| Legend |
|---|
| Justification for qualification based on EPPO PM 4 Standards |
| Justification for disqualification |
| Additional or non-conclusive information |
| Standard text |
NAME OF THE ORGANISM: Aleurothrixus floccosus (ALTHFL)
GENERAL INFORMATION ON THE PEST
Name as submitted in the project specification (if different):
Pest category:
Insecta
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):
Remarks:
- Fortunella is considered to be a synonym of Citrus by some authors. Using SSRs markers, Fortunella clusters within the genus Citrus (Barkley et al., 2006). These should be considered the same genus.
- Poncirus is considered to be a synonym of Citrus by some authors, and is categorized as such in EPPO GD. However, when using SSRs markers, Poncirus is a sister genus to Citrus (Barkley et al., 2006). In addition, one chromosomal marker can be used to distinguish Poncirus from Citrus species (Brasileiro Vidal et al., 2007). Whether to consider these as synonym or not is still a matter of debate.
According to Martin et al. (2000), there is a question over the identity of A. floccosus, with some populations having the puparial subdorsum darkly coloured, whilst others have the puparia entirely pale; the significance of this difference remains to be investigated.
- Fortunella is considered to be a synonym of Citrus by some authors. Using SSRs markers, Fortunella clusters within the genus Citrus (Barkley et al., 2006). These should be considered the same genus.
- Poncirus is considered to be a synonym of Citrus by some authors, and is categorized as such in EPPO GD. However, when using SSRs markers, Poncirus is a sister genus to Citrus (Barkley et al., 2006). In addition, one chromosomal marker can be used to distinguish Poncirus from Citrus species (Brasileiro Vidal et al., 2007). Whether to consider these as synonym or not is still a matter of debate.
According to Martin et al. (2000), there is a question over the identity of A. floccosus, with some populations having the puparial subdorsum darkly coloured, whilst others have the puparia entirely pale; the significance of this difference remains to be investigated.
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):
Croatia (2019); Cyprus (1997); France (1997); France/Corse (1997); Greece (2017); Greece/Kriti (2017); Italy (1997); Italy/Sicilia (1997); Italy/Sardegna (2012); Malta (2012); Portugal (2008); Portugal/Azores (2005); Portugal/Madeira (2008); Spain (2012); Spain/Islas Canárias (2012)
Conclusion:
Candidate
Justification (if necessary):
Data of the presence of this pest on the EU territory are available in EPPO Global Database (https://gd.eppo.int/).
HOST PLANT N°1: Citrus (Poncirus) (1CIDG) 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 Aleurothrixus floccosus is recommended in EPPO Standard PM 4-12 Pathogen-tested citrus trees and rootstocks. In responses to the consultation about draft recommendations for RNQP Project part 2, ES supported deregulation in the EU, considering that the pest has low economic impact and that plants for planting is not a significant pathway. Evaluation continues on these two criteria.
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:
Aleurothrixus floccosus is reported as a polyphagous whitefly species, having been recorded on more than twenty different plant genera of various families (Martin et al., 2000; Malumphy et al., 2015). Poncirus trifoliata is cited as a host in Turkey (Ulusoy et al., 2003). However, citrus is the most preferred host (Pauloson and Beardsley, 1986). In the Mediterranean region where the whitefly was introduced, it infests almost exclusively species of the genus Citrus (CABI, 2021; Barbagallo et al., 1986 in García-Marí, 2012).
Plants for planting is a pathway for entry in a new area (CABI, 2021).
Although, according to Katsoyannos (1991), adults rarely fly and, even when they do so, they fly rather short distances, García-Marí (2012) reports that they fly actively and are borne by the wind, thus dispersing to other trees and/or nearby plantations. The rapid spread of this pest after its introduction in Spain and Italy (reviewed by García-Marí, 2012) is compatible with a dissemination mainly through other means than plant reproductive material.
The Fruit SEWG concluded that plants for planting was not their main means of dissemination in areas where the pest is already present.
Remark: Although CABI (2021) indicates that C. noacki does not attack populations with heavily pigmented nymphs and pupae, no other reference to this fact has been found in the bibliography consulted. See also remarks on taxonomy.
Plants for planting is a pathway for entry in a new area (CABI, 2021).
Although, according to Katsoyannos (1991), adults rarely fly and, even when they do so, they fly rather short distances, García-Marí (2012) reports that they fly actively and are borne by the wind, thus dispersing to other trees and/or nearby plantations. The rapid spread of this pest after its introduction in Spain and Italy (reviewed by García-Marí, 2012) is compatible with a dissemination mainly through other means than plant reproductive material.
