The new Plant Health Regulation (EU) 2016/2031, on the protective measures against pests of plants, is applying from 14 December 2019. Conditions are laid down in this legislation in order for pests to qualify for listing as Union quarantine pests, protected zone quarantine pests or Union regulated non-quarantine pests. The lists of the EU regulated pests together with the associated import or internal movement requirements of commodities are included in Commission Implementing Regulation (EU) 2019/2072. Additionally, as stipulated in the Commission Implementing Regulation 2018/2019, certain commodities are provisionally prohibited to enter in the EU (high risk plants, HRP). EFSA is performing the risk assessment of the dossiers submitted by exporting to the EU countries of the HRP commodities, as stipulated in Commission Implementing Regulation 2018/2018. Furthermore, EFSA has evaluated a number of requests from exporting to the EU countries for derogations from specific EU import requirements.
In line with the principles of the new plant health law, the European Commission with the Member States are discussing monthly the reports of the interceptions and the outbreaks of pests notified by the Member States. Notifications of an imminent danger from pests that may fulfil the conditions for inclusion in the list of the Union quarantine pest are included. Furthermore, EFSA has been performing horizon scanning of media and literature.
As a follow-up of the above-mentioned activities (reporting of interceptions and outbreaks, HRP, derogation requests and horizon scanning), a number of pests of concern have been identified. EFSA is requested to provide scientific opinions for these pests, in view of their potential inclusion by the risk manager in the lists of Commission Implementing Regulation (EU) 2019/2072 and the inclusion of specific import requirements for relevant host commodities, when deemed necessary by the risk manager.
Terms of ReferenceEFSA is requested, pursuant to Article 29(1) of Regulation (EC) No 178/2002, to provide scientific opinions in the field of plant health.
EFSA is requested to deliver 53 pest categorisations for the pests listed in Annex 1A, 1B, 1D and 1E (for more details see mandate M-2021-00027 on the Open.EFSA portal). Additionally, EFSA is requested to perform pest categorisations for the pests so far not regulated in the EU, identified as pests potentially associated with a commodity in the commodity risk assessments of the HRP dossiers (Annex 1C; for more details see mandate M-2021-00027 on the Open.EFSA portal). Such pest categorisations are needed in the case where there are not available risk assessments for the EU.
When the pests of Annex 1A are qualifying as potential Union quarantine pests, EFSA should proceed to phase 2 risk assessment. The opinions should address entry pathways, spread, establishment, impact and include a risk reduction options analysis.
Additionally, EFSA is requested to develop further the quantitative methodology currently followed for risk assessment, in order to have the possibility to deliver an express risk assessment methodology. Such methodological development should take into account the EFSA Plant Health Panel Guidance on quantitative pest risk assessment and the experience obtained during its implementation for the Union candidate priority pests and for the likelihood of pest freedom at entry for the commodity risk assessment of High Risk Plants.
Interpretation of the Terms of ReferenceNilaparvata lugens is one of a number of pests listed in Annex 1D to the Terms of Reference (ToR) to be subject to pest categorisation to determine whether it fulfils the criteria of a potential Union quarantine pest (QP) for the area of the EU excluding Ceuta, Melilla and the outermost regions of Member States referred to in Article 355(1) of the Treaty on the Functioning of the European Union (TFEU), other than Madeira and the Azores, and so inform EU decision making as to its appropriateness for potential inclusion in the lists of pests of Commission Implementing Regulation (EU) 2019/2072. If a pest fulfils the criteria to be potentially listed as a Union QP, risk reduction options will be identified.
Additional informationThis pest categorisation was initiated as a result of media monitoring, PeMoScoring1 (EFSA, 2022), and subsequent discussion at the Standing Committee on Plants, Animals, Food and Feed, resulting in it being included in the current mandate within the list of pests identified by horizon scanning and selected for pest categorisation.
Data and methodologies Data Literature searchA literature search on N. lugens was conducted at the beginning of the categorisation in the ISI Web of Science bibliographic database, using the scientific name of the pest as search term. Papers relevant for the pest categorisation were reviewed, and further references and information were obtained from experts, as well as from citations within the references and grey literature.
Database searchPest information, on host(s) and distribution, was retrieved from the European and Mediterranean Plant Protection Organization (EPPO) Global Database (EPPO, online), the CABI databases and scientific literature databases as referred above in Section 2.1.1.
Data about the import of commodity types that could potentially provide a pathway for the pest to enter the EU and about the area of hosts grown in the EU were obtained from EUROSTAT (Statistical Office of the European Communities).
The Europhyt and TRACES databases were consulted for pest-specific notifications on interceptions and outbreaks. Europhyt is a web-based network run by the Directorate General for Health and Food Safety (DG SANTÉ) of the European Commission as a subproject of PHYSAN (Phyto-Sanitary Controls) specifically concerned with plant health information. TRACES is the European Commission's multilingual online platform for sanitary and phytosanitary certification required for the importation of animals, animal products, food and feed of non-animal origin and plants into the European Union, and the intra-EU trade and EU exports of animals and certain animal products. Up until May 2020, the Europhyt database managed notifications of interceptions of plants or plant products that do not comply with EU legislation, as well as notifications of plant pests detected in the territory of the Member States and the phytosanitary measures taken to eradicate or avoid their spread. The recording of interceptions switched from Europhyt to TRACES in May 2020.
GenBank was searched to determine whether it contained any nucleotide sequences for N. lugens which could be used as reference material for molecular diagnosis. GenBank® (
The Panel performed the pest categorisation for N. lugens, following guiding principles and steps presented in the EFSA guidance on quantitative pest risk assessment (EFSA PLH Panel, 2018), the EFSA guidance on the use of the weight of evidence approach in scientific assessments (EFSA Scientific Committee, 2017) and the International Standards for Phytosanitary Measures No. 11 (FAO, 2013).
