Introduction

Successfully established invasive organisms, such as insect pests, have often been proven to severely damage host crops and adversely influence ecosystem components and functioning as well as biodiversity dynamics, and to inducing substantial economic losses in the invaded areas (Sala et al., 2000; Pimentel et al. 2005; Olson 2006; Simberloff et al. 2013; Asplen et al. 2016; Kirichenko et al. 2019; McLaughlin and Dearden 2019; Milosavljević et al. 2019; Moore et al. 2019). Within this category of (exotic) invasive species, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) is a devastating insect pest of tomato crops (Solanum lycopersicon L.) and a great economic challenge both in South America, its area of origin, and in several invaded areas of Europe, Africa, Asia and Central America (Campos et al. 2017; Biondi et al. 2018; Han et al. 2019; Mansour et al. 2018; Santana et al. 2019; Verheggen and Fontus 2019).

In addition to tomato, many cultivated and wild plant species belonging to the Solanaceae have also been reported as potential hosts for this pest (Desneux et al., 2010, 2011; Bawin et al. 2016; Sylla et al. 2019). Tuta absoluta has a high reproduction rate and may develop several generations per year in tomatoes (Desneux et al. 2010; Cocco et al. 2015; Biondi et al. 2018). However, successful establishment and rapid spread, as well as development and life cycle of this pest, depend on various factors, such as favorable temperature and relative humidity conditions, intensive tomato production system, and continuous host plant availability (Desneux et al. 2010, 2011; Cuthbertson et al. 2013; Machekano et al. 2018; Cherif et al. 2019a, b). Damage caused by T. absoluta larvae can be seen on tomato leaves, stems, twigs and fruits, which generally induce major crop yield and economic losses (Desneux et al. 2010; Campos et al. 2017; Biondi et al. 2018).

Considering these serious crop health and economic issues, several pest management approaches have been tested and, whenever possible, implemented against this pest worldwide (Biondi and Desneux 2019). These approaches include (i) prophylactic and cultural practices, (ii) pheromone-based tactics such as mass trapping and mating disruption; (iii) biological control releasing parasitoids and/or mirid predators, and (iv) application of insecticides, which constitutes the most commonly adopted control option (Desneux et al. 2010; Caparros-Megido et al. 2013; Cocco et al. 2013; Campos et al. 2017; Biondi et al. 2018; Majidiani et al. 2019; Mansour et al. 2019). The latter, when using broad-spectrum chemical pesticides, has generally two major constraints: adverse side effects on non-target beneficial arthropods including pest’s natural enemies (parasitoids and predators) and pollinators (Mommaerts et al. 2006; Desneux et al. 2007; Arnó and Gabarra 2011; Wanumen et al. 2016; Biondi et al. 2018; Mansour et al. 2018) and development of insect resistance to various pesticide active substances used (Campos et al. 2014; Haddi et al. 2017; Roditakis et al. 2018; Guedes et al. 2019; Silva et al. 2019; Richardson et al. 2020). For these reasons, adopting ecofriendly control methods, as alternatives to widespread applications or even to misuse of hazardous chemical pesticides, is of crucial importance. In this regard, biological control programs through releases of either egg and/or larval parasitoids, mirid predators, or their combination, and applying biopesticides (microbial or botanical active substances) have successfully been incorporated in integrated pest management (IPM) programs against T. absoluta in South America, Europe, Africa, and Asia (Desneux et al. 2010; Zappalà et al. 2013; Han et al. 2019; Mansour et al. 2018; Ferracini et al. 2019).

Herein, all relevant, up-to-date published research focusing on testing, developing, implementing and enhancing various biorational control options against the invasive T. absoluta in the Middle East and North Africa (MENA) region, performed during the last decade, are thoroughly reviewed and elucidated for the first time.