The Fruit SEWG concluded that plants for planting was not their main means of dissemination in areas where the pest is already present.
Remark: Although CABI (2021) indicates that C. noacki does not attack populations with heavily pigmented nymphs and pupae, no other reference to this fact has been found in the bibliography consulted. See also remarks on taxonomy.
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Yes
Justification:
As with most whitefly species, A. floccosus affects the host plant by the suction of sap from the infested young leaves. High infestations can be detrimental to young plants. Indirect damage is also caused by the large amount of honeydew produced by the nymphs. Another type of indirect damage is the formation of sooty moulds on the honeydew which impairs the photosynthetic process of the plant part affected (CABI, 2021).
However, A. floccosus has only the status of occasional pest in several EU countries because it is very effectively controlled by Cales noacki (it only causes economic damage in circumstances where control by this parasitoid is interfered with e.g. inadequate treatments with broad spectrum insecticides) (Franco et al., 2006; García-Marí, 2012; MAPA, 2022).
C. noacki was first introduced into Europe in 1970, in France - imported from Chile (Onillon and Onillon, 1972). One year after its release, it had achieved total control of A. floccosus populations (Onillon, 1990). Also in 1970, three species of parasitoids were introduced into Spain: C. noacki, Amitus spiniferus and Eretmocerus paulistis (Beitia, 1984). Of these, only C. noacki was able to establish and reproduce in the field, and its high parasitoid activity and expansion throughout the Spanish citrus-growing area was reported. A. spiniferus also became established in some areas where currently it appears parasitizing A. floccosus together with C. noacki and exerting a complementary action in whitefly control (reviewed by Castañé et al., 2010 and García-Marí, 2012).
Before 1978, Amitus spiniferus and Cales noacki were accidentally introduced into Italy through the French border. A. spiniferus was successfully established in north-western Italy with appreciable activity (Arzone and Vidano, 1983; Barbagallo et al., 1992; Viggiani, 1993) but failed to establish in the southern regions of the country (Longo et al., 1985; Maniglia, 1988). Cales noacki showed better adaptation throughout Italy, with high levels of parasitism (Arzone and Vidano, 1983; Longo et al., 1985; Ortu and Prota, 1986; Guerrieri and Viggiani, 1988) (reviewed by García-Marí, 2012).
C. noacki was imported into Greece in 1991 from Valencia (Spain) (Katsoyannos, 1991). Later, Katsoyannos et al. (1998) considered that, in Greece, C. noacki is an effective natural enemy against woolly whitefly with parasitism rates exceeding 82 %.
C. noacki is considered widespread in citrus growing countries of the EPPO region and economic impact is nowadays much reduced.
However, A. floccosus has only the status of occasional pest in several EU countries because it is very effectively controlled by Cales noacki (it only causes economic damage in circumstances where control by this parasitoid is interfered with e.g. inadequate treatments with broad spectrum insecticides) (Franco et al., 2006; García-Marí, 2012; MAPA, 2022).
C. noacki was first introduced into Europe in 1970, in France - imported from Chile (Onillon and Onillon, 1972). One year after its release, it had achieved total control of A. floccosus populations (Onillon, 1990). Also in 1970, three species of parasitoids were introduced into Spain: C. noacki, Amitus spiniferus and Eretmocerus paulistis (Beitia, 1984). Of these, only C. noacki was able to establish and reproduce in the field, and its high parasitoid activity and expansion throughout the Spanish citrus-growing area was reported. A. spiniferus also became established in some areas where currently it appears parasitizing A. floccosus together with C. noacki and exerting a complementary action in whitefly control (reviewed by Castañé et al., 2010 and García-Marí, 2012).
Before 1978, Amitus spiniferus and Cales noacki were accidentally introduced into Italy through the French border. A. spiniferus was successfully established in north-western Italy with appreciable activity (Arzone and Vidano, 1983; Barbagallo et al., 1992; Viggiani, 1993) but failed to establish in the southern regions of the country (Longo et al., 1985; Maniglia, 1988). Cales noacki showed better adaptation throughout Italy, with high levels of parasitism (Arzone and Vidano, 1983; Longo et al., 1985; Ortu and Prota, 1986; Guerrieri and Viggiani, 1988) (reviewed by García-Marí, 2012).
C. noacki was imported into Greece in 1991 from Valencia (Spain) (Katsoyannos, 1991). Later, Katsoyannos et al. (1998) considered that, in Greece, C. noacki is an effective natural enemy against woolly whitefly with parasitism rates exceeding 82 %.
