| Legend |
|---|
| Justification for qualification based on EPPO PM 4 Standards |
| Justification for disqualification |
| Additional or non-conclusive information |
| Standard text |
NAME OF THE ORGANISM: Phytoptus avellanae sensu lato (ERPHAV)
GENERAL INFORMATION ON THE PEST
Name as submitted in the project specification (if different):
Phytoptus avellanae
Pest category:
Acari
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):
The big bud mite, P. avellanae, includes two cryptic species based on phylogenetic analyses of mitochondrial cytochrome oxidase subunit I (COI) DNA and the nuclear D2 region of 28S rDNA sequences (Cvrković et al., 2016). The first one, P. avellanae sensu stricto, lives in hazelnut buds, causes their increase in size (big buds) and drying. The second one is vagrant and should be named after its morphological characterization and more exhaustive study of bio-ecology (Özman & Toros, 1997a; de Lillo et al., 2018). The impact of the second species on hazelnut production needs to be ascertained (de Lillo et al., 2018).
Considering complexity of the taxonomic status, the Fruit SEWG recommended to use the name P. avellanae sensu lato, covering both gall-living and vagrant taxa.
Considering complexity of the taxonomic status, the Fruit SEWG recommended to use the name P. avellanae sensu lato, covering both gall-living and vagrant taxa.
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):
-
Conclusion:
Candidate
Justification (if necessary):
Phytoptus avellanae has been reported in Austria, Bulgaria, Croatia, Cyprus, Czech Republic, Denmark, Estland, Finland, France, Germany, Greece, Hungaria, Italy, Latvia, Lithuania, Luxemburg, Netherlands, Poland, Portugal, Slovenia and Spain (De Jong et al., 2016; Pesi, 2024)
HOST PLANT N°1: Corylus avellana (CYLAV) for the Fruits (including hops) sector.
Origin of the listing:
Commission Implementing Directive (EU) 2014/98/EU and Commission Implementing Regulation (EU) 2019/2072
Plants for planting:
Plants intended for planting
3 - Is the pest already listed in a PM4 standard on the concerned host plant?
Yes
Conclusion:
Evaluation continues
Justification (if necessary):
Inspection for 'Phytoptus avellanae' is recommended in EPPO Standard PM 4-31 Certification scheme for hazelnut. Any plant found to be infected should be recorded and immediately removed. In the responses to the questionnaire, DE and PL supported deregulation in the EU. DE considered that 'a generally known pest that can be easily controlled by the operator should not be regulated as RNQP. Horizontal regulation in the marketing regulations should ensure that the consignments to be marketed/moved are “practically free from pests”'. DE also considered that plats for planting was not the main pathway. Evaluation continues on the pathway and impact, considering existing measures to control the pest.
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:
Phytoptus avellanae is an eriophyid mite, which is monophagous on Corylus spp. (Ellis, 2001-2024). It has also been identified on hybrid hazels (European hazel, Corylus avellana × American hazel, Corylus americana) (Shanovich et al., 2023).
Mites infest floral and vegetative buds of hazels and feed on the epidermal cells, causing the buds to form galls and swell to several times their normal size. Ultimately, this 'big bud' syndrome causes developmental failure and desiccation of the flowers (Castagnoli & Oldfield, 1996; Shanovich et al., 2023).
The formation of 'big buds' can be observed as early as late summer when generations begin to overlap as eggs hatch and the infestation spreads to the outer scales of the buds. The mites continue reproducing and feeding through the winter, cycling through several generations inside the buds, until the following spring where the adults of the last generation begin to lay eggs and produce nymphs that will migrate. Nymphs continually migrate by walking from 'big buds' to axillary newly formed buds on the hazel plant or by dispersing via wind or phoresy to buds on other hazel plants. For perspective, thousands of nymphs migrate from last year’s big buds, yet only several reach and enter newly formed buds (Özman & Toros 1997a, 1997b; Shanovich et al., 2023).
