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

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

To support management decisions, molecular characterization of data and geo-reference of incidence records of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) were combined with data on the biology and ecology of the pest to estimate its climatic suitability and potential spread at regional and global scale. A CLIMEX model was developed and used for the global prediction of current and future climate-induced changes in the distributional shifts of T. absoluta. Results revealed that temperature and moisture characterized T. absoluta population growth while the pest ability to survive the cold, hot, wet and dry stress conditions are the primary characteristics defining its range frontiers. Simulated irrigation also played an important role in the model optimization. Model predictions suggest that T. absoluta represents an important threat to Africa, Asia, Australia, Northern Europe, New Zealand, Russian Federation and the United States of America (USA). Under climate change context, future predictions on distribution of T. absoluta indicated that the invasive nature of this pest will result in significant crop losses in certain locations whereas some parts of Africa may witness diminution in ranges. The following scenarios may occur: 1) T. absoluta damage potential may upsurge moderately in areas of Africa where the pest currently exists; 2) a range diminution in temperate to Sahel region with moderate upsurge in damage potential; 3) a range expansion in tropical Africa with reasonable upsurge of damage potential. These possible outcomes could be explained by the fact that the continent is already warm, with the average temperature in majority of localities near the threshold temperatures for optimal development and survival of T. absoluta. Outputs from this study should be useful in helping decision-makers in their assessment of site-specific risks of invasion and spread of T. absoluta with a view to developing appropriate surveillance, phytosanitary measures and management strategies.

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Identification and Risk Assessment for Worldwide Invasion and Spread of Tuta absoluta with a Focus on Sub-Saharan Africa: Implications for Phytosanitary Measures and Management

The tomato leafminer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) has recently invaded Mediterranean countries and is a major pest in tomato crops. Trichogrammatid oophagous parasitoids have shown promising potential for controlling the pest before the yield decreases in the greenhouse. In protected tomato crops (greenhouse), mirid predators are commonly used for biological control of whiteflies and they also prey on T. absoluta. These predators do not attack Trichogramma adults but they may partially decrease the overall impact of parasitoids on T. absoluta if intraguild predation (IGP) occurs on parasitized eggs. Under laboratory conditions, we tested if the mirid predator Macrolophus pygmaeus shows preference between parasitized and unparasitized T. absoluta eggs. We also tested if the predator reduces the number of parasitized eggs on caged tomato plants (microcosms) and assessed the efficacy of natural enemies used alone or together in limiting T. absoluta populations. We found that IGP is inflicted on the parasitoid Trichogramma achaeae by M. pygmaeus and that the risk of IGP depends on the developmental stage of T. achaeae inside the egg because the larva is at risk mostly early in its development (when parasitized egg is still yellow). In addition, we observed that non-consumptive events, likely probing of the predator on parasitized eggs, may induce mortality in parasitoid offspring without actual feeding on parasitized eggs. However, both IGP and non-consumptive events decreased when the predator was not confined with parasitized eggs in small arenas. Despite negative effects of the predator to the parasitoid, results demonstrate that adding Trichogramma parasitoids may significantly increase the level of control of the pest over what could be attained when only the mirid predator M. pygmaeus is present on tomato. Implications of results are discussed regarding potential of these natural enemies for biological control of T. absoluta in greenhouse tomato crops.

Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest Tuta absoluta

The omnivorous predators Nesidiocoris tenuis (Reuter) and Macrolophus pygmaeus Rambur (Hemiptera: Miridae) are indigenous natural enemies that commonly inhabit tomato crops in the Mediterranean basin. Both predators are mass-reared and primarily released to control whiteflies, although recently they have also contributed to the control of the invasive tomato pest Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). The life history traits of these two predators have been studied in the laboratory under the conditions of being fed exclusively the eggs of T. absoluta or the eggs of the factitious prey Ephestia kuehniella (Zeller) (Lepidoptera: Pyralidae). Immature stages of both predator species successfully developed while preying on eggs of T. absoluta. However, the mature M. pygmaeus females produced significantly lower numbers of offspring in comparison to the offspring produced when preying on E. kuehniella eggs. This resulted in higher than expected demographic indexes for N. tenuis when compared to M. pygmaeus (e.g., the intrinsic rates of increase were 0.127 and 0.005, respectively). Our results support previous studies on the potential of N. tenuis has as biological control agent of T. absoluta, and indicate that the role of M. pygmaeus in controlling T. absoluta in the absence of other food sources is possibly limited.

A comparative life history study of two mirid bugs preying on Tuta absoluta and Ephestia kuehniella eggs on tomato crops: implications for biological control

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.

Trichogramma achaeae Nagaraja and Nagarkatti (Hymenoptera: Trichogrammatidae) is currently used as biological control agent for several lepidopteran pests. Knowledge of thermal requirements is essential to optimize its rearing procedures and inundative releases. The biological characteristics and two-sex life table parameters of T. achaeae were determined at five constant temperatures (15, 20, 25, 30, and 35 °C) using Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) eggs. T. achaeae was able to develop and survive from 15 °C to 30 °C, but not at 35 °C. Temperature significantly affected the preadult development time and adult longevity, decreasing when temperature increased from 15 °C to 30 °C. Temperature significantly altered the sex ratio, being female biased between 15 °C and 25 °C. Age-stage, two-sex life table analysis indicated that net reproductive rate (R0) was highest at 20 °C. Both the intrinsic rate of increase (r) and finite rate of increase (λ) increased with increasing temperature, while the mean generation time (T) decreased significantly. In addition, functional response of T. achaeae was studied, being significantly affected by temperature and host egg density, displaying a Holling type-I at 15 °C and a Holling type-II at 25 °C. The relevance of these results is discussed for the use of T. achaeae as biological control agent.

https://www.mdpi.com/2075-4450/11/8/482/pdf

Estrella Hernández Suárez

Papers

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

Effect of Temperature on Life History and Parasitization Behavior of Trichogramma achaeae Nagaraja and Nagarkatti (Hym.: Trichogrammatidae).

Bases para la gestión integrada de Chrysodeisis chalcites (Lep. Noctuidae) en cultivos de platanera de Canarias