EFSA Journal 2013;11(4):3162 SCIENTIFIC OPINION Scientific Opinion on the risks to plant health posed by Bemisia tabaci species complex and viruses it transmits for the EU territory1 EFSA Panel on Plant Health (PLH)2, 3 European Food Safety Authority (EFSA), Parma, Italy ABSTRACT The Panel on Plant Health conducted a pest risk assessment for Bemisia tabaci and the viruses it transmits, including an evaluation of risk reduction options and an assessment of the effectiveness of the special requirements linked to B. tabaci and the viruses listed in Council Directive 2000/29/EC. B. tabaci and a large number of viruses transmitted by this polyphagous insect occur in subtropical and tropical climates around the world. Five entry pathways for B. tabaci and associated viruses were identified, with the plants for planting pathway being most significant and rated for entry of insects and viruses as likely and moderately likely, respectively. The most invasive B. tabaci species and several of its associated viruses responsible for severe diseases in major European food crops are established outdoors in coastal Mediterranean regions. Because of similar climate requirements and host plant preferences, B. tabaci and associated viruses currently not present in Europe are likely to establish within the temperature limits set for B. tabaci. Trade between European Member States allows B. tabaci to reach greenhouses in northern Europe, including those in areas with protected zone status. Because of the cool climate, establishment and spread outdoors of B. tabaci is rated unlikely for northern Europe. This situation is likely to continue even under a climatic scenario with an increase in temperature of +2 °C. B. tabaci -transmitted viruses cause severe diseases with major negative impact on crop production when risk reduction measures are not used. Risk reduction options will also apply to B. tabaci and viruses new to Europe. Risk reductions options are evaluated in terms of reducing B. tabaci populations, crop infestations, virus incidence and the impact of diseases. © European Food Safety Authority, 2013 KEY WORDS Bemisia tabaci, European and non-European Bemisia tabaci, begomoviruses, non-circulatively transmitted viruses, pest risk assessment, risk reduction options. 1 On request from the European Commission, Question No EFSA-Q-2011-01157, adopted on 20 March 2013. 2 Panel members: Richard Baker, Claude Bragard, Thierry Candresse, Gianni Gilioli, Jean-Claude Grégoire, Imre Holb, Michael John Jeger, Olia Evtimova Karadjova, Christer Sven Magnusson, David Makowski, Charles Manceau, Maria Navajas, Trond Rafoss, Vittorio Rossi, Jan Schans, Gritta Schrader, Gregor Urek, Johan Coert van Lenteren, Irene Vloutoglou, Wopke Van der Werf, and Stephan Winter. Correspondence: [email protected] 3 Acknowledgement: The Panel wishes to thank the members of the Working Group on Bemisia tabaci: Pablo Bielza, Nathalie Gauthier, Gianni Gilioli, Jean-Claude Grégoire, Dirk Janssen, Olia Evtimova Karadjova, Maria Navajas, Johan Coert van Lenteren, Sara Pasquali, Jan Schans, Alberto Urbaneja and Stephan Winter for the preparatory work on this scientific opinion, and the hearing expert: Paul J. De Barro and EFSA staff: Svetla Kozelska, Morgan Ruffini, Olaf Mosbach-Schulz and Tilemachos Goumperis for the support provided to this scientific opinion. Suggested citation: EFSA Panel on Plant Health (PLH); Scientific Opinion on the risks to plant health posed by Bemisia tabaci species complex and viruses it transmits for the EU territory. EFSA Journal 2013;11(4):3162. [302 pp.] doi:10.2903/j.efsa.2013.3162. Available online: www.efsa.europa.eu/efsajournal © European Food Safety Authority, 2013 Risk assessment of Bemisia tabaci and viruses it transmits SUMMARY Following a request from the European Commission, the Panel on Plant Health was asked to deliver a scientific opinion on the risks posed by Bemisia tabaci to plant health in the European Union territory, with particular regard to the viruses it transmits. The Panel was also requested to identify risk management options and to evaluate their effectiveness in reducing the risks to plant health posed by these organisms. In addition, the Panel was asked to provide an opinion on the effectiveness of the present EU special requirements linked to B. tabaci, which are listed in Annex IV of Council Directive 2000/29/EC, which aim to reduce the risks of introduction and spread of this pest, and of the viruses it can transmit, into and within the EU territory. The Panel conducted the risk assessment, the evaluation of identified risk reduction options and the evaluation of the effectiveness of the present EU special requirements linked to B. tabaci and the viruses it transmits listed in Annex IV of the Council Directive 2000/29/EC following the general principles of the ―Guidance on a harmonised framework for pest risk assessment and the identification and evaluation of pest risk management options‖ (EFSA Panel on Plant Health (PLH), 2010). The identification of risk reduction options was performed according to the ―Guidance