The mite can travel with plant material: Phytoptus avellanae was most likely introduced to North America via imports of cultivars of C. avellana derived from its native range in Europe (Lovett 1919; Ourecky & Slate 1969; AliNiazee 1998; cited in Shanovich et al., 2023).
The morphological characteristics of eriophyids considerably compromise the active search for a new host plant, so that dispersal is generally passive, mainly due to wind transportation or by exploiting other organisms, such as other arthropods or even humans working in the field (de Lillo et al., 2018; Contarini et al., 2022). However, considering that its biology is closely linked to the crop (they can only live and reproduce on hazel buds), plants for planting may act as its main dispersal route in areas without previous presence of its host (e.g. establishment of new plantations).
The Fruit SEWG considered that both, plants for planting and spread by wind, were significant pathways in areas where the pest is present.
Mites infest floral and vegetative buds of hazels and feed on the epidermal cells, causing the buds to form galls and swell to several times their normal size. Ultimately, this 'big bud' syndrome causes developmental failure and desiccation of the flowers (Castagnoli & Oldfield, 1996; Shanovich et al., 2023).
The formation of 'big buds' can be observed as early as late summer when generations begin to overlap as eggs hatch and the infestation spreads to the outer scales of the buds. The mites continue reproducing and feeding through the winter, cycling through several generations inside the buds, until the following spring where the adults of the last generation begin to lay eggs and produce nymphs that will migrate. Nymphs continually migrate by walking from 'big buds' to axillary newly formed buds on the hazel plant or by dispersing via wind or phoresy to buds on other hazel plants. For perspective, thousands of nymphs migrate from last year’s big buds, yet only several reach and enter newly formed buds (Özman & Toros 1997a, 1997b; Shanovich et al., 2023).
The mite can travel with plant material: Phytoptus avellanae was most likely introduced to North America via imports of cultivars of C. avellana derived from its native range in Europe (Lovett 1919; Ourecky & Slate 1969; AliNiazee 1998; cited in Shanovich et al., 2023).
The morphological characteristics of eriophyids considerably compromise the active search for a new host plant, so that dispersal is generally passive, mainly due to wind transportation or by exploiting other organisms, such as other arthropods or even humans working in the field (de Lillo et al., 2018; Contarini et al., 2022). However, considering that its biology is closely linked to the crop (they can only live and reproduce on hazel buds), plants for planting may act as its main dispersal route in areas without previous presence of its host (e.g. establishment of new plantations).
The Fruit SEWG considered that both, plants for planting and spread by wind, were significant pathways in areas where the pest is present.
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Yes
Justification:
Phytoptus avellanae, with its feeding activity, is responsible of damages to generative and vegetative buds and induces physiological changes, such as a reduced photosynthetic activity, a disruption of normal plant growth processes, deformation, and necrosis of tissues (¨Ozman and Toros, 1997). All these physiologic effects can have a significant impact on the quality and quantity of nut production (Turco et al., 2024).
Phytoptus avellanae infestations are well known in many areas where the hazelnut is cultivated, but, in recent years, outbreaks have been rising to alarming levels, probably due to the gradual increase in temperatures and the expansion of the crop towards areas not particularly suitable for growth (Contarini et al., 2024). In recent years, this mite has become a major pest of hazelnut orchards in Georgia where sometimes the loss caused by them reaches 90% (Abramishvili et al., 2018). Likewise, Contarini et al. (2022) show an overall increase, in recent years, of big bud mite infestation in the monitored hazelnut orchard located in central Italy. This pest exhibits its harmfulness on several cultivars grown in Europe, becoming one of the main pests in hazelnut plantations and causing remarkable commercial losses.
The damage caused by P. avellanae ranged from 18% to 70% of big bud incidence for different varieties and countries (Pesante, 1961; Viggiani, 1973; Viggiani and Bianco, 1973; Krantz, 1979; Maziarz, 1984; Ozman, 1995; Stamenkovic et al., 1997) (see references in Özman-Sullivan and Akça, 2005). In Oregon (USA), bud damage of up to 20% has been observed in susceptible cultivars of C. avellana such that development of cultivars resistant to P. avellanae is now part of the hazel breeding program at Oregon State University (Krantz 1974; Murray & Jepson 2018). Phytoptus avellanae s.s. damages 50% of buds in South Europe and Middle East (de Lillo et al., 2018). An economic threshold has been established at 15-20% of infested buds (Viggiani & Bianco, 1974; cited in Castagnoli & Oldfield, 1996).