The criteria to be considered when categorising a pest as a potential Union quarantine pest (QP) is given in Regulation (EU) 2016/2031 Article 3 and Annex I, Section 1 of the Regulation. Table 1 presents the Regulation (EU) 2016/2031 pest categorisation criteria on which the Panel bases its conclusions. In judging whether a criterion is met the Panel uses its best professional judgement (EFSA Scientific Committee, 2017) by integrating a range of evidence from a variety of sources (as presented above in Section 2.1) to reach an informed conclusion as to whether or not a criterion is satisfied.
Table 1 Pest categorisation criteria under evaluation, as derived from Regulation (EU) 2016/2031 on protective measures against pests of plants (the number of the relevant sections of the pest categorisation is shown in brackets in the first column)
| Criterion of pest categorisation | Criterion in Regulation (EU) 2016/2031 regarding Union quarantine pest (Article 3) |
| Identity of the pest (Section 3.1) | Is the identity of the pest clearly defined, or has it been shown to produce consistent symptoms and to be transmissible? |
| Absence/presence of the pest in the EU territory (Section 3.2) |
Is the pest present in the EU territory? If present, is the pest in a limited part of the EU or is it scarce, irregular, isolated or present infrequently? If so, the pest is considered to be not widely distributed. |
| Pest potential for entry, establishment and spread in the EU territory (Section 3.4) | Is the pest able to enter into, become established in, and spread within, the EU territory? If yes, briefly list the pathways for entry and spread. |
| Potential for consequences in the EU territory (Section 3.5) | Would the pests' introduction have an economic or environmental impact on the EU territory? |
| Available measures (Section 3.6) | Are there measures available to prevent pest entry, establishment, spread or impacts? |
| Conclusion of pest categorisation (Section 4) | A statement as to whether (1) all criteria assessed by EFSA above for consideration as a potential quarantine pest were met and (2) if not, which one(s) were not met. |
The Panel's conclusions are formulated respecting its remit and particularly with regard to the principle of separation between risk assessment and risk management (EFSA founding regulation (EU) No 178/2002); therefore, instead of determining whether the pest is likely to have an unacceptable impact, deemed to be a risk management decision, the Panel will present a summary of the observed impacts in the areas where the pest occurs, and make a judgement about potential likely impacts in the EU. While the Panel may quote impacts reported from areas where the pest occurs in monetary terms, the Panel will seek to express potential EU impacts in terms of yield and quality losses and not in monetary terms, in agreement with the EFSA guidance on quantitative pest risk assessment (EFSA PLH Panel et al., 2018). Article 3 (d) of Regulation (EU) 2016/2031 refers to unacceptable social impact as a criterion for QP status. Assessing social impact is outside the remit of the Panel.
Pest categorisation Identity and biology of the pest Identity and taxonomy
Is the identity of the pest clearly defined, or has it been shown to produce consistent symptoms and/or to be transmissible?
Yes, the identity of the species is established and Nilaparvata lugens (Stål) is the accepted name.
N. lugens (Stål) is an insect within the Order Hemiptera and Family Delphacidae. It is commonly known as the brown planthopper. It was first described as Delphax lugens Stål in 1854 and synonyms include Delphax sordescens Motschulsky, Liburnia oryzae (Matsumura), Nilaparvata oryzae (Matsumura) (EPPO, online; Dmitriev, 2019).
There are two N. lugens forms feeding on cultivated and wild rice, which differ in mating signals and DNA sequences, and they may represent sibling species. N. lugens populations appear to contain abundant polygenic variation for host-associated traits. The physiological and behavioural strains are referred to as ‘biotypes’ (Sezer and Butlin, 1998). Reports of N. lugens feeding on Leersia hexandra are referable to a different species (Claridge et al., 1985; Ferrater, 2015 and references cited therein).
The EPPO code2 (Griessinger and Roy, 2015; EPPO, 2019) for this species is: NILALU (EPPO, online).
Biology of the pestN. lugens is a plant phloem sap feeder infesting rice (Oryza sativa). It can complete 12 generations in a single year in tropical areas, where it resides year-round, and fewer generations in temperate areas, where it is a migratory pest (Stout, 2014). It cannot overwinter in temperate and subtropical regions (such as mainland China, Japan and the Korean Peninsula) (Chen et al., 1979; Kisimoto and Sogawa, 1995) because winter climate is not suitable both for the insect and rice cultivation, thus N. lugens must engage in long-distance migratory flights to overwinter in warmer permanent breeding areas (Peng et al., 2012).
N. lugens acts as the vector of two important plant viruses: the rice grassy stunt virus (Tymoviridae; Tymovirus) and the rice ragged stunt virus (Reoviridae; Oryzavirus) (Mochida and Okada, 1979; Saxena and Khan, 1989).
The brown planthopper is dimorphic, with fully winged ‘macropterous’ and truncate-winged ‘brachypterous’ forms. The macropterous forms are potentially migrants and are responsible for colonising new fields. Long-distance return migrations occur in China in mid and late September, with N. lugens being carried on the prevailing wind towards overwintering areas; mass take-off occurs in the late afternoon or at dusk and then the migrants fly for several hours during the evening, at heights between about 400 and 1,000 m above ground with an air temperature limit of about 16°C. The distance covered can be up to 240 km. In the presence of strong winds (i.e. 12 m/s) migrants could conceivably travel as much as 500 km in one night's flight (Riley et al., 1991). After settling on rice plants, they produce the following generation, where most of the female insects develop as brachypterous and males as macropterous. Adults usually mate on the day of emergence, and the females start laying eggs from the day following mating. Oviposition usually occurs in the leaf sheath tissues near the rice plant base or in the ventral midribs of leaf blades. The eggs are laid in masses of 1–27 eggs each, arranged in 2 straight lines. The average number of eggs laid is 244.2 per female. At 29°C this average declined to 86.8 and at 33°C no oviposition occurred (Bae and Pathak, 1970). The most favourable temperatures for the survival and reproduction of N. lugens ranges from 25°C to 30°C (Bae and Pathak, 1970; Kumar et al., 2022). Both male and female planthoppers had the longest life spans at 25°C; at higher temperatures the longevity of females declined considerably. At 33°C the average longevity of male and female planthoppers was 3.9 and 4.1 days, respectively, as compared with 11.6 and 18.6 days at 25°C (Bae and Pathak, 1970). In the Northern Hemisphere, the brown planthopper could overwinter only in south of isotherm of 10°C in January (Hu et al., 2018; Guru-Pirasanna-Pandi et al., 2021). In terms of relative humidity, the highest survival rate of N. lugens nymphs was recorded at 70% RH and the pest infestation was significantly positively correlated with the RH values (Sharma et al., 2018). Fecundity of N. lugens was significantly higher with a higher leaf nitrogen content; besides, fecundity, hatching rate, adult longevity and development duration were seen to be significantly influenced by the rice variety (Kumar et al., 2022). The nymphs hatch in 7–9 days; the newly hatched nymphs are cottony-white, and turn purple-brown within an hour. They feed on plant sap and pass through five instars before becoming adults. The nymphal period varies between 12 and 15 days and the adults usually live for about 10–21 days (Kumar et al., 2022). In some cases, N. lugens lay eggs in the rice seed beds (rice nurseries) shortly before transplanting, so they enter the field in this manner (Preap et al., 2002).