The collection of scientific articles published in either English, French, or Arabic to be analyzed in the present article was achieved through searches on the online databases CAB Abstracts, Google Scholar, Web of Science, Scopus, and PubMed, using the following keywords in various combinations: “South American tomato pinworm”, “Tomato leafminer”, “Tuta absoluta”, “biological control”, “biorational control”, “natural enemies”, “egg parasitoid”, “larval parasitoid”, “Trichogramma”, “release rate”, “predatory mirids”, “Nesidiocoris”, “Macrolophus”, “Entomopathogen”, “microbial pesticide”, “Bacillus thuringiensis”, “spinosad”, “fungus”, “virus”, “essential oils”, “plant extracts”, “botanical pesticide”, “azadirachtin”, “pheromone-mass trapping”, “North Africa”, “Middle East”, “Mediterranean basin”, “Asia”, “tomato greenhouse”, and “open-field tomato crops”.

Releasing parasitoids, predators or their combination

Biological control using insect predators and parasitoids has long been regarded as an environmentally sound, effective and sustainable invasive pest management approach adopted as alternative to repetitive and extensive applications of harmful synthetic chemical pesticides (Barratt et al. 2018; Rossi Stacconi et al. 2018; Van Lenteren et al. 2018a; Giorgini et al. 2019; Konopka et al. 2019). Such a reality is particularly true and has been of great interest when developing the most suitable management programs of T. absoluta in several, but not all, invaded tomato-producing areas around the world (Cabello et al. 2009; Desneux et al. 2010; Biondi et al. 2018; Mansour et al. 2018; Ferracini et al. 2019; Salas Gervassio et al. 2019). More specifically, in the MENA region, biological control of T. absoluta exploiting pest’s species-specific or generalist natural enemies has mainly been based on either consecutive single or combined augmentative releases of egg parasitoids and/or predatory bugs (Table 1). On the other hand, the performance of further different biocontrol categories such as conservation or classical biological control, which have been adopted in South America as well as in some European invaded areas, are yet to be tested and evaluated by researchers in North African and Middle Eastern countries.

Table 1 Overview on parasitoid and/or predatory species successfully released alone or in combination against Tuta absoluta in open-field or greenhouses in countries of the MENA region
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Releases of parasitoids

In North Africa, field releases using Trichogramma egg parasitoids as a potential component of pest management have mainly been tested and developed in two countries: Tunisia and Egypt. In greenhouse tomatoes in southwestern Tunisia, a release rate of 40 Trichogramma cacoeciae Marchal (Hymenoptera: Trichogrammatidae) adults per plant significantly reduced T. absoluta crop damage by 75% (Zouba and Mahjoubi 2010). Similarly, releasing a total of 25,000 individuals of either indigenous parasitoid T. cacoeciae or Trichogramma bourarachae Pintureau & Babault per greenhouse (480 m2 with a density of 3 plants per m2) per week in southwestern Tunisia resulted in a reduction of either 78% or 87% in T. absoluta mines on tomato leaves, respectively (Zouba et al. 2013). In northern Egyptian tomato greenhouses, El-Arnaouty et al. (2014) demonstrated that releases of either parasitoid Trichogramma euproctidis (Girault) or Trichogramma achaeae Nagaraja & Nagarkatti (50 or 75 parasitoids per m2) resulted in significant decrease of T. absoluta mines in greenhouses. However, in greenhouse tomato crops located in the same region in Egypt, releases of T. achaeae at a rate of 50 adults/m² significantly decreased number of T. absoluta larvae and mines on tomatoes (Kortam et al. 2014). As such, two releases of Trichogramma evanescens (Westwood) (about 190,000 parasitoids per ha) at seedling stage significantly reduced tomato leaf and fruit damage in Egyptian open-field conditions (Rizk 2016). In protected and open-field tomato crops of the Cap-Bon region, the largest tomato-producing area in Tunisia, Cherif et al. (2019a, b) provided evidence that three weekly releases of 20 T. cacoeciae adult parasitoids per plant significantly reduced pest’s life stage densities and infestation rates caused by T. absoluta, implying that T. cacoeciae could be a promising biocontrol candidate of T. absoluta in conditions of northeastern Tunisia. More recently, field releases of T. evanescens at a rate of 1,500 parasitized eggs per card decreased the number of T. absoluta eggs on tomatoes under plastic tunnels in Giza governorate, northern Egypt (Abdel-Razek et al. 2019).