In the hazelnut cultivars in the Blacksea Region, Ozman and Toros (1997b) show that the gall form of P. avellanae feeds exclusively on generative buds and causes formation of bigbuds; whereas the vagrant form of P. avellanae does not cause big bud formation, but feeds intensively on both vegetative and generative buds, on catkins and on young fruit clusters which eventually fall. It can therefore be assumed that the vagrant form also has an economic impact on the crop.
Phytoptus avellanae infestations are well known in many areas where the hazelnut is cultivated, but, in recent years, outbreaks have been rising to alarming levels, probably due to the gradual increase in temperatures and the expansion of the crop towards areas not particularly suitable for growth (Contarini et al., 2024). In recent years, this mite has become a major pest of hazelnut orchards in Georgia where sometimes the loss caused by them reaches 90% (Abramishvili et al., 2018). Likewise, Contarini et al. (2022) show an overall increase, in recent years, of big bud mite infestation in the monitored hazelnut orchard located in central Italy. This pest exhibits its harmfulness on several cultivars grown in Europe, becoming one of the main pests in hazelnut plantations and causing remarkable commercial losses.
The damage caused by P. avellanae ranged from 18% to 70% of big bud incidence for different varieties and countries (Pesante, 1961; Viggiani, 1973; Viggiani and Bianco, 1973; Krantz, 1979; Maziarz, 1984; Ozman, 1995; Stamenkovic et al., 1997) (see references in Özman-Sullivan and Akça, 2005). In Oregon (USA), bud damage of up to 20% has been observed in susceptible cultivars of C. avellana such that development of cultivars resistant to P. avellanae is now part of the hazel breeding program at Oregon State University (Krantz 1974; Murray & Jepson 2018). Phytoptus avellanae s.s. damages 50% of buds in South Europe and Middle East (de Lillo et al., 2018). An economic threshold has been established at 15-20% of infested buds (Viggiani & Bianco, 1974; cited in Castagnoli & Oldfield, 1996).
In the hazelnut cultivars in the Blacksea Region, Ozman and Toros (1997b) show that the gall form of P. avellanae feeds exclusively on generative buds and causes formation of bigbuds; whereas the vagrant form of P. avellanae does not cause big bud formation, but feeds intensively on both vegetative and generative buds, on catkins and on young fruit clusters which eventually fall. It can therefore be assumed that the vagrant form also has an economic impact on the crop.
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:
Evidence of its economic impact is available in the literature
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:
Cultivar differences in susceptibility, monitoring big buds and discission thresholds (Contarini et al., 2022): Several studies highlighted differences in susceptibility between cultivars commonly grown in Europe (e.g. Barrios et al., 2014; Contarini et al., 2024) and genetic bases of the susceptibility of hazelnut to big bud mite have been explored, but susceptible cultivars are still preferred by hazelnut industry (de Lillo et al., 2018).
Budbreak to shoot elongation: monitoring, pesticide application (Murray & Jepson 2018).
Chemical treatment of moment of migration (Castagnoli & Oldfield, 1996).
To date, the application of sulphur-based products remains a standard strategy for controlling mite outbreaks, either in IPM or organic hazelnut orchards (Contarini et al., 2024). To complement the use of sulphur, it is also recommended to remove big buds in winter, as this largely removes the sources of infestation for the following spring (Özman-Sullivan and Akça, 2005).
Budbreak to shoot elongation: monitoring, pesticide application (Murray & Jepson 2018).
Chemical treatment of moment of migration (Castagnoli & Oldfield, 1996).
