The tomato leafminer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) is a devastating pest of tomato originating from South America. After its initial detection in eastern Spain in 2006, it rapidly invaded various other European countries and spread throughout the Mediterranean basin. If no control measures are taken, then the pest can cause up to 80–100% yield losses in tomato crops in recently invaded areas and may pose a threat to both greenhouse and open-field tomato production. The exceptional speed and extent of T. absoluta invasion have called for studies documenting its biology and ecology, while indicating an urgent need for efficient and sustainable management methods. The development of approaches to manage T. absoluta would be facilitated through a detailed revision of information on this pest in its area of origin. This review combines information on the invasion by T. absoluta, its ecology, and potential management strategies, including data that may help the implementation of efficient biological control programs. These programs, together with a variety of other management tactics, may allow efficient integrated pest management of T. absoluta in Europe and Mediterranean Basin countries.

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Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control

The South American tomato leafminer, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), is an invasive Neotropical pest. After its first detection in Europe, it rapidly invaded more than 30 Western Palaearctic countries becoming a serious agricultural threat to tomato production in both protected and open-field crops. Among the pest control tactics against exotic pests, biological control using indigenous natural enemies is one of the most promising. Here, available data on the Afro-Eurasian natural enemies of T. absoluta are compiled. Then, their potential for inclusion in sustainable pest control packages is discussed providing relevant examples. Collections were conducted in 12 countries, both in open-field and protected susceptible crops, as well as in wild flora and/or using infested sentinel plants. More than 70 arthropod species, 20 % predators and 80 % parasitoids, were recorded attacking the new pest so far. Among the recovered indigenous natural enemies, only few parasitoid species, namely, some eulophid and braconid wasps, and especially mirid predators, have promising potential to be included in effective and environmentally friendly management strategies for the pest in the newly invaded areas. Finally, a brief outlook of the future research and applications of indigenous T. absoluta biological control agents are provided.

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Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle East, and their potential use in pest control strategies

Since its detection in the Mediterranean basin at the end of 2006 and later in other European countries, the South American tomato pinworm, Tuta absoluta (Meyrick), has become a serious threat to tomato crops. In newly infested areas, it is especially problematic during the first years of its presence. Nevertheless, after 2-3 years, the incidence of T. absoluta has become less severe in certain areas. There are several factors contributing to this decline, such as the increase in growers' knowledge of pest behaviour and biology and the correct application of integrated pest control strategies. The impact of opportunistic native natural enemies (fortuitous biological control) should be considered as one of the key factors in this decline. In this review, available information on indigenous natural enemies is updated, and the current pest management approaches used against T. absoluta are addressed. Finally, future scenarios for biological control of this pest are discussed.

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Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin

The South American tomato pinworm, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), is a devastating pest currently threatening the global tomato industry worldwide. In the last 10 years, it has spread and expanded to most of Europe, Africa and Asia, causing extensive damage to the crop itself and to the international tomato trade. With the aim of providing an overview of the current knowledge on this pest, we have briefly reviewed the available literature relying on its spread, quarantine, modeling and management. Finally, we have underlined the gaps in knowledge and provided several recommendations on how to achieve sustainable control as well as how to prevent further spread into unaffected areas.

From the Western Palaearctic region to beyond: Tuta absoluta 10 years after invading Europe

The tomato borer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), is considered to be one of the most devastating pests affecting tomato crops in South America, where crop losses range from 60 to 100%. After its detection in the Spanish tomato-growing area at the end of 2006, it spread quickly to other European and northern African countries. Currently, T. absoluta management in these countries is mainly based on chemical treatments. Nonetheless, special emphasis is being placed on implementing environmentally safe strategies. Commercial formulates based on Bacillus thuringiensis may be a good alternative, as they have been used to control other insect pests successfully. The laboratory, greenhouse, and open-field experiments presented in this work are evidence that B. thuringiensis is highly efficient in controlling T. absoluta. First instar larvae were the most susceptible, while susceptibility was lower in second and third instar larvae. Our results have shown that the impact of T. absoluta can be greatly reduced by spraying only B. thuringiensis-based formulates, with no need for chemical insecticides. Furthermore, the integration of this technology with other biological control methods focused on T. absoluta eggs, such as the use of mirid predators or parasitoids, could reduce the number of B. thuringiensis treatments and the use of chemicals, with the consequent reduction of residues on fruits.

