernandes et al., 2020). Hybridisation with Castanea mollissima also provides resistance.
- Disease prevention is very important, especially in nurseries. Seedlings should be grown in pathogen-free soil and any residual roots remaining in the soil should be eliminated to prevent any carry-over of inoculum before new plants are grown in the same soil. Soil should be well drained and water stagnation prevented, because excess soil moisture favors the fungus. Seedlings should not be watered with river water originating from infected areas. It is advisable to use of pathogen-free planting material, potting mixes and containers.
- Resistant rootstocks: In chestnut, high levels of resistance have been reported for Asiatic chestnut (Castanea crenata) and the hybrids C. sativa x C. crenata. Studies on the resistance of these hybrids to P. cambivora and Phytophthora cinnamomi are continuing and some offer interesting perspectives with regard to their graft compatibility with cultivated varieties and to productivity (Santos et al., 2014, Fernandes et al., 2020). Hybridisation with Castanea mollissima also provides resistance.
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:
No
Proposed Risk management measure:
REFERENCES:
- Batini F (1973) Jarrah dieback - a disease of the Jarrah Forest of Western Australia. Bulletin 84, Forests Department Perth, Western Australia.
- Benson DM & Campbell CL (1985) Spatial pattern of Phytophthora root rot and dieback of azalea in container-grown nursery stock. Plant Disease 69(12), 1049-1054.
- Brasier CM (2008) The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathology 57, 792-808. Doi: 10.1111/j.1365-3059.2008.01886.x
- Brasier CM & Scott JK (1994) European oak declines and global warming: a theoretical assessment with special reference to the activity of Phytophthora cinnamomi. EPPO Bulletin 24(1), 221-232. https://doi.org/10.1111/j.1365-2338.1994.tb01063.x
- Bregant C, Mulas AA, Rossetto G, Deidda A, Maddau L, Piras G & Linaldeddu BT (2021) Phytophthora mediterranea sp. nov., a new species closely related to Phytophthora cinnamomi from nursery plants of Myrtus communis in Italy. Forests 12, 682. https://doi.org/10.3390/f12060682
- Breisch H & Hennion B (2004). Chestnut rootstock: towards more resistance. Infos-Ctifl 198, 35-38.
- CABI (Davison E) (2021) Phytophthora cinnamomi (Phytophthora dieback) (last updated 3/May/2024; accessed 14/May/2024). https://www.cabidigitallibrary.org/doi/10.1079/cabicompendium.40957
- Colquhoun IJ & Petersen AE (1994). The impact of disease on mining. Journal of the Royal Society of Western Australia 77, 151-158.
- Davison EM, Drenth A, Kumar S, Mack S, Mackie AE & McKirdy S (2006). Pathogens associated with nursery plants imported into Western Australia. Australasian Plant Pathology 35(4), 473-475. http://www.publish.csiro.au/nid/39.htm
- Fernandes P, Amaral A, Colavolpe B, Balonas D, Serra M, Pereira A & Costa RL (2020). Propagation of new chestnut rootstocks with improved resistance to Phytophthora cinnamomi – New cast rootstocks. Silva Lusitana 28(1), 15-29.
- Fernandez J, Míguez B, Miranda ME, Fernández J, Barciela S & Martínez R (2014) O material vexetal na plantación de soutos. In “Guía de cultivo do castiñeiro para a produción de castaña”. Consellería do Medio Rural e do Mar. Xunta de Galicia.
- Hardham R & Blackman LM (2018) Pathogen Profile Update: Phytophthora cinnamomi. Molecular plant pathology 19(2), 260-285. https://doi.org/10.1111/mpp.12568
- Harshani HS, Tsakalos JL, Mansfield, TM, McComb J, Burgess TI, St. J. Hardy GE (2023) Impact of Phytophthora cinnamomi on the taxonomic and functional diversity of forest plants in a mediterranean-type biodiversity hotspot. Journal of Vegetation Science 34, e13218, 13 pp. https://doi.org/10.1111/jvs.13218
- Jung T, Vettraino AM, Cech T & Vannini A (2013) The impact of invasive Phytophthora species on European forests. In Phytophthora: a global perspective (ed Lamour, K). Wallingford, UK: CABI, 146-158.
- Jung T, Orlikowski L, Henricot B, Abad-Campos P, Aday AG, Aguín Casal O, Bakonyi J, Cacciola SO, Cech T, Chavarriaga D, Corcobado T, Cravador A, Decourcelle T, Denton G, Diamandis S, Doğmuş-Lehtijärvi HT, Franceschini A, Ginetti B, Green S, Glavendekíc M, Hantula J, Hartmann G, Herrero M, Ivic D, Horta Jung M, Lilja A, Keca N, Kramarets V, Lyubenova A, Machado H, Magnano di San Lio G, Mansilla Vázquez PJ, Marçais B, Matsiakh I, Milenkovic I, Moricca S, Nagy ZA, Nechwatal J., Olsson C, Oszako T, Pane
- Matsiakh I & Menkis A (2023) An Overview of Phytophthora Species on Woody Plants in Sweden and Other Nordic Countries. Microorganisms 11(5), 1309. https://doi.org/10.3390/microorganisms11051309 A, Paplomatas EJ, Pintos Varela C, Prospero S, Rial Martínez C, Rigling D, Robin C, Rytkönen A, Sánchez ME, Sanz Ros AV, Scanu B, Schlenzig A, Schumacher J, Slavov S, Solla A, Sousa E, Stenlid J, Talgø V, Tomic Z, Tsopelas P, Vannini A, Vettraino AM, Wenneker M, Woodward S & Peréz-Sierra A (2016) Widespread Phytophthora infestations in European nurseries put forest, semi‐natural and horticultural ecosystems at high risk of Phytophthora diseases. Forest Pathology, 46(2), 134-16. https://doi.org/10.1111/efp.12239.