N. lugens is known to be able to develop resistance both to insecticides which have been widely used for controlling the pest (Zhang et al., 2016; Fang et al., 2018; Wu et al., 2018) and to N. lugens-resistant rice varieties (Sezer and Butlin, 1998). Indeed, outbreaks of brown planthopper became more frequent and more intense after the introduction of improved rice varieties and input-intensive farming practices during the green revolution of the 1960s (Kumar et al., 2022). The increased importance of the brown planthopper as a pest prompted efforts to identify sources of planthopper resistance (Stout, 2014).
Several natural enemies are known to feed on this species. Predators include the
Numerous parasitoids belonging to the orders Strepsiptera, Diptera and, especially, Hymenoptera have been found developing on N. lugens in Asia with highly variable levels of field parasitism between parasitoid species and locations (Gurr et al., 2011). For example, studies in Peninsular Malaysia found total egg mortality to be as high as 92% for N. lugens with parasitoids being responsible for 68% of this mortality (Watanabe et al., 1992) (Table 2).
Table 2 Important features of the life history strategy of
| Life stage | Phenology and relation to host | Other relevant information |
| Egg | Eggs are laid in masses of 1 to 27 eggs each, all year round in tropical areas, in the leaf sheath tissues near the plant base or in the ventral midribs of leaf blades. The average number of eggs laid is 244.2 per female. They can also be laid in rice seed beds before transplanting. | The nymphs hatch in 7–9 days |
| Nymph | Newly hatched nymphs are cottony-white and turn purple-brown within an hour. |
They feed on plant sap and pass through five instars before becoming adults. The mean Critical Thermal maximum of nymphs was 34.9°C; the Heat Coma Temperature was 37.7°C. The Upper Lethal Temperature was 41.8°C (Piyaphongkul et al., 2012a, b). |
| Adult | Adults are fully winged (macropterous) or truncate-winged (brachypterous). |
The macropterous forms are potentially migrants and are responsible for colonising new fields. After settling on rice plants, they produce the following generation, where most of the female insects develop as brachypterous and males as macropterous. Adults usually mate on the day of emergence, and the females start laying eggs from the day following mating. The mean critical thermal maximum of adult females and males were 37.0°C and 37.4°C, respectively; the heat coma temperatures were 43.5°C and 42.0°C. The upper lethal temperature value for adults was 42.5°C (Piyaphongkul et al., 2012a, b). |
N. lugens feeds and reproduces on rice. It can use many rice varieties as a host plant and can adapt rapidly to resistant varieties (Den Hollander and Pathak, 1981). Some wild Oryza species in Asia were reported as field hosts for N. lugens, but there are no published studies on this topic (CABI, online). N. lugens has been reported also on Leersia hexandra, a genus occurring in the EU. However, bioassays and molecular studies have indicated that populations feeding on rice and feeding on the weed L. hexandra represent distinct species (sibling species or cryptic species) (Claridge et al., 1985, Ferrater, 2015 and references cited therein). Kumar et al. (2020) citing Jones et al. (1996) report that N. lugens is believed to have undergone a host shift from Leersia plants to rice about 0.25 million years ago. Subsequently, N. lugens evolved as a monophagous insect, which selectively feeds on rice plants (Jing et al., 2017; Zhao et al., 2016).
Intraspecific diversityThe two N. lugens forms feeding on cultivated and wild rice, differ in mating signals and DNA sequences and may represent sibling species. N. lugens populations appear to contain abundant polygenic variation for host-associated traits. The physiological and behavioural strains are referred to as ‘biotypes’ (Sezer and Butlin, 1998).
Detection and identification of the pest
Are detection and identification methods available for the pest?
Yes, visual detection is possible, and morphological and molecular identification methods are available.
Detection
N. lugens adults and nymphs suck the plant phloem of the leaf blades and leaf sheaths causing yellowing of the plants. At early infestation, circular yellow patches appear which soon turn brownish due to the drying up of the plants. N. lugens is usually more abundant and therefore more easily detected in the dry season than in the wet season. It is commonly found in rain-fed and irrigated fields during the reproductive stage of the rice plant. Hopperburn caused by the plant hoppers is distinguished from other hopperburn symptom by the presence of visible sooty moulds at the base of the rice plant (TNAU, 2023). The grain setting is also affected to a great extent. Plant-shaking and light traps can be used to detect this planthopper (Hu et al., 2014). Hyperspectral remote sensing was also used to detect plants damaged by this pest (Prasannakumar et al., 2013).
SymptomsThe main symptoms of N. lugens infestation are:
- yellowing of the plants,
- leaves initially turn orange-yellow before becoming brown and dry; this condition is called hopperburn and kills the plant,
- during sustained feeding, it excretes a large amount of honeydew.