C. noacki is considered widespread in citrus growing countries of the EPPO region and economic impact is nowadays much reduced.
What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
Minor
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?
Yes
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?
No
Conclusion:
Not candidate
Justification:
Considering that there may be a time lapse between pest occurrence and parasitoid action, the Fruit SEWG rated economic impact as ‘minor’ (this pest may cause some damage). Its 'Minor' economic impact does not qualify it as RNQP.
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?
Conclusion:
Justification:
In Spanish certification scheme, the pest is only controlled by visual examination and, in case of doubt, sampling and testing. It is considered that the 'substantially free from' requirement would be enough.
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 unacceptable economic impact after that biological control was established. Plants for planting is not considered as a significant pathway compared to natural spread.
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:
- Barkley NA, Roose ML, Krueger RR & Federici CT (2006) Assessing genetic diversity and population structure in a citrus germplasm collection utilizing simple sequence repeat markers (SSRs). Theor Apple Genet 112(8), 1519-31.
- Brasileiro-Vidal AC, Dos Santos-Serejo JA, Soares Filho Wdos S & Guerra M (2007) A simple chromosomal marker can reliably distinguishes Poncirus from Citrus species. Genética 129(3), 273-9.
- Castañe C, Arnó J, Beitia F, Gabarra R (2010) Capítulo 15. Control biológico de moscas blancas. In “Control biológico de plagas agrícolas”. Ed. Jacas J.A., Urbaneja A. M.V. Phytoma-España S.L. 496 pp.
- CABI (2021) Datasheet on Aleurothrixus floccosus (wooly whitefly). CABI Compendium. 4538. Available at https://doi.org/10.1079/cabicompendium.4538
- Franco JC, Garcia-Mari F, Ramos AP & Besri M (2006) Survey on the situation of citrus pest management in Mediterranean countries. IOBC wprs Bulletin 29(3), 335-346.
- Garcia-Mari F (2012) Plagas de los cítricos. Gestión Integrada en países de clima mediterráneo. M.V. Phytoma-España, S.L. 556 pp.
- Garrido A (1994) Problemas actuales de las moscas blancas en el cultivo de los cítricos (I). Phytoma 58, 48-54.
- Garrido A (1995) Moscas blancas en España en los cítricos: importancia, interacciones entre especies, problemática y estrategia de control. Phytoma 72, 41-47.
- Hamon AB (1981) Wolly whitefly, Aleurothrixus floccosus (Maskell) (Homoptera: Aleyrodidae: Aleyrodinae). Entomoloy Circular, 32.
- Malumphy C, Radonjic S, Hrncic S, Raicevic M (2015). New data on the whiteflies (Insecta: Hemiptera: Aleyrodidae) of Montenegro, including three new species new for the country. Acta entomologica serbica 20, 29-41.
- Katsoyannos P (1991) First record of Aleurothrixus floccosus (Mask.) (Homoptera: Aleyrodidae) in Greece and some observations on its phenology. Entomologia Hellenica 9, 69-72.
- Katsoyannos P, Kontodimas DC & Stathas GJ (1998) The inundative release of Cales noacki Howard (Hymenoptera: Aphelinidae), for curative treatment of Aleurothrixus floccosus (Maskell) (Homoptera: Aleyrodidae) on heavily infested citrus in Greece. Annals of the Benaki Phytopathological Institute 18, 111–122.
- MAPA (2022) Cítricos. Guía de gestión integrada de plagas. Ministerio de Agricultura, Pesca y Alimentación. Gobierno de España. https://www.mapa.gob.es/es/agricultura/temas/sanidad-vegetal/guiagipcitricos_vers2_tcm30-57942.pdf
- Martin JH, Mifsud D & Rapisarda C (2000) The whiteflies (Hemiptera: Aleyrodidae) of Europe and the Mediterranean Basin. Bulletin of Entomological Research 90, 407-448.
- Pauloson GS & Beardsley JW (1986) Development, oviposition, and longevity of Aleurothrixus floccosus (Maskel) (Hemiptera: Aleyrodidae). Proc. Hawaii Entomol. Soc., 26, 97-99.
- Ulusoy MR, Vatansever G, Erkilic L & Uygun N (2003) Studies on Aleurothrixus floccosus (Maskell) (Homoptera, Aleyrodidae) and its parasitoid, Cales noacki Howard (Hymenoptera, Aphelinidae) in the East Mediterranean Region of Turkey. J. Pest Science 76, 163–169.