In some Asian Middle Eastern countries, mainly Turkey and Iran, egg parasitoids have been released alone or in combination with either predators (see the sub-Sect. 2.3) or other biorational tools (see the Sect. 5). In tomato greenhouses in western Turkey, twelve (seven in autumn and five in spring) releases of 75 T. evanescens parasitoids/m2, repeated twice per week, were not sufficient to generate promising control results of egg and larval densities of T. absoluta on tomatoes (Keçeci and Öztop 2017).

In contrast to egg parasitoids that have been commercially released in tomato-producing areas in the MENA region and resulted in promising pest control, releases of larval parasitoids have not been sufficiently tested and developed as a powerful control tactic of T. absoluta in this geographical area. In all other concerned areas around the world, including South America and Europe, releases of larval and pupal parasitoids are not yet recommended as an effective control approach to control T. absoluta in tomato-producing areas where releasing egg parasitoids has been shown to be the most successful biological control approach (Calvo et al. 2016; Bodino et al. 2019; Ferracini et al. 2019).

Releases of predators

Releasing Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) has been a promising IPM option adopted against T. absoluta in Moroccan greenhouses where one or two releases of this predatory mirid at a rate of 1.5–2 individuals per m2 are generally recommended after plantation (Elaini 2011; Ouardi et al. 2012). Macrolophus caliginosus Wagner (Hemiptera: Miridae) released respecting a density of 1–2 per m2 after planting is among the IPM tools suggested for controlling T. absoluta in Iran (Baniameri and Cheraghian 2012). Likewise, releases of the predator M. caliginosus at a rate of 1–2 adult(s) per m² induced significant reduction in number of T. absoluta larvae and mines on tomato leaves in northern Egyptian greenhouses (Kortam et al. 2014). Either N. tenuis preplant augmentation with one egg per tomato seedling or augmentative release of commercially reared N. tenuis with one adult per plant released one month after planting was as effective as application of conventional insecticides, reducing T. absoluta densities and preventing crop damage in open-field tomatoes in Israel (Shaltiel-Harpaz et al. 2016). One release of N. tenuis at a rate of 2 adults per m2 significantly reduced T. absoluta egg and larval densities infesting fruits in greenhouse tomato crops in western Turkey (Keçeci and Öztop 2017). Moreover, releasing the mirid bug N. tenuis before establishment of T. absoluta was shown to be more effective in enhancing overall tomato yield than releasing it after pest establishment in Iranian plastic greenhouse tomato crops (Mirhosseini et al. 2019). Lately, releases of an indigenous strain of N. tenuis at 2 adults per m2 geothermal greenhouse in Kebili (South-West Tunisia) was by far more effective in eliminating all life stages of T. absoluta population, than an introcuded strain of this predatory species (Ettaib et al. 2019). This finding clearly indicates that, to effectively controlling T. absoluta, it would be more practical and promising to release native strain of the predator N. tenuis that are already well adapted to the specific abiotic conditions of geothermal greenhouses in southern Tunisia.

Similarly to the MENA region, in South America and Europe, some predators, mainly including the mirid bugs N. tenuis, Macrolophus pygmaeus (Rambur), and M. basicornis (Stål), have been released in greenhouse and/or open-field tomatoes and showed promising performance in controlling T. absoluta populations (Michaelides et al. 2018; Van Lenteren et al. 2018b; Ferracini et al. 2019). However, it is worth mentioning that despite the proven effectiveness of N. tenuis in controlling T. absoluta populations, previous studies provided evidence that this predatory mirid can also be considered as an insect pest seriously damaging host tomato crops (Arnó et al. 2010; Pérez-Hedo and Urbaneja 2016; Siscaro et al. 2019), implying that more attention should be paid to the possible phytophagous behavior of this predator before releasing it in tomatoes. In this context, N. tenuis phytophagy mitigation strategies, such as the use of tolerant varieties (Siscaro et al. 2019), of alternative food (e.g. tomato plants with sugar dispensers for attracting the damaging predatory nymphs) and/or plants including, for example, Dittrichia viscosa L. (Asteraceae) and Sesamum indicum (L.) (Pedaliaceae) (Biondi et al. 2016; Urbaneja-Bernat et al. 2019), have yet to be implemented in the MENA region to further reduce damage caused mainly by nymphs of this zoophytophagous mirid.