These symptoms are similar to those caused by other plant-sap feeding insects and should not be considered as diagnostic.
IdentificationThe identification of N. lugens requires microscopic examination of slide mounted adult male specimens. Morphological keys are available for specific identification (Wilson and Claridge, 1991). However, no taxonomic keys for the nymphal stage are available (Caro et al., 2015).
Molecular techniques based on multiplex PCR and loop-mediated isothermal amplification (LAMP) have been developed for species identification (Rahman et al., 2023). The complete assembled (chromosome level) genome (including mtDNA) of N. lugens is available (King et al., 2023).
DescriptionEggs are white, transparent, slender cylindrical with broad flat egg caps and are laid in straight-line in two rows in leaf sheath near the plant base or in the ventral midribs of leaf blades. They are covered with a dome-shaped egg plug secreted by the female. Only the tips protrude from the plant surface.
Nymph – Freshly hatched nymph is cottony white, 0.6 mm long and it then turns purple-brown in later stages. In the fifth instar, it is 3.0 mm long.
Adult – Adult hopper is 4.5–5.0 mm long and has a yellowish brown to dark brown body. It has two characteristic wing morphs: macropterous (long winged) and brachypterous (short winged). The wings are subhyaline with a dull yellowish tint.
Pest distribution Pest distribution outside theN. lugens is native to Asia, where it is widely distributed, and naturalised in Oceania (EPPO, online; CABI, online) (Figure 1). For a detailed list of countries where N. lugens is present, see Appendix B.
Enlarge this image.Figure 1. : Global distribution of Nilaparvata lugens (Copyright: EPPO Global Database accessed on 13 March 2023)
Is the pest present in the EU territory? If present, is the pest in a limited part of the EU or is it scarce, irregular, isolated or present infrequently? If so, the pest is considered to be not widely distributed.
No, N. lugens is not known to be present in the EU.
Regulatory status Commission Implementing Regulation 2019/2072
N. lugens is not listed in Annex II of Commission Implementing Regulation (EU) 2019/2072, an implementing act of Regulation (EU) 2016/2031, or in any emergency plant health legislation.
Hosts or species affected that are prohibited from entering the union from third countries (Table 3)Table 3 List of plants, plant products and other objects that are
| List of plants, plant products and other objects whose introduction into the Union from certain third countries is prohibited | |||
| Description | CN code | Third country, group of third countries or specific area of third country | |
| 14. | Plants for planting of the family Poaceae, other than plants of ornamental perennial grasses of the subfamilies Bambusoideae and Panicoideae and of the genera Buchloe, Bouteloua Lag., Calamagrostis, Cortaderia Stapf., Glyceria R. Br., Hakonechloa Mak. ex Honda, Hystrix, Molinia, Phalaris L., Shibataea, Spartina Schreb., Stipa L. and Uniola L., other than seeds | ex 0602 90 50 ex 0602 90 91 ex 0602 90 99 | Third countries other than Albania, Algeria, Andorra, Armenia, Azerbaijan, Belarus, Bosnia and Herzegovina, Canary Islands, Egypt, Faeroe Islands, Georgia, Iceland, Israel, Jordan, Lebanon, Libya, Liechtenstein, Moldova, Monaco, Montenegro, Morocco, North Macedonia, Norway, Russia (only the following parts: Central Federal District (Tsentralny federalny okrug), Northwestern Federal District (Severo- Zapadny federalny okrug), Southern Federal District (Yuzhny federalny okrug), North Caucasian Federal District (Severo-Kavkazsky federalny okrug) and Volga Federal District (Privolzhsky federalny okrug)), San Marino, Serbia, Switzerland, Syria, Tunisia, Türkiye, Ukraine and the United Kingdom |
The viruses vectored by N. lugens (rice grassy stunt virus and rice ragged stunt virus) are not regulated in the EU, while they are both quarantine in the USA (EPPO, online).
Entry, establishment and spread in the
Is the pest able to enter into the EU territory? If yes, identify and list the pathways.
Yes, possible but very unlikely. If host plants were imported as fresh cut or plants for planting, they could provide an entry pathway for this species. However, there is no evidence that such trade exists.
Comment on plants for planting as a pathway.
Plants for planting include seeds. On a commercial scale N. lugens host plants are planted mainly as seeds. However, seeds do not provide a pathway for this pest.
The EU does import rice from regions where N. lugens is known to occur, however this is rice as grains (wholly milled or semi-milled, broken, in the husk and husked) and not rice plants for planting or cut rice plants. In the EU, rice is mainly drilled as seed into production sites (Kraehmer et al., 2017); when transplanted as seedlings, the seedlings are sourced locally. Table 4 shows two hypothetical pathways. However, there is no evidence that hosts are traded as growing or cut plants. Immature and adult planthoppers are highly mobile, departing plants when disturbed and are likely to hop off plants at origin and so not be transported on traded plants. Planthoppers in general are infrequently intercepted relative to other families in Hemiptera (Turner et al., 2021).
Table 4 Potential pathways for
| Pathways (e.g. host/intended use/source) | Life stage | Relevant mitigations [e.g. prohibitions (Annex VI), special requirements (Annex VII) or phytosanitary certificates (Annex XI) within Implementing Regulation 2019/2072] |
| Freshly cut host plants | Eggs, nymphs, adults | No prohibitions nor special requirements are in place |
| Hitchhiking | Nymphs, adults | No prohibitions nor special requirements are in place |
Entry to the EU via migration is unlikely given the distance from tropical rice growing areas.
Notifications of interceptions of harmful organisms began to be compiled in Europhyt in May 1994 and in TRACES in May 2020. As at 8.3.2023, there were no records of interception of N. lugens in the Europhyt and TRACES databases. Note that because N. lugens is not a quarantine pest, member states are not obliged to notify findings to plant health authorities.
Establishment
Is the pest able to become established in the EU territory?
