Eotetranychus lewisi

European Food Safety Authority (EFSA), Elena Lázaro, Pilar Vanaclocha, Antonio Vicent, Alice Delbianco

Updated 12 April 2023 ( Version 1 )

Abstract

This pest survey card was prepared in the context of the EFSA mandate on plant pest surveillance (M-2020-0114), at the request of the European Commission. Its purpose is to guide the Member States in preparing data and information for Eotetranychus lewisi surveys. These are required to design statistically sound and risk-based pest surveys, in line with current international standards. The Lewis spider mite, E. lewisi, is a clearly defined taxonomic entity and a Union quarantine pest. The introduction into the EU of some of the most relevant cultivated E. lewisi host plants is either regulated or prohibited, which is the case of citrus plants, while the import of citrus fruit is subject to some requirements. E. lewisi distribution in the EU territory is restricted to Portugal (Madeira and the mainland). This pest is highly polyphagous with a wide host range. The species Citrus limon (lemon), Citrus sinensis (sweet orange), Euphorbia pulcherrima (poinsettia), Fragaria x ananassa (strawberry), Prunus persica (peach), Rubus sp. (raspberry) and Vitis vinifera (vine) are the host species in the EU that are most relevant for detection surveys. Due to climatic similarities with the distribution area outside the EU and the widespread availability of hosts present both in open fields and in protected cultivation, larger parts of the EU are considered potentially suitable for its establishment. Long-distance spread is likely to occur through the movement of infested host plants. Detection in the field should be performed from mid–late summer to early–mid autumn by visual examination of symptoms followed by sampling. Guides for the morphological identification of E. lewisi adults are available and DNA-based methods are complementary. Based on the analyses of the information on the pest–host plant system, the various units that are needed to design a survey should be defined and tailored to the situation in each Member State.

© European Food Safety Authority, 2023

Heading picture: © EPPO Global Database, courtesy of Elke Mester (Landwirtschaftskammer Schleswig-Holstein, DE)

Authors' affiliation: Elena Lázaro, Instituto Valenciano de Investigaciones Agrarias (IVIA); Pilar Vanaclocha, Instituto Valenciano de Investigaciones Agrarias (IVIA); Antonio Vicent, Instituto Valenciano de Investigaciones Agrarias (IVIA); Alice Delbianco, European Food Safety Authority (EFSA).

Copyright for non-EFSA content: EFSA may include images or other content for which it does not hold copyright. In such cases, EFSA indicates the copyright holder and users should seek permission to reproduce the content from the original source.

The designations employed and the presentation of material on the maps in this document do not imply the expression of any opinion whatsoever on the part of the European Food Safety Authority concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries.


Introduction

The objective of this pest survey card is to provide the relevant information needed to prepare surveys for Eotetranychus lewisi (McGregor) (Acari: Prostigmata: Tetranychidae) 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 31: FAO, 2021b ) and surveillance guide ( FAO, 2021c ). 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 Eotetranychus lewisi

ii.            General documents:

b.    The statistical tools:  RiBESS+  and SAMPELATOR.

This pest survey card was prepared in the context of the EFSA mandate on plant pest surveillance (M-2020-0114) at the request of the European Commission. The information presented in this pest survey card was summarised from the EFSA Scientific Opinion on the pest categorisation of E. lewisi ( EFSA PLH Panel, 2014 ), the EFSA Pest risk assessment of E. lewisi for the EU territory ( EFSA PLH Panel, 2017 ), the European and Mediterranean Plant Protection Organization (EPPO) Global datasheet ( EPPO, online ) and reviewed literature.

The main challenges relevant for surveillance of E. lewisi are:

  • uncertainty about host range;
  • lack of information on the spread capacity;
  • difficult detection in the field.

