
Aleurocanthus spiniferus, A. woglumi and A. citriperdus
European Food Safety Authority (EFSA), Gabriele Rondoni, Alice Delbianco
Updated 14 May 2024 ( Version 2 )
Abstract
This document is an update of the pest survey card on Aleurocanthus spiniferus, A. woglumi and A. citriperdus that was prepared in the context of the EFSA mandate on plant pest surveillance (M-2017-0137) at the request of the European Commission. Its purpose is to guide the Member States in preparing data and information for surveys of the whiteflies Aleurocanthus spiniferus (Quaintance, 1903), A. woglumi (Ashby, 1915) and A. citriperdus Quaintance & Baker, 1916. These three Aleurocanthus species are listed as Union quarantine pests. They originate from south-east Asia, with A. spiniferus being the only one present in the EU. Although A. spiniferus and A. woglumi are highly polyphagous, all the three species have a preference for Citrus spp., where they mainly feed on leaves. Aleurocanthus spp. are multivoltine. Establishment of these Aleurocanthus species throughout the EU is likely because to the presence of suitable hosts and favourable climatic conditions, particularly in the Mediterranean area. In fact, A. spiniferus is already present in some European countries. Detection surveys should be conducted on Citrus spp. and other hosts cultivated on a large scale. Delimiting surveys after introduction should target all known host plants. Aleurocanthus spp. group into small, black spiny lumps on the underside of leaves, causing leaf distortion and, eventually, abscission. The most effective detection method is the visual examination of host plants for the presence of symptoms and/or insect lumps. Yellow sticky traps can also be used. Expertise is required for morphological identification at the species level, which relies on microscopic examination of the puparia and can be supported by molecular methods. The three species are present all year round, but the best timing for surveys is during the summer, when population densities usually peak.
© European Food Safety Authority, 2024
Heading picture: © Florida Division of Plant Industry, Florida Department of Agriculture and Consumer Services, Bugwood.org (Aleurocanthus woglumi).
Authors' affiliation: Gabriele Rondoni, Department of Agricultural, Food and Environmental Sciences, University of Perugia (UNIPG, Italy); Alice Delbianco, European Food Safety Authority (EFSA).
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Introduction
The objective of this pest survey card is to provide the relevant information needed to prepare surveys for Aleurocanthus spiniferus (Quaintance, 1903), A. woglumi (Ashby, 1915) and A. citriperdus Quaintance & Baker, 1916, in EU Member States (MSs) following the methodology described in EFSA et al. (2018) . It is part of a toolkit that has been developed to assist the MSs with planning a statistically sound and risk-based pest survey approach in line with the recommendations and guidelines provided by the International Plant Protection Convention (IPPC) in the various International Standards for Phytosanitary Measures (ISPM 6: FAO 2021a ; ISPM 8: FAO, 2021b ; ISPM 31: FAO, 2021c ) and surveillance guide ( FAO, 2021d ). The EFSA Plant Pest Survey Toolkit consists of pest specific documents and more general documents relevant for all pests to be surveyed:
i. Pest-specific documents:
a. The pest survey card on Aleurocanthus spiniferus, A. woglumi, and A. citriperdus.
ii. General documents:
a. General guidelines for statistically sound and risk-based surveys of plant pests (EFSA et al., 2020).
c. The RiPEST manual , RiBESS+ manual and video tutorial .
This document is an update of the pest survey card on Aleurocanthus spiniferus, A. woglumi and A. citriperdus (EFSA, 2020), which was prepared in the context of the EFSA mandate on plant pest surveillance (M-2017-0137) at the request of the European Commission. The information presented in this pest survey card was summarised from pest categorisation of Aleurocanthus spp. ( EFSA PLH Panel, 2018 ), the European and Mediterranean Plant Protection Organization (EPPO) datasheets on A. spiniferus and on A. woglumi (EPPO, 2024a , b ), the EPPO Global Database for A. citriperdus ( EPPO, 2024c ) and the Centre for Agriculture and Bioscience International (CABI) Compendium on A. spiniferus, A. woglumi and A. citriperdus (CABI, 2022a,b; Nguyen, 2022), and other documents.
The main challenges relevant for surveillance of Aleurocanthus spp. is the identification at species level, which should be conducted through microscopic observation of the puparia.