Efficacy of Bacillus thuringiensis (Berliner) in controlling the tomato borer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae)

The South American tomato pinworm, Tuta absoluta (Meyrick) has been introduced into new geographic areas, including the Mediterranean region, where it has become a serious threat to tomato production. Three greenhouse trials conducted in tomato crops during 2009 and 2010 explored control strategies using the egg-parasitoid Trichogramma achaeae Nagaraja and Nagarkatti compared with chemical control. The effectiveness of the predator Nesidiocoris tenuis (Reuter) was also tested. In greenhouses with early pest infestations (discrete generations), periodic inundative releases (eight releases at a rate of 50 adults/m2, twice a week) were necessary to achieve an adequate parasitism level (85.63 +/- 5.70%) early in the growing season. However, only one inoculative release (100 adults/m2) was sufficient to achieve a comparatively high parasitism level (91.03 +/- 12.58%) under conditions of high pest incidence and overlapping generations. Some intraguild competition was observed between T. achaeae and the predator, N. tenuis. This mirid species is commonly used in Mediterranean greenhouse tomato crops for the control of the sweetpotato whitefly, Bemisia tabaci (Gennadius). Tomato cultivars were also observed to influence the activity of natural enemies, mainly N. tenuis (whose average numbers ranged between 0.17 +/- 0.03 and 0.41 +/- 0.05 nymphs per leaf depending on the cultivar). This may be because of differences in plant nutrients in different cultivars, which may affect the feeding of omnivorous insects. In contrast, cultivar effects on T. achaeae were less apparent or possibly nonexistent. Nevertheless, there was an indirect effect in as much as T. achaeae was favored in cultivars not liked by N. tenuis.

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Biological control strategies for the South American tomato moth (Lepidoptera: Gelechiidae) in greenhouse tomatoes.

Biological control of the South American tomato pinworm, Tuta absoluta (Lep.: Gelechiidae), with releases of Trichogramma achaeae (Hym.: Trichogrammatidae) in tomato greenhouses of Spain.

The damsel bug Nabis pseudoferus (Hem.: Nabidae) as a new biological control agent of the South American Tomato Pinworm, Tuta absoluta (Lep.: Gelechiidae), in tomato crops of Spain.

The recent development and adoption of IPM programs in the southeast of Spain, where the largest concentration of protected crops of the world has developed, excluding China, has become a reference model for other areas, specially with Mediterranean climatic conditions. At least four key driving forces have been involved, strong regulatory framework, subsidies to the growers, extension of knowledge, and Research and Innovation. The last has motivated a drastic change in the mind-set of growers since they recognize biocontrol as the best pest management after selection and development of suitable species and efficient biocontrol programs, which are mainly based on augmentative releases of commercially mass-reared populations. The quality and price of the beneficials, which has deserved less attention when analyzing the failure or success of biocontrol, has contributed significantly to this achievement. Biosystems engineering progress to mass rear the key species of insects and mites currently used in these augmentative programs are reviewed. Specifically, attention is paid to the predatory mites Phytoseidae and some species of the families Miridae and Anthocoridae, as well as some parasitoids. Changes in the productions and formulation of new release systems, such as sachets a la carte that have increased the affordable quantities of individuals, are discussed. Finally, trends and challenges on complementary and artificial diets, as well as automatisms, which may decrease production costs and open new opportunities for open field crops, are explored.

Biosystems Engineering Applied to Greenhouse Pest Control

En los anos 2007 y 2008 se selecciono un parasitoide de huevos autoctono, la especie Trichogramma achaeae, que ofrece un comportamiento muy agresivo contra la recien llegada polilla exotica Tuta absoluta, el principal problema actual del tomate. Este parasitoide muestra una mejor adaptacion a las condiciones de invernadero que las otras especies de Trichogramma ensayadas en Europa o Suramerica para esta y otras plagas. Despues de tres anos de ensayos de laboratorio, semicampo y campo (2007-2009), se presenta un programa de control biologico utilizando, entre otras medidas, introducciones inundativas del parasitoide, que se ha mostrado totalmente valido para el control de plagas del tomate en invernaderos de Espana y Francia. Un analisis comparativo de los costes del programa de control integrado respecto al control quimico exclusivo, evidencia que este tambien es viable economicamente.

Enric Vila

Papers

Biological control strategies for the South American tomato moth (Lepidoptera: Gelechiidae) in greenhouse tomatoes.

Biological control of the South American tomato pinworm, Tuta absoluta (Lep.: Gelechiidae), with releases of Trichogramma achaeae (Hym.: Trichogrammatidae) in tomato greenhouses of Spain.

The damsel bug Nabis pseudoferus (Hem.: Nabidae) as a new biological control agent of the South American Tomato Pinworm, Tuta absoluta (Lep.: Gelechiidae), in tomato crops of Spain.

Biosystems Engineering Applied to Greenhouse Pest Control

Aplicación de parasitoides de huevos en el control de Tuta absoluta en España