on methodology for evaluation of the effectiveness of options for reducing the risk of introduction and spread of organisms harmful to plant health in the EU territory‖ (EFSA Panel on Plant Health (PLH), 2012). After consideration of the evidence, the Panel reached the following conclusions: With regard to the assessment of the risks to plant health: B. tabaci is considered to be one of the most serious threats to crop cultivation worldwide, predominantly because of the large number of viruses it transmits. In regions where B. tabaci is established, viruses transmitted by this insect, especially those affecting tomato and cucurbits, and also beans, pepper and aubergines, are responsible for severe diseases that have a strong negative impact on crop yield. As a consequence, crop production in those areas is not possible without a system-wide and comprehensive set of pest and disease management measures in place. In the risk assessment area, B. tabaci is present outdoors in coastal areas with a Mediterranean climate, and in many EU countries the pest is present in greenhouses. B. tabaci is a complex of at least 28 indistinguishable morphocryptic species, of which four occur in Europe. Two species, Mediterranean (Med, formerly referred to as biotype Q) and Middle East–Asia Minor 1 (MEAM1, formerly referred to as biotype B), are mostly associated with negative effects on crops such as ornamentals, tomato and cucurbits, and are prevalent both in Europe and in many regions across the world. Many other B. tabaci species exist outside the risk assessment area, and these can reach high population densities, but it is only Med and MEAM1 that are considered invasive. All B. tabaci species can transmit viruses, and the viruses associated with B. tabaci reported from around the world have an immense diversity, which is reflected in numerous species and strains. In general, diseases resulting from virus infections have a serious negative impact on crops and, thus, the introduction of B. tabaci-transmitted viruses currently not present in the EU would be a significant risk. ENTRY For entry of B. tabaci and the viruses it transmits, five pathways have been identified, and the most relevant one is the plants for planting pathway. Plants not intended for planting (cut flowers and branches with foliage) and the pathway represented by fruits and vegetables were also considered, while entry of B. tabaci through human-associated means not involving plants (e.g. on vehicles or clothes) and entry of insects by natural means (e.g. with wind or active flight) were considered negligible pathways and not assessed in this opinion. Viruses can enter with infected plant material and with insects carrying the viruses (viruliferous insects). The transmission modes of B. tabaci-transmitted viruses are substantially different and have a EFSA Journal 2013;11(4):3162 2 Risk assessment of Bemisia tabaci and viruses it transmits strong influence on the probability of entry. Therefore, viruses were grouped into circulatively transmitted viruses (begomoviruses) and non-circulative viruses (all other viruses); these two groups are considered separately in the opinion. The evaluation of the likelihood of entry of pest and viruses was supported with a probabilistic model that combined expert assessment of the presumed risk of entry from the major world areas with trade volumes of commodities related to the three pathways. Pathway 1. Plants for planting Entry of B. tabaci can be expected from all world areas where populations of this insect are established, because B. tabaci is not only a polyphagous pest infesting a wide range of plant species (host plants) but can also be carried along on non-hosts, that is with plants on which the insect is only visiting (non-host plants). The probability of entry of B. tabaci into the EU by the plants for planting pathway is rated as likely, because of the frequent association of insects with the pathway at origin and based on the number of interception records despite strict phytosanitary requirements for places of production of plants for planting. Although the fraction of intercepted consignments relative to the total number of consignments imported into the EU is low, the high trade volumes justify this rating. The major volume of trade in this pathway mainly concerns ornamental plants. The specific ornamental plant species that are imported via this pathway are non-host plants for B. tabaci- transmitted viruses. Entry of circulatively transmitted viruses can occur with viruliferous B. tabaci insects and with infected plants while non-circulatively transmitted viruses can enter only with infected host plants, because of their limited persistence in their vector. Entry of viruses with viruliferous B. tabaci or with infected crop plants is considered as moderately likely. Pathway 2. Cut flowers and branches with foliage The probability of entry of B. tabaci into the EU with the pathway of cut flowers and branches with foliage is considered as moderately likely because eggs and nymphal stages of the pest can survive transport.