1. The pest and its biology
1.1. Taxonomy
Current scientific name: Aleurocanthus spiniferus (Quaintance, 1903) Class: Insecta Order: Hemiptera Family: Aleyrodidae Genus: Aleurocanthus Species: Aleurocanthus spiniferus Synonyms: Aleurodes spinifera, Aleurodes citricola, Aleurocanthus citricolus, Aleurocanthus rosae EPPO code: ALECSN Common name: Orange spiny whitefly, spiny blackfly Taxonomic rank: species
Current scientific name: Aleurocanthus woglumi (Ashby, 1915) Class: Insecta Order: Hemiptera Family: Aleyrodidae Genus: Aleurocanthus Species: Aleurocanthus woglumi Synonyms: Aleurocanthus punjabensis, Aleurocanthus woglumi var. formosana, Aleurodes woglumi EPPO code: ALECWO Common name: Citrus blackfly Taxonomic rank: species
Current scientific name: Aleurocanthus citriperdus Quaintance & Baker, 1916 Class: Insecta Order: Hemiptera Family: Aleyrodidae Genus: Aleurocanthus Species: Aleurocanthus citriperdus Synonym: Aleurocanthus cameroni EPPO code: ALECCT Taxonomic rank: species
Conclusion on taxonomy
1.2. EU pest regulatory status
Aleurocanthus spiniferus, A. woglumi and A. citriperdus are Union quarantine pests listed in Annex II of Commission Implementing Regulation (EU) 2019/2072 . A. citriperdus and A. woglumi are listed in Part A of the Annex (pests not known to occur in the Union territory), while A. spiniferus is listed in Part B of the Annex (pests known to occur in the Union territory).
Commission Implementing Regulation (EU) 2022/192 of 11 October 2022 establishes measures for the containment of A. spiniferus within certain demarcated areas in the EU.
Special import requirements are laid down in Annex VII of Commission Implementing Regulation (EU) 2019/2072 (point 30.1) for some plants for planting originating from third countries where the presence of A. spiniferus is known.
Special import requirements are laid down in Annex VIII of Commission Implementing Regulation (EU) 2019/2072 (point 17.1) for some plants for planting (including Citrus spp. and Vitis vinifera) originating in the Union territory for their movement within the Union territory in order to prevent further spread of A. spiniferus.
The import of ‘Plants of Vitis L., other than fruits’ from third countries other than Switzerland and of ‘Plants of Citrus L., Fortunella Swingle, Poncirus Raf. and their hybrids, other than fruits and seeds’ from third countries is prohibited (Annex VI of Commission Implementing Regulation (EU) 2019/2072, points 10 and 11). Fruits of Citrus L., Fortunella Swingle, Poncirus Raf. and their hybrids imported from third countries must be free from peduncles and leaves and the packaging must bear an appropriate origin mark (Annex VII of Commission Implementing Regulation (EU) 2019/2072, point 57).
The general requirements for surveys of quarantine pests in the EU territory are laid down in Regulation (EU) 2016/2031 and Commission Implementing Regulation (EU) 2020/1231 .
Overview of the EU regulatory status
1.3. Pest distribution
Of the three Aleurocanthus species, A. spiniferus is the only one that is currently present in the EU ( EFSA PLH Panel, 2018 ; EPPO, 2024a ). Aleurocanthus spiniferus and A. woglumi originate from south-east Asia and occur in tropical and subtropical Asia and the Pacific, central and southern Africa, and Hawaii ( EFSA PLH Panel, 2018 ; EPPO, 2024a , b ). Aleurocanthus woglumi is also present in Central and South America, while A. spiniferus is present in the EU (Croatia, France, Greece and Italy), Albania and Montenegro (Porcelli, 2008; EPPO, 2024a , b ). Aleurocanthus citriperdus has a more restricted distribution, which is limited to parts of south-east Asia (Dubey and Ko, 2012; EFSA PLH Panel, 2018 ).
Note: the map on the right panel displays the distribution of A. spiniferus. To show the distribution of the other species, click on the above hyperlinks. The information included in this section is aligned with the EPPO map updated on 26-01-2024 for A. spiniferus and on 08-09-2023 for A. woglumi and A. citriperdus.