1. The pest and its biology

1.1. Taxonomy

Current scientific name: Eotetranychus lewisi (McGregor) Class: Arachnida Subclass: Acari Order: Prostigmata Family: Tetranychidae Genus: Eotetranychus Species: Eotetranychus lewisi Synonym: Tetranychus lewisi EPPO Code:  EOTELE  Common name: Lewis spider mite, ácaro-da-poinsetia, ácaro-do-pessegueiro, araña roja del duraznero Taxonomic rank: species

Eotetranychus lewisi (figure below) is a clearly defined taxonomic entity (the taxonomy presented is according to Evans (1992)). However, the similarity between the names of the genera Eotetranychus and Eutetranychus, both including species that are pests of citrus, has been a source of confusion in the literature. A similar case occurs with the resemblance between the taxonomical names of Eotetranychus lewisi and Brevipalpus lewisi (McGregor, 1949) (Acari: Prostigmata: Tenuiplapidae), the citrus flat mite ( EPPO, 2022a ).

In the field, E. lewisi can be confused with Tetranychus urticae Koch (Acari: Prostigmata: Tetranychidae), a cosmopolitan species, as well as with different species of the genera Eotetranychus and Eutetranychus, which co occur on the same host plants (i.e., citrus). Several characteristics of common use in taxonomy clearly distinguish these two species ( EPPO, 2006 ).

Adults of of Eotetranychus lewisi (Source: © EPPO Global Database, courtesy of Jörg Schaller, LELF Brandenburg)

1.2. EU pest regulatory status

Eotetranychus lewisi is a Union quarantine pest listed in Annex II (Part A, Section 3. Insects and mites, point 31) of  Commission Implementing Regulation (EU) 2019/2072 .

The host range of E. lewisi is broad including both cultivated and wild species (see  Section 2.1  of this survey card for further details). The introduction into the Union territory of several host species (including plants of Citrus L., Fortunella Swingle, Poncirus Raf., and their hybrids, other than fruits and seeds) of E. lewisi is prohibited under Annex VI of  Commission Implementing Regulation (EU) 2019/2072 . Moreover, fruits of Citrus L., Fortunella Swingle, Poncirus Raf. and their hybrids introduced from third countries shall be free from peduncles and leaves and the packaging shall bear an appropriate origin mark, as detailed in point 57 of Annex VII of  Commission Implementing Regulation (EU) 2019/2072 .

Furthermore, special requirements for E. lewisi are laid down in Annex VII, point 24.1 for plants for planting of Euphorbia pulcherrima Willd., Fragaria L. and Rubus L., other than plants in tissue culture, pollen and seeds, introduced into the EU from third countries.

The general requirements for survey of quarantine pests in the EU territory are laid down in  Regulation (EU) 2016/2031  and  Commission Implementing Regulation (EU) 2020/1231 .

1.3. Pest distribution

The region of origin of E. lewisi is not known although it is thought to be native to Central America where this spider mite is known to occur naturally on native Euphorbia spp. According to EPPO (online), E. lewisi is present in Africa (Libya and South Africa), the Americas (Bolivia, Brazil, Canada, Chile, Colombia, Costa Rica, Ecuador, El Salvador, Guadeloupe, Guatemala, Honduras, Mexico, Nicaragua, Panama, Peru and the United States), Asia (Iran, Japan, the Philippines and Taiwan) and Europe (Portugal) (hyperlink on the right panel).

In the EU, E. lewisi was first detected in Madeira, on E. pulcherrima plants (poinsettias) in 1988 and on Vitis sp. in 1990. In the following 10 years, it was detected on Annona sp., and then again at different locations in Madeira between 2017 and 2019 ( EPPO, 2020 ). Although eradication measures were implemented, the pest was found in 2021 in continental Portugal (Algarve) on poinsettia plants in a flower bed in a private garden. Interestingly, the spider mite could not be found on other potential hosts (including citrus) present in the same garden (Naves et al., 2022). The current pest status of E. lewisi in Portugal is officially declared as: ‘present, under eradication, only in some parts of the Member State concerned’ ( EPPO, 2021a ). Additional EU countries where E. lewisi has been found infesting poinsettias in several greenhouses, include Germany ( EPPO, 2021b ), Poland (Labanowski, 2009;  EFSA PLH Panel, 2017 ) and the Netherlands ( EPPO, 2021c ,  2022b ; NPPO of the Netherlands, 2021). Eradication measures were successfully implemented in all these cases.

