Natural Enemies of the South American Moth, Tuta Absoluta, in Europe, North Africa and Middle East, and Their Potential Use in Pest Control Strategies
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J Pest Sci DOI 10.1007/s10340-013-0531-9 RAPID COMMUNICATION Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle East, and their potential use in pest control strategies Lucia Zappala` • Antonio Biondi • Alberto Alma • Ibrahim J. Al-Jboory • Judit Arno` • Ahmet Bayram • Anaı¨s Chailleux • Ashraf El-Arnaouty • Dan Gerling • Yamina Guenaoui • Liora Shaltiel-Harpaz • Gaetano Siscaro • Menelaos Stavrinides • Luciana Tavella • Rosa Vercher Aznar • Alberto Urbaneja • Nicolas Desneux Received: 16 June 2013 / Accepted: 23 September 2013 Ó Springer-Verlag Berlin Heidelberg 2013 Abstract The South American tomato leafminer, Tuta crops, as well as in wild flora and/or using infested sentinel absoluta Meyrick (Lepidoptera: Gelechiidae), is an invasive plants. More than 70 arthropod species, 20 % predators and Neotropical pest. After its first detection in Europe, it rap- 80 % parasitoids, were recorded attacking the new pest so idly invaded more than 30 Western Palaearctic countries far. Among the recovered indigenous natural enemies, only becoming a serious agricultural threat to tomato production few parasitoid species, namely, some eulophid and braconid in both protected and open-field crops. Among the pest wasps, and especially mirid predators, have promising control tactics against exotic pests, biological control using potential to be included in effective and environmentally indigenous natural enemies is one of the most promising. friendly management strategies for the pest in the newly Here, available data on the Afro-Eurasian natural enemies invaded areas. Finally, a brief outlook of the future research of T. absoluta are compiled. Then, their potential for and applications of indigenous T. absoluta biological con- inclusion in sustainable pest control packages is discussed trol agents are provided. providing relevant examples. Collections were conducted in 12 countries, both in open-field and protected susceptible Keywords Biological control Á Generalist predators Á Integrated pest management Á Invasive species Á Parasitoid community Á Western Palaearctic Communicated by M. Traugott. L. Zappala` Á A. Biondi Á G. Siscaro A. Bayram Department of Agri-food and Environmental Systems Plant Protection Department, Agriculture Faculty, Dicle Management, University of Catania, via Santa Sofia 100, University, 21280 Diyarbakir, Turkey 95123 Catania, Italy A. El-Arnaouty A. Biondi Á A. Chailleux Á N. Desneux (&) Department of Economic Entomology and Pesticides, Cairo French National Institute for Agricultural Research (INRA), University, Giza, Egypt 400 Route des Chappes, 06903 Sophia-Antipolis, France e-mail: [email protected] D. Gerling Department of Zoology, Tel Aviv University, 69978 Tel Aviv, A. Alma Á L. Tavella Israel Dipartimento di Scienze Agrarie, Forestali e Alimentari (DISAFA), University of Torino, via L. da Vinci 44, Y. Guenaoui 10095 Grugliasco, TO, Italy Department of Agronomy, University Ibn Badis of Mostaganem, 27000 Mostaganem, Algeria I. J. Al-Jboory Department of Plant Protections, University of Baghdad, Abu L. Shaltiel-Harpaz Ghraib, Iraq Northern R&D, Migal–Galilee Research Institute, P.O.B. 831, 11016 Kiryat Shmona, Israel J. Arno` Department of Entomology, IRTA, Ctra. Cabrils km.2, 08348 Cabrils, Barcelona, Spain 123 J Pest Sci Introduction et al. 2010; Tropea Garzia et al. 2012). Afterwards, it rap- idly spread throughout the Mediterranean basin, in Europe, The composition of worldwide biotic communities has North Africa and the Middle East (Desneux et al. 2011). greatly changed in recent years due to the collapse of natural Tuta absoluta is considered a typical invasive species barriers to wild species movements mainly in relation to because of its capacity to develop very quickly on tomato human activities (Liebhold and Tobin 2008). Among the cultivations and to spread rapidly in new areas causing newly introduced insect species, some can become invasive, economically relevant damage (Desneux et al. 2010; Ca- with subsequent significant economic impacts. The success parros Megido et al. 2012). or failure of a biological invasion may depend on the species’ Although chemical control has been the first strategy life history parameters, on its response to climatic condi- adopted in the newly invaded areas, alternative control tions, on the competition with native species and on the measures are being investigated (Cagnotti et al. 2012; impact of natural enemies (Grabenweger et al. 2010). This Cocco et al. 2013) in compliance with the EU Directive on last factor may be crucial in the invasion mechanism and the sustainable use of pesticides (Directive 2009/128/EC). In success of an invader, in terms of distribution and abundance, the case of T. absoluta, the need for alternative control and could be related to the absence or low efficacy of natural methods is strengthened by the development of resistance control in the new territories, as stated by the so-called to insecticides by the pest (Haddi et al. 2012; Gontijo et al. Enemy release hypothesis (Keane and Crawley 2002). 