Conclusion on pest distribution
1.4. Life cycle
The available information on the biology of Aleurocanthus spp. is primarily based on A. spiniferus and A. woglumi, which are very similar ( EFSA PLH Panel, 2018 ). Fewer data are available for A. citriperdus, but it is believed that all species of Aleurocanthus have broadly similar habits ( EFSA PLH Panel, 2018 ). As for all Aleyrodidae, species within the genus Aleurocanthus have three developmental stages: egg, nymph (four instars, the last usually known as pupa) and adult ( EFSA PLH Panel, 2018 ). Adults are winged, emerge in spring, are facultative parthenogenetic, and start laying batches of a variable number of eggs in a characteristic spiral on the underside of young leaves (CABI, 2022b; Nguyen, 2022; EPPO, 2024a , b ). The first instars are active and disperse over a short distance, avoiding strong sunlight and generally settling in a dense colony of up to several hundred on the undersides of young leaves (Dubey and Ko, 2012; CABI, 2022a,b; Nguyen, 2022; EPPO, 2024a , b ). Older immature instars are attached to the leaf by their mouthparts ( EFSA PLH Panel, 2018 ). All instars feed on phloem sap, except for the pupa, which is a resting non-feeding phase (CABI, 2022b). The infestation occurs mainly on the lower part of the tree, mostly on the leaves (EPPO, 2002a , b , 2020b ). Aleurocanthus spiniferus has also been reported on fruit post-harvest, but this is probably due to the presence of the insect on the leaves attached to the fruit peduncle ( EFSA PLH Panel, 2018 ). The duration of the life cycle and the number of generations per year are greatly influenced by the prevailing climate (Gyeltshen et al., 2017). The life cycle takes 2–4 months and can develop 3–6 generations per year (multivoltinism) (CABI, 2022b). In tropical and subtropical climates, there may be continuous overlapping generations with slowed development during short, cold periods (Hodges and Evans, 2005). The life cycle of A. woglumi in southern Africa takes between 6 and 12 weeks depending on temperature, resulting in 5–6 generations per year (Bedford, 1998). Optimal development occurs at 28–32°C and 70–80% relative humidity. Aleurocanthus woglumi has been shown to not survive at temperatures below freezing or exceeding 43°C ( EFSA PLH Panel, 2018 ). The lower threshold for development for A. woglumi is 13.7°C and the cumulative degree-days to complete one generation are approximately 981 (Dowell and Fitzpatrick, 1978; Akrivou et al., 2021). In Asia, A. spiniferus has been shown to overwinter as egg, nymph and pupa on evergreen plants (Akato, 1970; Liu et al., 2023; EPPO, 2024a ).
Conclusion on life cycle
2. Target population
This section provides the information needed to characterise the population of host plants to target in a survey, as described in the ‘General guidelines for statistically sound and risk-based surveys of plant pests’ (EFSA et al., 2020). This includes the pest’s host range and main hosts in the EU ( Section 2.1 ), the suitability of EU environments to the pest’s establishment ( Section 2.2 ), the ability of the pest to spread ( Section 2.3 ), and the identification of risk factors associated with an increased probability of presence ( Section 2.4 ).
Once the above parameters have been defined, the target population can be structured in multiple levels. At level 1 is the survey area, which corresponds to the entirety or part of the Member State. At levels 2 and 3 are the epidemiological units that can be distinguished within the survey area. Epidemiological units can be chosen as administrative regions (e.g. EU NUTS areas or Member State-level regions) if they are homogeneous, or further subdivided into the environments where host plants are present using a land-use categorisation (e.g. urban, agricultural and natural areas, nurseries). At level 4, if risk factors are identified, the risk areas are defined around the risk locations. At level 5 are the inspection units, the elementary subdivisions of the target population that are inspected for the detection of the pest (e.g. host plants), depending on the pest detection method ( Section 3 ). For the definitions of the target population, epidemiological units and inspection units, see also the glossary of terms available at the end of this document.
The hierarchical structure of the target population should be tailored to the situation in each Member State. A possible structure of the target population for surveys of Aleurocanthus spiniferus, A. woglumi and A. citriperdus within the EU is proposed in Section 2.5 .