To date, the application of sulphur-based products remains a standard strategy for controlling mite outbreaks, either in IPM or organic hazelnut orchards (Contarini et al., 2024). To complement the use of sulphur, it is also recommended to remove big buds in winter, as this largely removes the sources of infestation for the following spring (Özman-Sullivan and Akça, 2005).
7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
Yes
Conclusion:
Candidate
Justification:
CONCLUSION ON THE STATUS:
Recommended for listing as an RNQP based on data and PM 4 Standard.
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:
- AliNiazee MT (1998) Ecology and management of hazelnut pests. Annual Review of Entomology 43, 395–41.
- Abramishvili T, Gaganidze D, Ozman-Sullivan SK & Abashidze E (2018) Phylogenetic análisis of hazelnut big bud mite Phytoptus avellanae Nal. in the Black Sea Region of Georgia. Bulletin of the Georgian National Academy of Sciences 12(4), 113-118.
- Barrios G, Mateu J & Aymamí A (2014) La gestión de la sanidad vegetal en el cultivo del avellano. Phytoma 255, 36-46.
- Castagnoli M & Oldfield GN (1996) “Other fruit trees and nut trees”, In Eriophyoid Mites-Their Biology, Natural Enemies and Control (eds Lindquist EE, Sabelis MW & Bruin J). Elsevier Science BV, Amsterdam, NL. pages 543–559. doi: 10.3791/51738
- Contarini M, Rossini L, Di Sora N, de Lillo E & Speranza S (2022) Monitoring the bud mite pest in a hazelnut orchard of central Italy: do plant height and irrigation influence the infestation level? Agronomy 12, 1982. https://doi.org/10.3390/agronomy12081982.
- Cvrković T, Chetverikov P, Vidovic B & Petanović R (2016). Cryptic speciation within Phytoptus avellanae s.l. (Eriophyoidea: Phytoptidae) revealed by molecular data and observations on molting Tegonotus-like nymphs. Exp. Appl. Acarol. 68, 83–96. doi: 10.1007/s10493-015-9981-5
- Contarini M, Rossini L, Di Sora N, de Lillo E & Speranza S (2022) Monitoring the bud mite pest in a hazelnut orchard of Central Italy: do plant height and irrigation influence the infestation level? Agronomy, 12, 1982. https://doi.org/10.3390/agronomy12081982
- Contarini M, Masturzi R, Iezzi E, Petrovic M, Silvestri C, Turco S, Speranza S & Rossini L (2024) Can pest management and cultivar affect Phytoptus avellanae infestations on hazelnut? Insects, 15, 740. https://doi.org/10.3390/insects15100740
- De Jong Y, Kouwenberg J, Boumans L, Hussey C, Hyam T, Nicolson N, Kirk P, Paton A, Michel E, Guiry MD, Boegh PS, Ærenlund Pedersen H, Enghoff H, Von Raab-Straube E, Güntsch A, Geoffroy M, Müller A, Kohlbecker A, Berendsohn W, Appeltans W, Arvanitidis C, Vanhoorne B, Declerck G, Vandepitte L, Hernandez F, Nash R, Costello MJ, Ouvrard D, Bezard-Falgas P, Bourgoin T, Wetzel FT, Glöckler F, Korb G, Ring C, Hagedorn G, Häuser C, Aktaç N, Asan A, Ardelean A, Vieira Borges PA, Dhora D, Khachatryan H, Malicky M, Ibrahimov S, Tuzikov A, De Wever A, Moncheva S, Spassov N, Chobot K, Popov A, Boršić I, Sfenthourakis S, Kõljalg U, Uotila P, Olivier G, Dauvin JC, Tarkhnishvili D, Chaladze G, Tuerkay M, Legakis A, Peregovits L, Gudmundsson G, Ólafsson E, Lysaght L, Galil BS, Raimondo FM, Domina G, Stoch F, Minelli A, Spungis V, Budrys E, Olenin S, Turpel A, Walisch T, Krpach V, Gambin MT, Ungureanu L, Karaman G, Kleukers RMJC, Stur E, Aagaard K, Valland N, Loennechen Moen T, Bogdanowicz W, Tykarski P, Węsławski JM, Kędra M, De Frias Martins AM, Domingos Abreu A, Silva T, Medvedev S, Ryss A, Šimić S, Marhold K, Stloukal E, Tome D, Ramos MA, Valdés B, Pina F, Kullander S, Telenius A, Gonseth Y, Tschudin P, Sergeyeva O, Vladymyrov V, Bohdanovych Rizun V, Raper C, Lear D, Stoev P, Penev L, Casino Rubio A, Backeljau T, Saarenmaa H, Ulenberg S (2015) PESI - a taxonomic backbone for Europe. Biodiversity Data Journal 3: e5848. https://doi.org/10.3897/BDJ.3.e5848.