Eotetranychus lewisi was also detected on poinsettias in a greenhouse in the United Kingdom ( EPPO, 2014 ). This outbreak was eradicated ( EPPO, 2018 ). In 2021 this spider mite was detected on poinsettias in Switzerland. Official phytosanitary measures were taken and the pest status of E. lewisi in Switzerland has been officially declared to be ‘transient’ ( EPPO, 2021d ) (hyperlink on the right panel).

Note: the information included in this section is aligned with the EPPO map updated on 30-01-2023

1.4. Life cycle

The life cycle of E. lewisi comprises five stages: egg, larva, protonymph, deutonymph and adult (figure on the right panel). This species reproduces sexually and parthenogenetically and can complete at least six generations per year (Jeppson et al., 1975). The duration of the life cycle depends on the temperature. Under optimal conditions, a generation can be completed in just one to two weeks. E. lewisi do not enter diapause in the autumn and winter (British Columbia Ministry of Agriculture, 2020).

On most plant species E. lewisi is found feeding on theunderside of the leaves.

Both reproductive parameters and the longevity of E. lewisi are affected by the host plant species upon which it develops:

(i) On Euphorbia pulcherrima (poinsettia): Lai and Lin (2005) found mean generation times of 19.8, 16.7 and 13.2 days at 20, 24 and 28°C, respectively. The duration of the life cycle for females was 12.2, 16.0 and 9.6 days and 19.4, 12.3 and 7.9 days for males at 20, 24 and 28°C, respectively. The estimated degree-day accumulation from egg to adult was 159. The lower developmental temperature threshold has been estimated at 8.3–9.0°C, and the upper development threshold lies at 28.2°C. The time from egg deposition to hatching ranged between 2.5 and 8.1 days at 16–8°C while no egg hatching has been registered at or above 30°C. The estimated developmental time of the larva stage is 1.8-3.9 days for the same temperature range while developmental times of protonymph and deutonymph range from 1.4 to 2.9 and 2.3 to 4.1 days, respectively. Estimated fecundity at 20, 24 and 28°C is 20.7, 50.5 and 32.1 eggs, respectively.

(ii) On Citrus spp. (citrus): according to McGregor (1943), when E. lewisi was reared on tender Citrus limon (lemon) leaves at temperatures between 17 and 23°C, the time between oviposition and female emergence was estimated at 12 days. According to Jeppson et al (1975), the life cycle duration from egg to adult is 12.0 and 14.5 days for males and females, respectively, in the temperature range between 17 and 23°C. In this case, the average duration of each developmental stage was estimated at 6 days for egg incubation, 2 days for the larval stage, 2 days for the protonymph and another 2 days for the deutonymph. The life cycle of males was 2 days shorter than that of females ( EFSA PLH Panel, 2014 ) (figure on the right panel). The females started oviposition less than 24 h after emergence and deposited five eggs per day on average.

(iii) On Fragaria x ananassa (strawberry): the life cycle time on leaves decreases with increasing temperatures, varying between 32.7 and 10.6 days at a temperature range of 15–25°C. Maximum fecundity was observed at 25°C (Kaur and Zalom, 2017). On Prunus persica (peach): the life cycle from egg to adult was 16 days under controlled environmental conditions at 19°C (Miño et al., 2022).

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 E. lewisi within the EU is proposed in  Section 2.5 .

2.1. Host range and main hosts

Eotetranychus lewisi is a highly polyphagous spider mite with a wide host range that includes 89 herbaceous and woody plant species, belonging to 28 plant families (table below). The list of hosts includes both cultivated and wild species.

Cultivated hosts include Carica papaya (pawpaw), Citrus limon (lemon), C. sinensis (sweet orange), Euphorbia pulcherrima (poinsettia), Fragaria x ananassa (strawberry), Ficus carica (fig), Gossypium hirsutum (cotton), Prunus persica (peach), Olea europaea (olive), Ricinus communis (castor oil plant) Rubus sp. (raspberry) and Vitis vinifera (vine), among others. Within these species, the most relevant for the EU are lemon, sweet orange, poinsettia, strawberry, peach, raspberry and vine (EFSA PLH Panel,  2014 ,  2017 ).