No. N. lugens cannot overwinter in temperate or subtropical climates and the lack of rice growing in the EU from autumn until spring further reduces the likelihood of establishment. For these reasons, it is very unlikely to become established in the EU territory.
Climatic mapping is the principal method for identifying areas that could provide suitable conditions for the establishment of a pest taking key abiotic factors into account (Baker, 2002). Availability of hosts is considered in Section 3.4.2.1. Climatic factors are considered in Section 3.4.2.2.
The host of N. lugens is rice, a crop cultivated in the EU (Table 5).
Table 5 Harvested area of rice (Code: C2000 × 1,000 ha) in the EU, 2016–2020. (Source: Eurostat, accessed on 17 February 2023)
| MS/Year | 2016 | 2017 | 2018 | 2019 | 2020 |
| EU | 448.74 | 440.68 | 417.37 | 419.09 | 427.55 |
| Bulgaria | 11.99 | 10.43 | 11.00 | 11.82 | 12.35 |
| Greece | 35.14 | 30.95 | 30.35 | 29.86 | 36.09 |
| Spain | 109.27 | 107.60 | 105.01 | 103.37 | 102.06 |
| France | 16.71 | 16.72 | 13.28 | 15.10 | 14.81 |
| Italy | 234.13 | 234.13 | 217.19 | 220.03 | 227.32 |
| Hungary | 2.91 | 2.77 | 2.93 | 2.65 | 2.99 |
| Portugal | 29.15 | 28.94 | 29.35 | 28.83 | 25.94 |
| Romania | 9.44 | 9.13 | 8.25 | 7.43 | 6.00 |
Even in the warmest areas of the EU where rice is grown, rice planting starts around May and is harvested around October. The host is therefore not available for about 7 months, from October until May the following year, inhibiting the likelihood of establishment.
Climatic conditions affecting establishmentAlthough rice is grown in the EU, it is not present year-round and EU climates further limit the establishment of this tropical species. Figure 2 shows the distribution of selected EU Köppen–Geiger climate types (Kottek et al., 2006) that occur in the EU and in regions where N. lugens has been reported (shown by red dots). Recall that N. lugens migrates from tropical areas to sub-tropical and temperate regions and so records shown in Figure 2 outside of the tropics do not necessarily indicate locations where N. lugens is established.
Enlarge this image.Figure 2. Distribution of Köppen–Geiger climate types Bsh, BSk, Cfa, Cfb, Cfc and Csa that occur in the EU and in third countries where Nilaparvata lugens has been reported. The legend shows the list of Köppen–Geiger climates. Red dots indicate point locations where N. lugens was reported. This includes subtropical and temperate areas where transient populations exist
Describe how the pest would be able to spread within the EU territory following establishment?
The brown planthopper is a long-distance migratory insect known to migrate passively with prevailing winds (Hu et al., 2018). The pest could also spread by movement of plants for planting and freshly cut host plants.
Comment on plants for planting as a mechanism of spread.
Rice seedlings (plants for planting) could provide a pathway for spread although such transplants if used they are not moved great distances within the EU and are assumed to be transplanted locally, close to where the seed was originally planted. Most rice is, however, directly drilled and seed does not provide a mechanism for spread for this insect.
Impacts
Would the pests' introduction have an economic or environmental impact on the EU territory?
Yes, if N. lugens established in the EU, it could have an economic impact on rice production. However, establishment is not considered possible.
The brown planthopper is one of the most important insect pests of rice in Asia. Its feeding induces plant wilting and causes hopperburn, which does not usually appear until the crop reaches the milk or dough stages; in its vegetative stage, rice can tolerate a population of 100–200 nymphs/hill (hill being the term used in rice cultivation to identify a rice plant with multiple stems) without showing any outward symptom of injury on the plants. Under heavy infestations, it can cause the wilting and complete drying of plants (Bottrell and Schoenly, 2012). Lower infestations reduce the number of tillers, number of panicles, and total grain weight of the plants (Bae and Pathak, 1970).
The pest is also able to transmit grassy stunt and ragged stunt virus diseases (CABI, online). The species was a minor rice pest until the mid-1960s in much of tropical Asia (Pathak and Dhaliwal, 1981). However, it assumed the status of the most destructive pest in the 1970s causing billions dollar of economic loss (Heinrichs and Mochida, 1984). In India, it is considered one of the pests responsible for large-scale devastation to the rice crop, causing yield losses amounting to as high as 60% and up to 80% in case of outbreaks (Srivastava et al., 2009; Kumar et al., 2012; Narayana et al., 2022). The loss of rice yield in China caused by N. lugens was approximately 1,880,000 tn in 2005 (Hu et al., 2011).
Although establishment is not considered possible, if N. lugens did establish, yield losses in rice would be expected.
Available measures and their limitations
Are there measures available to prevent pest entry, establishment, spread or impacts such that the risk becomes mitigated?
Yes. Although the existing phytosanitary measures identified in Section 3.3.2 do not specifically target N. lugens, they mitigate the likelihood of its entry into, establishment and spread within the EU (see also Section 3.6.1).
Identification of potential additional measures
Phytosanitary measures (prohibitions) are currently applied to some host plants for planting (see Section 3.3.2).
Additional potential risk reduction options and supporting measures are shown in Sections 3.6.1.1 and 3.6.1.2.
Additional potential risk reduction optionsPotential additional control measures are listed in Table 6.