2.1. Host range and main hosts
Aleurocanthus spiniferus and A. woglumi are highly polyphagous, but with a marked preference for Citrus spp. ( EFSA PLH Panel, 2018 ). Aleurocanthus citriperdus is known to infest mainly Citrus spp. (Dubey and Ko, 2012).
In addition to Citrus spp., A. spiniferus attacks important crops, such as Vitis vinifera, Psidium guajava, Pyrus spp., Diospyros kaki and Rosa spp. (Cioffi et al., 2013; EPPO, 2024a ). It is also known to infest plants of other Rutaceae, as well as Araliaceae, Ebenaceae, Lauraceae, Leguminosae–Caesalpiniaceae, Malvaceae, Moraceae, Punicaceae, Rosaceae and Vitaceae in urban areas, parks and natural protected habitats. In infested areas of Italy, A. spiniferus was recorded from new host plants, which are Ailanthus altissima, Arbutus unedo, Citrus medica, C. reticulata, C. limon, Clematis vitalba, Pistacia vera, Prunus avium, P. cerasus, P. domestica, Rosa banksiae and R. x damascene, suggesting the ability of this species to easily adapt to new hosts (Porcelli, 2008; EPPO, 2020a ; Nugnes et al., 2020).
Aleurocanthus woglumi can attack more than 300 plant species, including cultivated plants, ornamentals and weeds ( EFSA PLH Panel, 2018 ). According to EPPO, 75 species in 38 families have been reported in Mexico as hosts on which A. woglumi can complete its life cycle ( EPPO, 2024b ). However, it is believed that A. woglumi cannot permanently infest plants other than Citrus spp. ( EFSA PLH Panel, 2018 ).
As for A. citriperdus, the host range includes mainly Citrus species (e.g. C. acida, C. aurantium, C. hystrix, C. limonum, C. nobilis and C. sinensis) but also other plants such as Terminalia catappa, Bischofia javanica, Psydium and Coffea spp. (Dubey and Ko, 2012; Gillespie, 2012).
Detection surveys in EU areas could target major plants where whiteflies can complete development, such as Citrus spp. (all three Aleurocanthus spp.), P. communis, V. vinifera and Rosa spp. (for A. spiniferus and A. woglumi) (EPPO, 2024a , b , c ). Delimiting surveys after detection should target all potential hosts occurring in the EU territory. The full list of reported host plants is available in Evans (2007), EFSA PLH Panel (2018) , CABI (2022a,b), Nguyen (2022) and EPPO ( 2022 , 2024a , b , c ).
Conclusion on host range and main hosts
2.2. Environmental suitability
Climate suitability
The Aleurocanthus genus originates from tropical areas, but some species occur in different regions of the world where the climate matches that of the EU. Particularly in the Mediterranean area, conditions are favourable for establishment of A. spiniferus and A. woglumi ( EFSA PLH Panel, 2018 ). In fact, A. spiniferus is already present in some European countries ( EPPO, 2024b ). As for A. citriperdus, its original area of distribution is limited to tropical climates, which do not correspond to the EU climate ( EFSA PLH Panel, 2018 ). However, this species is considered to be invasive, e.g. in Taiwan (a mostly subtropical climate), therefore possible establishment in some EU areas following accidental introduction cannot be completely excluded (Dubey and Ko, 2012; EPPO, 2024c ).
In tropical conditions, all stages of A. woglumi can be found throughout the year. The optimal conditions for its development are 28–32°C and 70–80% relative humidity (CABI, 2022b). The pest does not survive temperatures below freezing and does not occur in areas where temperatures exceed 43°C. Aleurocanthus spiniferus and A. woglumi both occur on citrus in Kenya where they seem to have different ecological preferences, with A. spiniferus being dominant at higher altitudes and A. woglumi at lower altitudes (CABI, 2022b). Also, A. woglumi does not occur in Korea, whereas A. spiniferus does. This may reflect a lower tolerance to low temperatures for A. woglumi than A. spiniferus (CABI, 2022b, Nguyen, 2022). The suitable areas for A. woglumi modelled with CLIMEX under an historical climate scenario includes the Mediterranean regions of France, Greece, Italy, Portugal and Spain (Akrivou et al., 2021). For A. spiniferus, suitable territories extend further north, including parts of the French and Spanish Atlantic coastal areas (e.g. the Bay of Biscay) (Grünig et al., 2020).