2013) as well as the side effects of pesticides on beneficial Indeed, it is assumed that natural enemies in the newly arthropods (Arno´ and Gabarra 2011; Biondi et al. 2012, invaded areas need time to get adapted to and control the 2013a; and see Desneux et al. 2007 for a thorough review). exotic species effectively. This may be due to the fact that On the other hand, various predators and parasitoids native antagonists need to adjust their behaviour and/or spontaneously attack T. absoluta in tomato crops in Europe physiology to be able to successfully develop on the exotic and in North Africa. Some of these, mainly native Miridae, prey/host. For these reasons, natural enemy complexes on have been already employed in integrated pest management invaders may perform initially low percentage predation/ (IPM) strategies (Castan˜e´ et al. 2011; Molla´ et al. 2011; parasitism (Cornell and Hawkins 1993). However, several Cabello et al. 2012; Zappala` et al. 2012b; Chailleux et al. examples of successful biological control using natural 2013a). However, several screenings for effective natural enemies that have not coevolved with the pest, the so-called enemy species in the invaded area are still ongoing (Chail- New species association, are also known (Hokkanen and leux et al. 2012; Gabarra et al. 2013). More than 70 species of Pimentel 1984; O’Connell et al. 2012). generalist natural enemies have been reported for T. absoluta In this framework, gaining knowledge on indigenous in the Western Palaearctic region so far. These have been natural enemies that get adapted to the new hosts and sampled both on open-field and protected susceptible crops understanding their role in limiting the alien species are as well as on wild flora and/or using infested sentinel plants. essential for establishing the basis of suitable and sustain- Here, we take into account all the available data, aiming to able control strategies of exotic pests. This also applies to give a comprehensive picture of the composition of the one of the latest invasive species that arrived in the Western species that spontaneously provide biological control ser- Palaearctic region: the South American tomato leafminer, vices and their current role in T. absoluta control Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). This programmes. moth is a Neotropical species and is considered a key pest of the tomato in South America (Guedes and Picanc¸o 2012; Luna et al. 2012), where it remained confined until its first Predators record in Western Palaearctic, in Spain in 2006 (Desneux Fifteen arthropod species were recorded preying on the M. Stavrinides South American tomato leafminer in the last few years in Department of Agricultural Sciences, Biotechnology and Food Science, Cyprus University of Technology, Arch. Kyprianos 30, newly invaded Western Palaearctic countries (Table 1). 3036 Limassol, Cyprus They mainly belong to the order Hemiptera (ten species) and in particular to the families Miridae, Anthocoridae and R. Vercher Aznar Nabidae in descending order of species numbers. These Instituto Agroforestal del Mediterra´neo (IAM), Universitat Polite`cnica de Vale`ncia, Camino de Vera s/n, 40622 Valencia, predators include zoophytophagous bugs that usually col- Spain onize and establish in organic and IPM crops where they are also able to build up their populations before pest A. Urbaneja arrival, exploiting alternative preys, such as whiteflies, Departamento de Entomologı´a, Centro de Proteccio´n Vegetal, Instituto Valenciano de Investigaciones Agrarias (IVIA), thrips, aphids, spider mites, leafminers and other Lepi- Moncada, Valencia, Spain doptera, and host plants [e.g. Dittrichia viscosa (L.) and 123 J Pest Sci Table 1 Predators observed feeding on Tuta absoluta in Western Palaearctic countries Order: Family Species Known T. absoluta Country(ies) Sampling Season(s) Reference(s) distributiona instars method(s) Mesostigmata: Amblyseius swirskii Western Eggs and L1 Spain Protected crop Summer Molla´ et al. (2010) Phytoseiidae Athias-Henriot Palaearctic (eggplant) sampling Amblyseius Cosmopolitan Eggs and L1 Spain Protected crop Summer Molla´ et al. (2010) cucumeris (eggplant) (Oudemans) sampling Hemiptera: Dicyphus sp. Eggs and France, Italy Open-field and Summer Biondi et al. (2013b), Miridae young larvae protected crop Zappala` et al. sampling unpublished data Dicyphus errans Western Eggs and L1 Algeria, Italy Open-field and Spring– Boualem et al. (2012),