Table 6 Selected control measures (a full list is available in EFSA PLH Panel, 2018) for pest entry/establishment/spread/impact in relation to currently unregulated hosts and pathways. Control measures are measures that have a direct effect on pest abundance
| Control measure/Risk reduction option (Blue underline = Zenodo doc, Blue = WIP) | RRO summary | Risk element targeted (entry/establishment/spread/impact) |
| Require pest freedom |
The presence of the pest is rather limited to southeast Asia and Oceania, therefore the origin of plants or plant products from pest free areas could be effective in preventing pest entry. Although we do not think that host plants present a pathway, if in the future rice seedlings are imported, they could be sourced from pest free areas. |
Entry |
| Managed growing conditions | Draining rice fields can be effective for reducing N. lugens infestation levels; growing no more than two crops per year and using early-maturing varieties is recommended. Judicious use of fertiliser by splitting nitrogen applications can also reduce planthopper outbreaks. The field should be drained for 3 or 4 days when heavy infestations occur. Increasing nitrogen levels, and higher relative humidity are known to increase N. lugens populations (CABI, online). | Impact/Spread |
| Crop rotation, associations and density, weed/volunteer control | Rice should not be planted at high density (CABI, online). In the tropics, growing no more than two crops per year, using early-maturing varieties is recommended (Reissig et al., 1986). In the EU, it is currently not possible to grow more than one crop in a year. | Establishment/Spread/Impact |
| Use of resistant and tolerant plant species/varieties | Approximately 10 major genes for resistance to N. lugens have been identified from rice germplasm, and many cultivars also show minor gene resistance. Three resistance genes have been used extensively in modern, semi-dwarf cultivars. However, some brown planthopper populations adapted to the new varieties in as little as 3 years. Host-plant resistance breaks down due to the high variation in field populations of N. lugens and it may happen more quickly with intense pesticide applications which lead to a more rapid population growth of surviving N. lugens. Wide hybridisation of Oryza sativa with wild rice species, and the use of genetic engineering, are providing new sources of resistance against N. lugens. Resistant varieties can also help to reduce pesticide use and thus assist in the build-up of natural enemies in areas where pesticides have been heavily used in previous seasons (CABI, online). | Entry/Establishment/Spread/Impact |
| Timing of planting and harvesting | Synchronous planting, including planting neighbouring fields within 3 weeks of each other and maintaining a rice-free period, may be effective (Reissig et al., 1986). However, asychronous rice cultivation within areas provides better continuity of natural enemy populations (Way and Heong, 1994). | Spread/Impact |
| Biological control and behavioural manipulation |
a) Biological control Existing species and levels of natural enemies in Asian rice areas are currently regarded as the key to the brown plant hopper management. N. lugens is normally controlled at low levels by the numerous predators, egg and nymphal parasites, pathogens and nematodes found in ricefield environments (CABI, online; Gurr et al., 2011). The fish Anabas testudineus caused a significant reduction of N. lugens population by 51% 85 days after sowing (Fahad et al., 2021). b) Mass trapping Light and yellow pan traps can be used. |
Spread/Impact |
| Chemical treatments on crops including reproductive material |
Several Economic Injury and Threshold Levels (ETL) were calculated at different growing stages in different countries (CABI, online). Five to ten N. lugens nymphs/plant at the seedling stage and 15 to 20 nymphs/plant represent the ETL causing yellowing in the lower leaves, and then wilting and death in the paddy crop (Kushwaha et al., 2016). In the 1980s, it was recognised that the over-use of insecticides was the root cause of outbreaks. Biological control, complemented by host-plant resistance, is now seen as the basis of management of N. lugens (Way and Heong, 1994). IPM programs emphasise that the routine use of insecticides should be avoided (Gallagher et al., 1994; Matteson et al., 1994). In temperate areas, where N. lugens does not overwinter, waves of migration in each cropping season can lead to a sudden build-up of the population. Consequently, insecticide use is more often needed in these areas than in the tropics, but should still be kept to a minimum. Kumar and Singh (2020) list active ingredients used in Asia for the management of N. lugens. |
Entry/Establishment/Impact |
| Chemical treatments on consignments or during processing | Use of chemical compounds that may be applied to plants or to plant products after harvest, during process or packaging operations and storage. | Entry/Spread |
|
The treatments addressed in this information sheet are:
|
||
| Conditions of transport | Specific requirements for mode and timing of transport of commodities to prevent escape of the pest and/or contamination.
|
Entry/Spread |
| Controlled atmosphere | Treatment of plants by storage in a modified atmosphere (including modified humidity, O2, CO2, temperature, pressure). | Entry/Spread (via commodity) |
Potential additional supporting measures are listed in Table 7.
Table 7 Selected supporting measures (a full list is available in EFSA PLH Panel, 2018) in relation to currently unregulated hosts and pathways. Supporting measures are organisational measures or procedures supporting the choice of appropriate risk reduction options that do not directly affect pest abundance
| Supporting measure (Blue underline = Zenodo doc, Blue = WIP) | Summary | Risk element targeted (entry/establishment/spread/impact) |
| Inspection and trapping |
Inspection is defined as the official visual examination of plants, plant products or other regulated articles to determine if pests are present or to determine compliance with phytosanitary regulations (ISPM 5). The effectiveness of sampling and subsequent inspection to detect pests may be enhanced by including trapping and luring techniques. Timely detection of brown planthopper incidence in the crop, through regular monitoring, is the key to effective pest management. Plant-shaking and light traps can be used to detect this planthopper (Hu et al., 2014. Hyperspectral remote sensing was also used to detect damaged plants by this pest (Prasannakumar et al., 2013). |
Entry/Establishment/Spread |
| Laboratory testing | Examination, other than visual, to determine if pests are present using official diagnostic protocols. Diagnostic protocols describe the minimum requirements for reliable diagnosis of regulated pests. | Entry/Spread |
| Sampling |
According to ISPM 31, it is usually not feasible to inspect entire consignments, so phytosanitary inspection is performed mainly on samples obtained from a consignment. It is noted that the sampling concepts presented in this standard may also apply to other phytosanitary procedures, notably selection of units for testing. For inspection, testing and/or surveillance purposes the sample may be taken according to a statistically based or a non-statistical sampling methodology. |
Entry |
| Phytosanitary certificate and plant passport |
An official paper document or its official electronic equivalent, consistent with the model certificates of the IPPC, attesting that a consignment meets phytosanitary import requirements (ISPM 5) a) export certificate (import) b) plant passport (EU internal trade) |
Entry/Spread |
| Surveillance | Surveillance to guarantee that plants and produce originate from a Pest Free Area could be an option. | Spread |
In case the European Commission wishes to introduce measures, the following could be limiting factors:
- Eggs may not be easily detectable as they are laid into in the leaf sheath tissues;
- long-distance migration;
- resistance to insecticides;
- overcoming resistance.