Host availability
Many plant species reported as hosts of A. spiniferus, A. woglumi and A. citriperdus occur in different areas of the EU. Some of them are cultivated (e.g. Citrus spp., V. vinifera) or planted in parks, private gardens and recreational areas (e.g. plants of the genera Buxus, Rosa, Populus and Camellia). In the event of accidental entry of Aleurocanthus spp. into the EU territory, the presence of many potential hosts would favour their establishment ( EFSA PLH Panel, 2018 ). The expansion of the host range following introduction to a new area could also occur, as observed for A. spiniferus in Italy (Cioffi et al., 2013).
Conclusion on environmental suitability
2.3. Spread capacity
Natural spread
Adults of Aleurocanthus spp. are capable of limited down-wind flights (187 m in 24 hours), which only allow dispersal to plants in the same or adjacent fields (Meyerdirk et al., 1979b). Among the nymphs, the first instar is the only one that can move actively, albeit only over short distances. Hence, natural spread cannot be considered an important source of long-range dispersal ( EFSA PLH Panel, 2018 ).
Human-assisted spread
Aleurocanthus spp. are more likely to enter the EU, or to further spread inside EU territories (for A. spiniferus), with commercial trade of host plants and plant products, not excluding fruit and attached leaves (CABI, 2022a). Therefore, the long-distance spread of Aleurocanthus species is primarily human-assisted ( EFSA PLH Panel, 2018 ). Ten interceptions of both A. woglumi and A. spiniferus have been recorded (EUROPHYT, online). Six of them were identified as A. woglumi on Citrus hystrix, Annona reticulata, Citrus sp. and Musaceae. Four interceptions of A. spiniferus were recorded on Camellia sasanqua and Camellia japonica. Aleurocanthus citriperdus has never been intercepted in the EU. Worldwide introductions of the three species are reported in Evans (2007).
Conclusion on spread capacity
2.4. Risk factor identification
Identification of risk factors and their relative risk estimation are essential for performing risk-based surveys. A risk factor is a biotic or abiotic factor that increases the probability of infestation by the pest in the area of interest. The risk factors that are relevant for surveillance need to be characterised by their relative risk (should have more than one level of risk for the target population) and the proportion of the overall target population on which they apply. The identification of risk factors needs to be tailored to the situation of each Member State. This section presents examples of risk factors for A. spiniferus, A. woglumi and A. citriperdus and is not necessarily exhaustive.
For the identification of risk areas, it is first necessary to identify the activities that could contribute to introductionor spread of A. spiniferus, A. woglumi and A. citriperdus. These activities should then be connected to specific locations. Around these locations, risk areas can be defined, knowing that their size depends on the spread capacity of the target pest and the availability of host plants around these locations.
The Member States can opt to utilise the information available on the EU Platforms of TRACES NT, EUROPHYT Interceptions and EUROPHYT Outbreaks. The information available, in particular, relating to the country of origin, type of commodity and hosts of intercepted or outbreak reports can be extracted from such platforms for specific harmful organisms. This information can allow Member States to identify potential pathways of introduction from previous historical findings. Thus, Member States might consider focusing their surveillance efforts around activities and locations related to previous interceptions and outbreaks.
Such information should only be considered as indicative and given the possible dynamic changes, it should be reviewed and analysed periodically.
According to the EFSA PLH Panel (2018) and the EUROPHYT interceptions database, A. spiniferus and A. woglumi were mainly identified on Citrus spp., ornamental plants of Camellia spp., and Annona reticulata. Import of Citrus spp. and other main host plants, including fruit, from third countries is prohibited or strictly regulated. Therefore, entrance of Aleurocanthus spp. via this pathway is unlikely. A realistic pathway for entry into the EU is through the trade of other hosts. Considering that A. spiniferus is already established in some areas of the EU, commercial trade of fruits can contribute to the further spread of the species. However, some Member States may adopt additional measures to strictly regulate the import of citrus fruit.