- de Lillo E, Pozzebon A, Valenzano D and Duso C (2018) An intimate relationship between eriophyoid mites and their host plants – a review. Frontiers in Plant Sciences 9, 1786. doi: 10.3389/fpls.2018.0178
- Ellis WN (2001-2024) Plant parasites of Europe: leafminers, galls and fungi. https://bladmineerders.nl/parasites/animalia/arthropoda/insecta/hemiptera/sternorrhyncha/psylloidea/psyllidae/psyllinae/cacopsylla/ (accessed 26/Aug/2024).
- Krantz GW (1974) The role of Phytocoptella avellanae (Nal.) and Cecidophyopsis vermiformis (Nal.)
- (Eriophyoidea) in big bud of filbert. In: Piefl E (ed) Proceedings of the 4th International Congress of Acarology. Akadémiai Kiadó, Budapest, Hungary, pp 62-62.
- Lovett AL (1919) Nut insects. Proceedings of the Western Walnut Association 1: 15-17.
- Murray K, Jepson P (2018) An integrated pest management strategic plan for hazelnuts in Oregon and Washington. Oregon State University. https://catalog.extension.oregonstate.edu/em9223 (accessed 26/Aug/2024).
- Ourecky DK & Slate GL (1969) Susceptibility of filbert varieties and hybrids to the filbert bud mite,
- Phytoptus avellanae Nal. Northern Nut Growers Association Annual Report 60, 89-91
- Özman SK & Toros S (1997a) Life cycles of Phytoptus avellanae Nal. and Cecidiopyopsis vermiformis Nal. (Eriphyoidea: Acarina). Acta Horticulturae 1997, 445, 493–501.
- Özman SK & Toros S (1997b) Damaged caused by Phytoptus avellanae Nal. and Cecidiopyopsis vermiformis Nal. (Eriphyoidea: Acarina) in hazelnut. Acta Horticulturae 445, 537-543.
- Özman-Sullivan SK & Akça I (2005) Efficiency of pesticides against big bud mites [Phytoptus avellanae Nal. and Cecidophyopsis vermiformis Nal. (Acarina: Eriophyoidea)] on hazelnut. Acta Horticulturae, 686: Proc. VI International Congress on Hazelnut: 393-398.
- PESI (2024) Pan-European Species directories Infrastructure. (Accessed through www.eu-nomen.eu/portal, 26/Aug/2024).
- Shanovich HN, Chediack A, Fischbach JA & Aukema B (2023) Spatial patterns suggest movement of the filbert bud mite (Phytoptus avellanae) between plants and overwintering infestations in a hazelnut (Corylus spp.) orchard. Preprint DOI: 10.21203/rs.3.rs-2684613/v1.
- Turco S, Brugneti F, Giubilei I, Silvestri C, Petrovic M., Drais MI, Cristofori V, Speranza S, Mazzaglia A, Contarini M & Rossini L (2024) A bud’s life: Metabarcoding análisis to characterize hazelnut big buds microbiome biodiversity. Microbiological Research, 287: 127851. https://doi.org/10.1016/j.micres.2024.127851
- Viggiani G & Bianco M (1974) Osservazioni ed esperienze per una lotta chimica razionale contro Phytoptus avellanae Nalepa (Acari : Eriophyidae). Boll. Lab. Ent. Agr. Portici, 31: 30-53