No key uncertainties have been identified.
ConclusionsThere is no data about rice being imported as freshly cut plants and/or growing plants for planting (excluding seed). Environmental conditions are not suitable for establishment, and consequently impacts are not expected. N. lugens does not satisfy the criteria that are within the remit of EFSA to assess for it to be regarded as a potential Union quarantine pest (Table 8).
Table 8 The Panel's conclusions on the pest categorisation criteria defined in Regulation (EU) 2016/2031 on protective measures against pests of plants (the number of the relevant sections of the pest categorisation is shown in brackets in the first column)
| Criterion of pest categorisation | Panel's conclusions against criterion in Regulation (EU) 2016/2031 regarding Union quarantine pest | Key uncertainties |
| Identity of the pest (Section 3.1) | The identity of the species is established and Nilaparvata lugens (Stål) is the accepted name. Morphological and molecular identification methods are available. | None |
| Absence/presence of the pest in the EU (Section 3.2) | N. lugens is not known to occur in the EU territory. | None |
| Pest potential for entry, establishment and spread in the EU (Section 3.4) |
N. lugens is unlikely to enter, become established or spread within the EU territory. A possible but unlikely potential pathway is import of infested freshly cut plants or plants for planting, for which we have no evidence of trade. Rice is mainly planted from seed; when transplanted, it is sourced locally. N. lugens cannot survive year-round in the EU due to unsuitable climate and lack of hosts during winter. |
None |
| Potential for consequences in the EU (Section 3.5) | If N. lugens established in the EU, it could have an economic impact. However, establishment is not considered possible. | None |
| Available measures (Section 3.6) | In a scenario where rice seedlings are imported, there are measures available to prevent entry, establishment and spread of N. lugens within the EU. Risk reduction options include inspections, chemical treatments, biological control on the crop and use of resistant varieties (although the pest has been developing resistance to insecticides and to resistant varieties), and the production of plants for import in the EU in pest free area. | None |
| Conclusion (Section 4) | N. lugens does not satisfy the criteria, that are within the remit of EFSA to assess, for it to be regarded as a potential Union quarantine pest. | None |
| Aspects of assessment to focus on/scenarios to address in future if appropriate: | It would be worthwhile noting whether N. lugens establishes within 500 km of EU rice growing areas. This could result in transient populations in the EU due to the pest's ability to migrate up to 500 km. | |
PeMoScoring is a ranking system that orders pests by risks posed to the EU and provide a tool to support risk managers in the decision of actions to take. It helps risk managers decide (i) whether further risk assessment, such as pest categorisation, is needed, (ii) whether EU surveillance and import control must be enforced for newly identified specific pests.
An EPPO code, formerly known as a Bayer code, is a unique identifier linked to the name of a plant or plant pest important in agriculture and plant protection. Codes are based on genus and species names. However, if a scientific name is changed the EPPO code remains the same. This provides a harmonised system to facilitate the management of plant and pest names in computerised databases, as well as data exchange between IT systems (Griessinger and Roy, 2015; EPPO, 2019).
-
Abbreviations
- EPPO
- European and Mediterranean Plant Protection Organization
- FAO
- Food and Agriculture Organization
- IPPC
- International Plant Protection Convention
- ISPM
- International Standards for Phytosanitary Measures
- MS
- Member State
- PAFF
- The Standing Committee on Plants, Animals, Food and Feed (PAFF Committee)
- PLH
- EFSA Panel on Plant Health
- PZ
- Protected Zone
- TFEU
- Treaty on the Functioning of the European Union
- ToR
- Terms of Reference
| Containment (of a pest) | Application of phytosanitary measures in and around an infested area to prevent spread of a pest (FAO, 2021) |
| Control (of a pest) | Suppression, containment or eradication of a pest population (FAO, 2021) |
| Entry (of a pest) | Movement of a pest into an area where it is not yet present, or present but not widely distributed and being officially controlled (FAO, 2021) |
| Eradication (of a pest) | Application of phytosanitary measures to eliminate a pest from an area (FAO, 2021) |
| Establishment (of a pest) | Perpetuation, for the foreseeable future, of a pest within an area after entry (FAO, 2021) |
| Greenhouse | A walk-in, static, closed place of crop production with a usually translucent outer shell, which allows controlled exchange of material and energy with the surroundings and prevents release of plant protection products (PPPs) into the environment. |
| Hitchhiker | An organism sheltering or transported accidentally via inanimate pathways including with machinery, shipping containers and vehicles; such organisms are also known as contaminating pests or stowaways (Toy and Newfield, 2010). |
| Impact (of a pest) | The impact of the pest on the crop output and quality and on the environment in the occupied spatial units |
| Introduction (of a pest) | The entry of a pest resulting in its establishment (FAO, 2021) |
| Pathway | Any means that allows the entry or spread of a pest (FAO, 2021) |
| Phytosanitary measures | Any legislation, regulation or official procedure having the purpose to prevent the introduction or spread of quarantine pests, or to limit the economic impact of regulated non-quarantine pests (FAO, 2021) |
| Quarantine pest | A pest of potential economic importance to the area endangered thereby and not yet present there, or present but not widely distributed and being officially controlled (FAO, 2021) |
| Risk reduction option (RRO) | A measure acting on pest introduction and/or pest spread and/or the magnitude of the biological impact of the pest should the pest be present. A RRO may become a phytosanitary measure, action or procedure according to the decision of the risk manager |
| Spread (of a pest) | Expansion of the geographical distribution of a pest within an area (FAO, 2021) |
Source: EPPO Global Database (EPPO, online)
| Host status | Host name | Plant family | Common name | |
| Cultivated hosts | Oryza | Poaceae | EPPO (online) | |
| Oryza sativa | Poaceae | Rice | EPPO (online) | |
| Zizania palustris* | Poaceae | Lake rice | EPPO (online) | |
| Wild weed hosts | Leersia oryzoides* | Poaceae | Cutgrass | EPPO (online) |
No reference provided to support this species as a host.