Wild hosts include weeds, such as Solanum elaegnifolium (nightshade), and several tree species including Acacia spp. (acacia), Pinus ponderosa (pine) and Populus tremuloides (aspen) (EFSA PLH Panel,  2014 ,  2017 ).

Several plant species reported as hosts of E. lewisi are economically important crops and some are widely cultivated in the EU in either protected agricultural systems and/or in open fields (e.g. poinsettia, strawberry, peach). In addition, several hosts species are widely distributed throughout the EU territory in residential landscapes, as lemon ( EFSA PLH Panel, 2017 ).

It should be noted, however, that the report of a species as a host of E. lewisi does not necessarily mean that the spider mite is able to complete its life cycle on it or that it can cause economic damage to that specific host. Therefore, there is uncertainty regarding the exact host status of many species listed in the table below (EFSA PLH Panel,  2014 ,  2017 ).

Detection surveys could target cultivated host plants reported as the most relevant within the EU. Ideally, these would be lemon, sweet orange, poinsettia, strawberry, peach, vine and raspberry. Delimiting surveys following an outbreak should focus on all known host species present within the survey area.

Host plants reported for E. lewisi (according to EFSA PLH Panel ( 2014 ,  2017 ), Migeon and Dorkeld (2022),  EPPO (2022a)  and additional literature. For additional info see printable version)

2.2. Environmental suitability

The development and spread of E. lewisi populations are strongly mediated by environmental conditions, especially temperature. This abiotic factor has a direct relationship with key life-history traits of the spider mite such as its growth rate, survivorship, fecundity and egg hatching (Devi and Challa, 2019). As with other spider mites, this species is also favoured by conditions of low relative humidity, especially when they are paired with high temperatures. Low rainfall and high temperature therefore encourage spider mite outbreaks (Choudhury et al., 2006). The strong dependency of E. lewisi life-history traits on environmental factors results in a high seasonality for its population densities (Di Sabatinol et al., 2010).

In general, in open fields in regions with climates experiencing hot and dry periods, this pest finds perfect conditions for its development and can become a problem. In greenhouses, with controlled and stable temperatures, the development of E. lewisi may occur throughout the year, thus achieving a higher number of generations ( EFSA PLH Panel, 2017 ).

The climate of the countries where E. lewisi is present (see  Section 1.3 ) encompasses the main Köppen–Geiger climate types of the Mediterranean parts (Csa, Csb) and the continental part (Cfb, Cfa) of the EU (Kottek et al., 2006).  EFSA PLH Panel (2017)  generated maps indicating that, from the southern Mediterranean northwards into Sweden and Finland, large areas have minimum temperatures that are suitable for the completion of at least one generation of E. lewisi per year. However, these maps are theoretical, as they do not take into account the time it takes to accumulate the thermal sum for the development of one generation, and in nature adults survive only a few weeks. Therefore, it is in southern Europe, where multiple generations are possible, that establishment is most likely (figure on the right panel). Indeed, the pest is currently present in mainland Portugal (Algarve) with restricted distribution ( EPPO, online ).

As mentioned in the previous section, host plants of E. lewisi are widely available throughout the year and thus would not present a limiting factor for the establishment and spread of this spider mite in Europe. Thus, E. lewisi could become established in large parts of the EU, but mainly in the Mediterranean basin (EFSA PLH Panel,  2014 ,  2017 ).

2.3. Spread capacity

Natural spread

The wide range of hosts upon which E. lewisi develops helps the spider mite to spread and increases the risks of new infestations.

Spider mites can disperse over short distances relatively well, within the same plant or to neighbouring ones, by crawling at the speed of 5 cm to 6 m/h, and by dropping down on silk threads from infested leaves (Kennedy and Smitley, 1985; Margolies and Kennedy, 1985; NAPPO, 2014). This type of dispersion can be highly effective when hosts are growing close together, and the plant canopies are in contact.

Webbing produced by spider mites can also be a means of natural long-distance spread. Spider mites spin down on silk threads and can be carried on the wind (ballooning). Although no reports of this spread mechanism have been described for E. lewisi, ballooning is common within the Tetranychidae family. Studies about the wind-borne dispersal of another tetranychid thriving on citrus, Tetranychus urticae, found spread distances between 15 and 200 m (Quayle, 1916; Hoelscher, 1967; Hoy et al., 1984; Jung and Croft, 2001). This type of passive spread can take spider mites further away when prevailing winds are strong. The success though depends on whether the spider mite lands on a suitable host.