- Jung T, Jung MH, Cacciola SO, Cech T, Bakonyi J, Seress D, ... & Scanu B (2017) Multiple new cryptic pathogenic Phytophthora species from Fagaceae forests in Austria, Italy and Portugal. IMA fungus, 8, 219-244.
- Jung T, Pérez-Sierra A, Durán A, Jung MH, Balci Y & Scanu B (2018) Canker and decline diseases caused by soil- and airborne Phytophthora species in forests and woodlands. Persoonia - Molecular Phylogeny and Evolution of Fungi, Volume 40, pp. 182-220(39)
- Kenerley C M, Bruck R I, 1983. Overwintering and survival of Phytophthora cinnamomi in Fraser fir and cover cropped nursery beds in North Carolina. Phytopathology. 73 (12), 1643-1647. DOI:10.1094/Phyto-73-1643
- Kinal J, Shearer BL & Fairman RG (1993). Dispersal of Phytophthora cinnamomi through lateritic soil by laterally flowing subsurface water. Plant Disease 77(11), 1085-1090.
- MacDonald JD, Ali-Shtayeh MS, Kabashima J & Stites J (1994). Occurrence of Phytophthora species in recirculated nursery irrigation effluents. Plant Disease 78(6), 607-611.
- MAPA (2018) Guía de Gestión Integrada de Plagas: castaño. Ministerio de Agricultura, Pesca y Alimentación. https://www.mapa.gob.es/es/agricultura/temas/sanidad-vegetal/productos-fitosanitarios/guias-gestion-plagas/frutales/default.aspx
- Martins L, Castro J, Macedo W, Marques C, Abreu C (2007) Assessment of the spread of chestnut ink disease using remote sensing and geostatistical methods. European Journal of Plant Pathology 119, 159-164. DOI 10.1007/s10658-007-9155-3
- Robin C, Smith I & Hansen EM (2012). Phythophthora cinnamomi. Forest Phytophthoras. doi: 10.5399/osu/fp.2.1.3041.
- Santos C, Machado H, Correia I, Gomes F, Gomes-Laranjo J & Costa R (2014) Phenotyping Castanea hybrids for Phytophthora cinnamomic resistance. Plant Pathology 64, 901–910 Doi: 10.1111/ppa.12313
- SEF (2023) Phytophthora cinnamomi Rands. In “Patógenos de plantas descritos en España”. Sociedad Española de Fitopatología. https://sef.es/patogeno/phytophthora-cinnamomi-rands (accessed: 07/22/2024).
- Sena K, Crocker E, Vincelli P & Barton C (2018) Phytophthora cinnamomi as a driver of forest change: Implications for conservation and management. Forest Ecology and Management 409, 799-807. https://doi.org/10.1016/j.foreco.2017.12.022;
- Serrano MS, Romero MA, Homet P & Gomez-Aparicio L (2022) Climate change impact on the population dynamics of exotic pathogens: The case of the worldwide pathogen Phytophthora cinnamomi. Agricultural and Forest Meteorology 322, 109002. Available at https://doi.org/10.1016/j.agrformet.2022.109002.
- Shea SR, Gillen KJ & Leppard WI (1980). Seasonal variation in population levels of Phytophthora cinnamomi Rands in soil in diseased, freely-drained Eucalyptus marginata sites in the northern Jarrah forest of South-Western Australia. Protection Ecology 2(2), 135-156.
- Smith PM (1988) Phytophthora cinnamomi. In European Handbook of Plant Diseases (eds Smith IM, Dunez J, Lelliott RA, Phillips DH &Archer SA). Oxford, UK: Blackwell Scientific Publications, 213-215.
- Trindade M, Costa e Silva F, Moreira AC, Gonçalves MdC, David TS, Cardillo E, Rodríguez-Molina MC, Silva CS, Ribeiro, Dina D & Santos G (2019) Prevenção e Gestão de Fitóftora em Viveiros Florestais. Ed: INIAV. Available at https://www.iniav.pt/images/publicacoes/livros-manuais/fitoftora_viveiros.pdf.
- Vannini A & Vettraino AM (2001) Ink disease in chestnuts: impact on the European chestnut. Forest Snow Landscape Research 76(3), 345–350.
- Vannini A, Vettraino AM, Fabi A, Montaghi A, Valentini R & Belli C (2005) Monitoring Ink disease of chestnut with the airborne multispectral system A.S.P.I.S. Acta Horticulturae 693, 529–533.
- Vettraino AM, Morel O, Perlerou C, Robin C, Diamandis S & Vannini A (2005) Occurrence and distribution of Phytophthora species in European chestnut stands, and their association with Ink Disease and crown decline. European Journal of Plant Pathology 111, 169-180.
- Weste G (1975). The distribution of Phytophthora cinnamomi within the National Park, Wilson's Promontory, Victoria. Australian Journal of Botany 23(1), 67-76
- Zentmyer GA & Mircetich SM(1966) Saprophytism and persistence in soil by Phytophthora cinnamomi. Phytopathology 56, 710-712.