Appendix B – Distribution of Nilaparvata lugensDistribution records based on EPPO Global Database (EPPO, online) and CABI CPC (CABI, online).
| Region | Country | Sub-national (e.g. State) | Status | References |
| Asia | Bangladesh | Present, widespread | EPPO (online) | |
| Brunei Darussalam | Present, no details | EPPO (online) | ||
| Cambodia | Present, no details | EPPO (online) | ||
| China | Present, widespread | EPPO (online) | ||
| China | Anhui | Present, no details | EPPO (online) | |
| China | Chongqing | Present, no details | CABI (online) | |
| China | Fujian | Present, no details | EPPO (online) | |
| China | Guangdong | Present, no details | EPPO (online) | |
| China | Guangxi | Present, no details | EPPO (online) | |
| China | Guizhou | Present, widespread | CABI (online) | |
| China | Hainan | Present, no details | EPPO (online) | |
| China | Hebei | Present, no details | EPPO (online) | |
| China | Henan | Present, no details | EPPO (online) | |
| China | Hubei | Present, no details | EPPO (online) | |
| China | Hunan | Present, no details | EPPO (online) | |
| China | Jiangsu | Present, no details | EPPO (online) | |
| China | Jiangxi | Present, no details | EPPO (online) | |
| China | Jilin | Present, no details | EPPO (online) | |
| China | Liaoning | Present, no details | EPPO (online) | |
| China | Shandong | Present, no details | EPPO (online) | |
| China | Shanxi | Present, no details | EPPO (online) | |
| China | Sichuan | Present, no details | CABI (online) | |
| China | Xianggang (Hong Kong) | Present, no details | EPPO (online) | |
| China | Yunnan | Present, widespread | EPPO (online) | |
| China | Zhejiang | Present, no details | EPPO (online) | |
| India | Present, no details | EPPO (online) | ||
| India | Andhra Pradesh | Present, no details | EPPO (online) | |
| India | Arunachal Pradesh | Present, widespread | CABI (online) | |
| India | Assam | Present, widespread | CABI (online) | |
| India | Bihar | Present, no details | EPPO (online) | |
| India | Delhi | Present, no details | CABI (online) | |
| India | Gujarat | Present, no details | CABI (online) | |
| India | Haryana | Present, no details | EPPO (online) | |
| India | Himachal Pradesh | Present, no details | EPPO (online) | |
| India | Karnataka | Present, no details | EPPO (online) | |
| India | Kerala | Present, no details | EPPO (online) | |
| India | Madhya Pradesh | Present, no details | EPPO (online) | |
| India | Maharashtra | Present, widespread | CABI (online) | |
| India | Meghalaya | Present, widespread | CABI (online) | |
| India | Odisha | Present, no details | EPPO (online) | |
| India | Punjab | Present, no details | EPPO (online) | |
| India | Tamil Nadu | Present, no details | EPPO (online) | |
| India | Uttar Pradesh | Present, no details | EPPO (online) | |
| India | West Bengal | Present, no details | EPPO (online) | |
| Indonesia | Present, no details | EPPO (online) | ||
| Indonesia | Java | Present, no details | EPPO (online) | |
| Indonesia | Kalimantan | Present, no details | EPPO (online) | |
| Indonesia | Lesser Sunda Islands | Present, no details | CABI (online) | |
| Indonesia | Maluku | Present, no details | EPPO (online) | |
| Indonesia | Nusa Tenggara | Present, no details | EPPO (online) | |
| Indonesia | Sulawesi | Present, no details | EPPO (online) | |
| Indonesia | Sumatra | Present, no details | EPPO (online) | |
| Japan | Present, widespread | EPPO (online) | ||
| Japan | Hokkaido | Present, widespread | CABI (online) | |
| Japan | Honshu | Present, no details | EPPO (online) | |
| Japan | Shikoku | Present, widespread | CABI (online) | |
| Korea Dem. People's Republic | Present, no details | EPPO (online) | ||
| Korea, Republic | Present, no details | EPPO (online) | ||
| Laos | Present, widespread | EPPO (online) | ||
| Malaysia | Present, no details | EPPO (online) | ||
| Malaysia | Sabah | Present, no details | EPPO (online) | |
| Malaysia | Sarawak | Present, no details | CABI (online) | |
| Malaysia | West | Present, no details | EPPO (online) | |
| Myanmar | Present, no details | EPPO (online) | ||
| Nepal | Present, no details | EPPO (online) | ||
| Pakistan | Present, no details | EPPO (online) | ||
| Philippines | Present, no details | EPPO (online) | ||
| Singapore | Present, no details | EPPO (online) | ||
| Sri Lanka | Present, no details | EPPO (online) | ||
| Taiwan | Present, no details | EPPO (online) | ||
| Thailand | Present, no details | EPPO (online) | ||
| Vietnam | Present, no details | EPPO (online) | ||
| Oceania | Australia | Present, no details | EPPO (online) | |
| Australia | Northern Territory | Present, no details | EPPO (online) | |
| Australia | Queensland | Present, no details | EPPO (online) | |
| Fiji | Present, no details | EPPO (online) | ||
| Guam | Present, no details | EPPO (online) | ||
| Micronesia | Present, no details | EPPO (online) | ||
| New Caledonia | Present, widespread | CABI (online) | ||
| Northern Mariana Islands | Present, no details | EPPO (online) | ||
| Palau | Present, no details | EPPO (online) | ||
| Papua New Guinea | Present, no details | EPPO (online) | ||
| Solomon Islands | Present, no details | EPPO (online) |
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