Human/animal-assisted spread

Spider mites can passively travel long distances by human and animal phoresis, such as via birds. After landing on heavily infested plants, birds are very likely to take off carrying some spider mites that can be transported to other hosts (Kennedy and Smitley, 1985;  EFSA PLH Panel, 2014 ; NAPPO, 2014). Ballooning spider mites can also be phoretic if the silk threads are carried away by humans or other animals (Brandenburg and Kennedy, 1982; Clotuche et al., 2011, 2013).

Spider mites can also easily move to new areas through transportation of infested plant material and human movement (attached to agricultural tools, clothes, etc.). The risk of inadvertent human spread of this pest is especially high owing to the minute size of this arthropod.

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 E. lewisi and is not necessarily exhaustive. 

For the identification of risk areas, it is first necessary to identify the activities that could contribute to introduction or spread of E. lewisi. 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.

Example 1: Import and trade of poinsettia, strawberry and raspberry plants for planting from countries where the pest occurs

Survey efforts should concentrate on activities that could potentially result in the introduction and spread of the pest. The import of poinsettia, strawberry and raspberry plants from countries where the pest occurs and the subsequent trade of this material within the EU territory may be identified as potential pathways of introduction and spread of E. lewisi ( EFSA PLH Panel, 2014 ). Although these pathways are subject to special requirements (see  Section 1.2 ), there are no restrictions on import to the EU as yet.

Poinsettia plants for planting seem to be the most likely pathway for introduction ( EFSA PLH Panel, 2017 ). This pathway includes both potted plants and cuttings ( EFSA PLH Panel, 2014 ). Poinsettia cuttings imported at the beginning of the year to obtain first-generation mother stock plants may host the pest. One of the key factors that could facilitate the spread of the pest is that poinsettia is a seasonal crop grown among other cultivated plants that can potentially host E. lewisi (Fransen, 1994). E. lewisi was reported ten years ago as an increasing concern on strawberry and raspberry in the USA (Howell and Daugovish, 2013). Importing strawberry plants and raspberry plants for planting from regions where the spider mite occurs therefore provides an additional potential pathway.

In line with this, nurseries and garden centres where poinsettias, strawberries, and raspberries are produced, stocked and/or distributed can be identified as risk locations. Surrounding areas where host plants are cultivated and/or propagated, or are present in natural landscapes, can be identified as risk areas.

Example 2: Import and trade of citrus fruit (oranges and lemons) from countries where the pest occurs

Eotetranychus lewisi is reported as having an impact on citrus fruit (lemons and oranges). Thus, the import and trade of oranges and lemons should be considered as a relevant pathway for the introduction and spread of E. lewisi, despite being subject to special requirements (see  Section 1.2 ) (EFSA PLH Panel,  2014 ,  2017 ). On citrus, the spider mites feed on the fruit and the eggs are laid mainly in the characteristic depressions on the fruit’s surface (Jeppson et al., 1975). The potential transfer of E. lewisi is therefore mainly related to the dispersal from discarded unmarketable whole fruit, fruit peel or citrus by-products, which are sometimes produced by citrus packing houses. A second relevant risk activity is related to the handling and processing of citrus fruit. Packing houses, processing plants, outdoor fruit-drying facilities, fresh fruit markets and livestock feeding areas can also be identified as risk locations. Surrounding areas where citrus plants or other alternative hosts are grown (as crops, ornamentals or as natural vegetation) can be identified as risk areas.

The table on the right panel schematises the identified risk activities for E. lewisi and their corresponding risk locations as described above. Different levels of risk could also be assigned to these locations considering an epidemiological criterion. The definition of risk areas around a certain risk location should take into consideration the spread capacity of E. lewisi and the availability of host plants, suggesting that areas of citrus orchards are of key interest. Geo-localising the risk locations (i.e. nurseries, garden centres, packing houses, neglected orchards, etc.) within the survey areas enables a detection survey to be designed and targeted accordingly even if these risk locations themselves are not going to be subject to that survey.