Example 1: Import, trade and storage of host plants for planting
Adult and juvenile Aleurocanthus spp. can infest different plant species, but only the import and trade of a few of them is prohibited or specifically regulated. Therefore, high-risk locations can be defined where there is a higher probability of detecting the pest, such as nurseries, packing houses, garden centres and other facilities handling imported plants for planting (mostly ornamental plants) or plant commodities from infested areas. Risk areas can be considered to be all neighbouring sites where the main host plants are present.
Example 2: Trade of fruit from infested areas within the EU
Aleurocanthus spiniferus can infest leaves attached to host fruit, notably Citrus spp. Facilities where fruit is packaged and sorted can be risk locations. Adults can escape these locations by active flight and land on surrounding cultivated or naturally occurring host plants located close by. The neighbouring sites where host plants are present are risk areas. The relative risk of the area depends on whether the fruit is kept refrigerated, and whether peduncles and leaves are present with the fruit. Finally, waste disposal procedures for peduncles and attached leaves should be considered.
2.5. Structure of the target population
The figure on the right panel gives examples of the components of a target population for Aleurocanthus spiniferus, A. woglumi and A. citriperdus and is not necessarily exhaustive.
3. Detection and identification
The presence of Aleurocanthus spp. can be observed by inspecting host plants for symptoms of attacks and for the presence of dense colonies (for immature stages and adults), or by using yellow sticky traps (for adults) (Augustin et al., 2012). EPPO produced a standard (PM 7/007 (2) Aleurocanthus citriperdus, Aleurocanthus spiniferus and Aleurocanthus woglumi) ( EPPO, 2022 ) allowing the identification of the three Aleurocanthus species under scrutiny based on the morphology of their puparia and on DNA barcoding of the cytochrome oxydase I (COI) gene. In any case, species identification is difficult, and identity is not established for all the species belonging to Aleurocanthus genus ( EFSA PLH Panel, 2018 ). Molecular identification based on COI barcode is useful to support morphological identification ( EPPO, 2021 ).
3.1. Detection and identification in the field
3.1.1. Visual examination
Symptoms
Symptoms associated with Aleurocanthus spp. are the consequence of intense feeding on the plant. They are not specific to Aleurocanthus spp., but can be observed at distance and, consequently, may lead to careful inspection of the vegetation.
- Leaves infested by Aleurocanthus spp. may appear curled and distorted (figure below, A), and can fall off during the season ( EPPO, 2024b ).
- Sticky honeydew deposits accumulate on leaves, stems and fruit, developing a sooty mould and giving the foliage (even the whole plant) a sooty appearance ( EPPO, 2024b ) (figures below, D,E,F).
- Insect colonies are grouped in black spiny lumps on the lower side of the leaves and are very noticeable at distance (Nguyen, 2022) (figures below, A,B,C).
- Ants climbing the tree in search of honeydew (CABI, 2022b).
Leaf damage caused by Aleurocanthus spiniferus colonies on Parthenocissus quinquefolia (A), Punica granatum (B) and citrus (C). Presence of sooty mould on citrus plants attacked by A. woglumi (D) and A. spiniferus (E, F) (Sources: © EPPO Global Database, courtesy of Maja Pintar, Centre for Plant Protection, Croatian Agency for Agriculture and Food (A, B); © EPPO Global Database, courtesy of Francesco Porcelli, Università di Bari (IT) (C, E); © Florida Division of Plant Industry, Florida Department of Agriculture and Consumer Services, Bugwood.org (D); © MA van den Berg, Institute for Tropical and Subtropical Crops, Bugwood.org (F))
Pest
- Eggs are elongate-oval, cream-white to pale yellow at first, laid in groups following a characteristic spiral pattern attached to the underside of the leaves ( EPPO, 2024a ) (figures in the right panel, B,D).
- The nymphal stage presents a first mobile instar, two sessile instars and a pupa. The pupa is characterised by numerous dorsal spines and is often surrounded by a white fringe of waxy secretion typical of the species (Dubey and Ko, 2012) (figures below, E,F,G).
- Aleurocanthus spiniferus and A. woglumi adults are smaller than 1.7 mm (females), or 1.35 mm (males). The wings of both species are metallic grey-blue in appearance, covered by a waxy powder, and light markings on the wings form a band across the middle of the red abdomen (CABI, 2022b; Nguyen, 2022; EPPO, 2022 , 2024a , b ) (figures in the right panel, A,B,C). Little information is available for A. citriperdus. Adults are characterised by having mottled wings (Quaintance and Baker, 1917).