2.5. Structure of the target population

The figure on the right panel gives examples of the components of a target population for E. lewisi and is not necessarily exhaustive.

3. Detection and identification

Eotetranychus lewisi and its characteristic symptomatology can be detected by visual examination. Identification of the pest should be then confirmed in the lab by morphological identification of specimens, possibly followed by molecular tests.

3.1. Detection and identification in the field

3.1.1. Visual examination

Pest

Eotetranychus lewisi eggs are typically pearly, globular and with a tiny dorsal stipe (figure below, A) (Pritchard and Baker, 1955). The larvae have three pairs of legs, while the protonymphs, deutonymphs and adults have four pairs. The adult females have several small spots on their body and are larger than the males (360 and 270 μm long, respectively) (figure on the right panel, A). The body of the female is light yellow to whitish in colour and the legs and gnathosoma are whitish with a slight reddish tone (Ochoa et al., 1991;  EPPO, 2006 ).

Eotetranychus lewisi colonies can be present on most parts of the plant, mainly on the leaves and fruit depending on the phenological stage of the plant organ (Jeppson et al., 1975; Ochoa et al., 1994;  EPPO, 2006 ). On leaves, it feeds preferentially on the underside part, preferring the regions close to the main veins (figure on the right panel, B), forming small colonies with usually sparse webbing (Pritchard and Baker, 1955; Ochoa et al., 1994). As the infestation progresses, the colonies spread and spider mites occupy the whole underside of the leaves. On poinsettias, E. lewisi prefer to establish their colonies on mature leaves while on pawpaw, they use both the young and mature leaves ( EPPO, 2006 ). On strawberry and prunus, E. lewisi infests the undersides of leaves where feeding occurs and they may form colonies and produce light webbing when abundant (Howell and Daugovish, 2013; UC IPM, 2018; Miño et al., 2022). On citrus, the spider mites mostly feed on the fruit and the eggs are laid mainly in the characteristic depressions of the fruit’s surface (Jeppson et al., 1975).

Although visible to the naked eye, owing to their small size, all the stages of the spider mite are difficult to detect. This is especially important at the early stages of an infestation since at low densities they tend to hide under plant hairs, calyces, stipules and other plant structures. An examination of the underside of leaves with a hand lens can detect the presence of spider mites ( EPPO, 2022a ). However, the identification of the species can only be achieved by a specialist under microscopy examination in laboratory.

Risk of misidentification

Eotetranychus lewisi can be confused with other Eotetranychus spp. (Seeman et al., 2017). Some of them are also known to occur in the EU (E. carpini (Oudemans), E. kankitus Ehara, E. pruni (Oudemans), E. prunicola Livshits and E. tilliarium (Hermann)) but none of them feeds on citrus or on euphorbiaceae (Migeon and Dorkeld, 2022).

Eotetranychus lewisi also looks similar to the two-spotted spider mite, T. urticae, and to Eutetranychus orientalis (Klein). Both species are also present in the EU and are polyphagous. Their host range includes species which are also hosts of E. lewisi, like citrus. Therefore, the identification of E. lewisi requires microscopic examination of slide-mounted adults and verification of the presence of key morphological characteristics, including the morphology of the aedeagus ( EPPO, 2006 ; Vacante, 2010).

(A) Female and eggs of Eotetranychus lewisi on Euphorbia pulcherrima (poinsettia) and (B) female of Tetranychus urticae (Source: (A) © Rayanne Lehman, Pennsylvania Department of Agriculture, Bugwood.org; (B) ©  Gipcitiricos , IVIA)

Symptoms

As previously mentioned, E. lewisi usually feeds on the leaves of its host plants (i.e. peach, poinsettia, raspberry, strawberry and grapevine), except for citrus, where the existing literature indicates a preference for feeding on the fruit.

For colony detection, inspection should focus first on finding small whitish, brownish or yellow remains of exuviae and webbing that are abundant on already developed colonies present either on leaves or fruit (figure below).

On leaves, this spider mite pierces mesophyll cells with its stylet and absorbs the cell contents causing a characteristic stippled appearance (Ochoa et al., 1994; Park and Lee, 2002). As the infestation progresses, E. lewisi spread to all parts of the leaf as well as the upper surface. This spider mite’s feeding causes mechanical injury, which results in a wide range of morphological and physiological plant responses, including changes in photosynthetic activity (Pérez-Santiago et al., 2007; Muimba-Kankolongo, 2018). At high densities, this pest usually causes chlorosis and bronzing of leaves (second figure below, A and B), webbing and reduction in fruit production (Howell and Daugovish, 2013; Kaur and Zalom, 2017). Eventually the entire leaf becomes bleached and falls off ( EFSA PLH Panel, 2014 ; British Columbia Ministry of Agriculture, 2020).

On citrus fruit, the feeding by E. lewisi results in stippling on the rind (McGregor, 1943). Heavy infestations cause silvering on lemons and oranges and russeting on oranges (Jeppson et al., 1975). This spider mite produces large quantities of webbing in its colonies, which collect dust and make infestations highly visible ( EFSA PLH Panel, 2014 ).

Characteristic appearance of Eotetranychus lewisi colonies (Source: © Droul Drove, inaturalist.org)

Euphorbia pulcherrima (poinsettia) leaves with characteristic feeding damage (yellow punctures) of Eotetranychus lewisi and without it (Source: © Dan Gilrein, Cornell Cooperative Extension of Suffolk County, NY USA)

3.1.2. Sample collection

There are two ways to collect spider mites in the field:

  • Visual sampling, the visual examination of leaves or fruit, is considered to be the most effective method for spider mite detection. The use of a hand lens will make identifications in the field easier. When no suspicious specimens or symptoms are observed, sampling should be addressed by making random checks of the sampling matrix (i.e. leaves or fruit). Owing to the ecological requirements of this species, the leaves and fruit of the outer parts of the south-facing plant canopy, and in plants close to the borders of planted groves, are most likely to harbour spider mite colonies. When suspicious specimens and/or compatible symptoms are observed, symptomatic samples must be taken. Samples should be taken to the laboratory in refrigerated plastic bags containing absorbent paper to avoid excess moisture.

In the laboratory, the samples can be inspected under a binocular stereoscope to confirm pest presence. If found, specimens should be recovered using a moist and fine brush for further species determination under the microscope. Alternatively, the samples can be placed in a large jar or sealed plastic bag filled with alcohol or soapy water. The jar/bag should be shaken and left for >1 h to help dislodge the spider mites. The liquid suspension should then be sieved through a 40–50 µm mesh to recover the specimens. In either case, if samples are not going to be examined soon, they should be stored at about 5°C to keep specimens alive for several days (NAPPO, 2014).

  • Tap sampling consists of tapping the foliage of the plant canopy, so that if spider mites are present, they will fall off into a funnel leading to a collecting jar containing 70–95% alcohol, or onto a black or white plastic tray where they can be picked up with a fine, moist brush (NAPPO, 2014).

When specimens are recovered, they should be placed in Eppendorf tubes containing 70–95% alcohol for further taxonomic determination or DNA extraction (NAPPO, 2014).

3.1.3. Timing of detection and identification

Owing to E. lewisi polyphagy ( Section 2.1 ), the exact timing of the surveys will depend both on the targeted host plant and the environmental conditions in the survey area. This will differ between Member States.

Calendars proposed for other tetranychid species sharing similar ecological requirements with E. lewisi, such as T. urticae, Panonychus citri, Eutetranychus banksii or Eutetranychus orientalis, can be used as a model ( http://gipcitricos.ivia.es/ ).

In open-field crops such as citrus, E. lewisi infestations are expected to occur from mid–late summer to early–mid autumn; therefore, visual examination from the second half of August until the end of October is recommended. In years experiencing hot and dry springs, infestations may begin earlier in the season, thus visual examinations should start at the end of spring (second half of May). Due to the short life cycle of this pest, a weekly/bi-weekly frequency is suggested.

In protected groves, the surveillance schedule should be adapted to the cropping calendars of the target crop.