Immature stages (A) and pupae (B) of A. spiniferus. Nymphs and puparia of A. woglumi (C) (Source: © EPPO Global Database, courtesy of Mladen Šimala, Centre for Plant Protection, Croatian Agency for Agriculture and Food (A); © EPPO Global Database, courtesy of Francesco Porcelli, Università di Bari (IT) (B); © Florida Division of Plant Industry, Florida Department of Agriculture and Consumer Services, Bugwood.org (C))
3.1.2. Trapping
Aleurocanthus spiniferus prefers yellow traps over other coloured traps (Wang et al., 2015). Males are captured more frequently than females, with the peak of captures occurring between 07:00 and 15:00 (Wang et al., 2015). Traps can be placed about 10 cm above the height of a tree canopy and placed at a density of approximately one trap per 30 m 2 (Wang et al., 2015).
Aleurocanthus woglumi was more attracted by translucent traps than opaque ones, and fluorescent yellow traps had a greater attractiveness than simple yellow ones (Meyerdirk et al., 1979a). Trap shape has no influence on trapping efficiency (Meyerdirk et al., 1979a). In citrus orchards, the optimal trap height was found to be between 1.5 m and 2.0–3.0 m above ground level (Hart et al., 1978; Meyerdirk et al., 1979b). There is no information on effectiveness and range of attraction of chromotropic traps in the literature.
A few reports suggest that attractive odours could improve trapping efficacy (Li and Maschwitz, 1983; Baranowski and Blaszak, 1996; Gorski, 2003), but there is no standardised procedure. The use of yellow sticky cards combined with the sex pheromone successfully mass-trapped A. spiniferus in China (Zhang et al., 2010; Liping and Test, 2016). The sensitivity of the traps is limited by the fact that adult specimens of Aleurocanthus spp. have limited dispersal abilities.
Sticky traps are considered less efficient than visual inspection of vegetation in detecting A. woglumi at low densities (<5% citrus leaves infested) (Dowell and Cherry, 1981). This can also be extended to A. spiniferus. In fact, visual surveys allowed the detection of the first and subsequent infestations of A. spiniferus in Italy (Porcelli, 2008; Rapisarda and Longo, 2021).
3.1.3. Other methods of detection
Adult Aleurocanthus spp. can occasionally be found on fruit (e.g. Citrus spp.) post-harvest ( EPPO, 2020b ). With high levels of field infestation, marketed fruit may also show a sticky and transparent honeydew, eventually covered by sooty mould. However, these symptoms are not specific and cannot be directly linked to Aleurocanthus spp. when observed on traded fruit ( EPPO, 2020b ).
3.1.4. Sample collection
If a suspected adult is trapped on a sticky card, to prevent sample damage the entire trap should be transferred to the laboratory for analysis. Potentially infested leaves should be collected and placed in sealed bags together with some tissue paper to absorb excess moisture, which could damage the sample. If eggs were collected, these can be reared on host plant material up to the pupa stage. In the laboratory, samples can be prepared immediately for morphological examination ( EPPO, 2022 ) or kept in 70% ethanol for later morphological analysis. For molecular analysis, samples can be preserved in 95% ethanol ( EPPO, 2021 ).
3.1.5. Timing of detection and identification
Aleurocanthus spp. are present all year round. However, the best time for detection is in summer, when the symptoms (leaf damage and sooty mould) are more evident and population density peaks. Traps can also be inspected for the presence of adults during this period. The specific timing of detection will vary depending on the specific climate conditions in each Member State.