3.2. Detection and identification in the laboratory

3.2.1. Morphological identification

The taxonomical identification of E. lewisi is based on the observation of morphological characteristics by microscopic examination of cleared and mounted male adult specimens. Spider mite identity should be established using morphological keys for the genus Eotetranychus (Vacante, 2010). The EPPO diagnostic standard PM 7/124 (1) ( EPPO, 2006 ) describes the procedures to identify this species. This standard provides a detailed description of the main morphological characteristics that should be considered to identify the genus Eotetranychus as well as the unique characteristics of this species. Specifically, this EPPO standard remarks that morphological identification of E. lewisi is only possible from adult male specimens positioned laterally as the distinguishing characters are found on the shape of aedeagus which presents a gentle sigmoid bend without a distinct distal knob or tip (figure on the right panel and figure below).

Aedeagus of adult male of Eotetranychus lewisi (Source: © EPPO Global Database, courtesy of Jean-François Germain, LNPV Entomologie, Montpellier (FR))

3.2.2. Laboratory testing and other methods of identification

DNA-based methods are available to discriminate between this and other tetranychid species. This approach is especially useful since classical taxonomy is only based on male adults and, sometimes they are hard to find. Naves et al. (2021) describes a molecular protocol to identify E. lewisi adults.

The pair of primers ITS2-F (5'GTCACATCTGTCTGAGAGTTGAGA3') and ITS2-R (5'GTARCCTCACCTRMTCTGAGATC3') can be used for ITS2 amplifications (Ben-David et al., 2007; Mirza et al., 2020), whereas COI-F (5'TTYGAYCCWAGAGGAGGAGG3') and COI- R (5'AAACCTARAAAATGTTGWGG3') can be used for COI amplifications (Matsuda et al., 2013). Recommended PCR cycling conditions are described by Mirza et al. (2020).

The ITS2 region (447 bp) and COI region (530 bp) sequences for E. lewisi are available in the GenBank database (NCBI) with accession numbers MW524105.1 and MW538648.1, respectively.

4. Conclusion

Information on whatwherewhen and how to conduct survey activities for E. lewisi 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 E. lewisi. 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.

Acknowledgments

EFSA wishes to acknowledge the following for the support provided to this scientific output: the Instituto Valenciano de Investigaciones Agrarias (IVIA) in the context of the grant GP/EFSA/ALPHA/2021/08 for the preparation, Josep Jaques Miret for the review, EFSA trainee Marina Elena Martino and ISA expert Giulia Mattion (in the context of contract EOI/EFSA/SCIENCE/2020/01) for the finalisation and publication of this survey card.

Suggested citation: EFSA (European Food Safety Authority), Elena Lázaro, Pilar Vanaclocha, Antonio Vicent, Alice Delbianco, 2023. Pest survey card on Eotetranychus lewisi. EFSA supporting publication 2023:EN-7966. Available online:  https://efsa.europa.eu/plants/planthealth/monitoring/surveillance/eotetranychus-lewisi . Last updated: 12 April 2023.


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Adults of of Eotetranychus lewisi (Source: © EPPO Global Database, courtesy of Jörg Schaller, LELF Brandenburg)

Host plants reported for E. lewisi (according to EFSA PLH Panel ( 2014 ,  2017 ), Migeon and Dorkeld (2022),  EPPO (2022a)  and additional literature. For additional info see printable version)

(A) Female and eggs of Eotetranychus lewisi on Euphorbia pulcherrima (poinsettia) and (B) female of Tetranychus urticae (Source: (A) © Rayanne Lehman, Pennsylvania Department of Agriculture, Bugwood.org; (B) ©  Gipcitiricos , IVIA)

Characteristic appearance of Eotetranychus lewisi colonies (Source: © Droul Drove, inaturalist.org)

Euphorbia pulcherrima (poinsettia) leaves with characteristic feeding damage (yellow punctures) of Eotetranychus lewisi and without it (Source: © Dan Gilrein, Cornell Cooperative Extension of Suffolk County, NY USA)

Aedeagus of adult male of Eotetranychus lewisi (Source: © EPPO Global Database, courtesy of Jean-François Germain, LNPV Entomologie, Montpellier (FR))