Conclusion on detection and identification in the field
3.2. Detection and identification in the laboratory
3.2.1. Morphological identification
The required stage for morphological identification is the puparium (pupal case) ( EPPO, 2022 ). Puparia of A. spiniferus, A. woglumi and A. citriperdus are similar in appearance and can also be confused with other Aleurocanthus spp. occurring in Citrus spp. (A. husaini). Morphological differences can be observed under a stereomicroscope and a compound microscope after samples are slide-mounted (Martin, 1999; EPPO, 2022 ). Other keys are available to identify adult whiteflies in Nguyen et al. (2016), Gillespie (2012) and Dubey and Ko (2012). Morphological distinctions of the puparia of Aleurocanthus from other genera are reported in Bink-Moenen (1983), Dubey and Ko (2012), Gillespie (2012) and EPPO (2022) , and the main distinctive characters are the following:
- A. spiniferus: large marginal teeth (6–12 per 0.1 mm). The female puparium has 11 pairs of submarginal glandular spines, placed singly (Dubey and Ko, 2012).
- A. woglumi: large marginal teeth (usually 3–5 per 0.1 mm), with the third posterior-most pair doubled (Gillespie, 2012). The female puparium has 10 pairs of submarginal spines (Dubey and Ko, 2012; EPPO, 2022 ).
- A. citriperdus: crenulated marginal teeth (8–12 per 0.1 mm). The female puparium has 15–16 pairs of submarginal glandular spines, never doubled at the base (Dubey and Ko, 2012). The abdominal spines are alternately longer or shorter than the adjacent spine (Gillespie, 2012).
3.2.2. Laboratory testing and other methods of identification
The DNA barcoding procedure based on the COI gene is reported in PM 7/129 ‘DNA barcoding for the identification of a number of regulated pests’ ( EPPO, 2021 ). The protocol can be used for all life stages of Aleurocanthus spp. to support morphological identification. However, molecular identification with the standard COI barcode is not providing reliable results due to the low capacity to discriminate different species (for details, see EPPO, 2022 ). The EPPO-Q-bank database (Bonants et al., 2013) contains 12 mtCOI sequences for A. spiniferus, but all of them originate from Italy, and 16 sequences for A. woglumi from Costa Rica and Malaysia. So far, only one sequence of A. citriperdus has been deposited in GenBank ( EPPO, 2022 ).
Conclusion on detection and identification in the laboratory
4. Conclusion
Information on what, where, when and how to conduct survey activities for Aleurocanthus spiniferus, A. woglumi and A. citriperdus is summarised in the Table on the right panel. The identification of the target population needs to be tailored to the situation in each Member State (example shown below).
5. Survey framework
The figure below shows the next steps after the survey preparation for designing statistically sound and risk-based detection and delimiting surveys of Aleurocanthus spiniferus, A. woglumi and A. citriperdus. Guidance on selecting the type of survey, related survey preparation and design, is provided in the the EFSA general guidelines for pest surveys on the right panel (EFSA et al., 2020).
Glossary
Scroll down the right panel to access the definitions included in the glossary.
Relevant EFSA outputs
Acknowledgments
EFSA wishes to thank the following for the support provided to this scientific output: Gritta Schrader of the Julius Kuehn Institute (JKI) in Germany and EFSA staff Sybren Vos for the preparation, Alan MacLeod for the review, and EFSA trainees Melanie Camilleri, Ramona Mihaela Ciubotaru and Makrina Diakaki for finalisation and publication of the first version of the survey card on Aleurocanthus spiniferus and Aleurocanthus woglumi (EFSA-Q-2018-00353).
EFSA wishes to thank Maria Chiara Rosace for the preparation of the first update of the survey card and the story map preparation (EFSA-Q-2020-00300) in the context of EFSA procurement PO/EFSA/ALPHA/2020/05.
EFSA also wishes to thank ISA expert Gabriele Rondoni (in the context of procedure EOI/EFSA/SCIENCE/2020/01) and EFSA staff Alice Delbianco for the preparation, Josep Jaques Miret for the review, and ISA expert Giulia Mattion (in the context of procedure EOI/EFSA/2022/01) for the finalisation and publication of this update of the pest survey card on Aleurocanthus spiniferus, A. woglumi and A. citriperdus (EFSA-Q-2023-00608).
Suggested citation: EFSA (European Food Safety Authority), 2024. Pest survey card on Aleurocanthus spiniferus, A. woglumi and A. citriperdus. EFSA supporting publication 2024:EN-8815. Available online: https://efsa.europa.eu/plants/planthealth/monitoring/surveillance/aleurocanthus-spiniferus-woglumi-citriperdus . Last updated: 14 May 2024.
Contact us: PLANTS@efsa.europa.eu
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