Combined releases of parasitoids and predators

Combined « parasitoid + predator » releases in the MENA region were mainly tested in Asian Middle Eastern countries including Turkey and Iran.

In greenhouses in the Mediterranean region in Turkey, numbers of T. absoluta eggs and larvae were significantly lower in plots with the combination « parasitoid T. evanescens + predatory bug N. tenuis », which significantly enhanced crop yield, relative to plots with releases of either natural enemy alone (Öztemiz 2013). Similarly, thirteen combined releases of the parasitoid T. evanescens and the predatory mirid N. tenuis were proven to significantly reduce T. absoluta population densities and fruit infestation in greenhouse tomatoes in the western Mediterranean region of Turkey (Keçeci and Öztop 2017). In some circumstances, this category of combined releases would not generate success in controlling T. absoluta. For example, combined releases of the mirid bug N. tenuis with the egg parasitoid Trichogramma brassicae (Bezdenko) (Hymenoptera: Trichogrammatidae) were not sufficiently effective against T. absoluta, as compared with single releases of the predator N. tenuis before pest establishment that significantly decreased damage and enhanced tomato yield in plastic greenhouse conditions in Iran (Mirhosseini et al. 2019). In fact, intraguild predation or competition (Cabello et al. 2012, 2015; Perdikis et al. 2014), which is a particular case of behavioral interaction (interference) between either a parasitoid and a predator or even two predators, may occur and could hamper the overall effectiveness of the released natural enemy (Chailleux et al. 2013; Naselli et al. 2017). In this context, Mohammadpour et al. (2019) provided evidence that the increasing age of T. absoluta eggs parasitized by T. brassicae decreased the intensity of intraguild predation between the predatory bug Nabis pseudoferus (Remane) (Hemiptera: Nabidae) and the parasitoid T. brassicae. Accordingly, these authors suggested the integration of both natural enemies in biological control programs of T. absoluta in tomatoes in Iran, respecting the condition that the first release of this predator should be carried out about three days after the parasitoid (T. brassicae) release, preventing the predator from consuming T. absoluta parasitized eggs.

Application of botanical insecticides

Botanical pesticides based on plant essential oils, characterized by repellent, insecticidal, and growth-reducing effects on a wide range of crop pests, but also showing constraints (i.e. flammability, phytotoxicity, poor water solubility) affecting their effective use, have long been considered among the most effective and environmentally safe pest control tools, applied as sustainable alternative to broad-spectrum synthetic pesticides (Campolo et al. 2017, 2018, 2020; Benelli et al. 2019a, b; Giunti et al. 2019; Petrović et al. 2019; Soares et al. 2019; Isman 2020). Application of biopesticide active substances to cope with problems caused by insect pests has been gaining increasing importance over the two last decades, which has also been consistent for refining IPM programs against the invasive T. absoluta in several countries including, among others, those of the MENA region (Table 2).

Table 2 Effective botanical insecticides tested, recommended or implemented alone in integrated pest management programs against Tuta absoluta in the MENA region
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In greenhouse conditions of Kafr El-Sheikh (northern Egypt), treatments based on either Artemisia cina Berg & Schmidt extract (500 ppm) or clove oil (500 ppm) extracted from Syzigium aromaticum (L.) were effective in reducing T. absoluta larvae and mines. Consequently, these natural active substances could be suggested as possible potential ecofriendly control tools of T. absoluta in Egypt (Derbalah et al. 2012). Similarly, clove oil (S. aromaticum) applied at 0.1 µL L− 1 significantly reduced numbers of insect larvae and overall infestation rates of tomatoes by T. absoluta in semi-field conditions, implying that this natural active substance can be used to control this pest as a sustainable alternative to the application of traditional chemical pesticides in Egypt (Ebadah et al. 2016). In the same context, laboratory bioassays showed that essential oil of S. aromaticum buds caused 100% mortality of T. absoluta larvae, thereby it has been proposed as suitable biopesticide to control this pest in Morocco (Benchouikh et al. 2016). High mortality rates of T. absoluta second instar larvae were obtained in laboratory conditions, following application of either plant extract grown in South-West Morocco (Souss region): leaves of Thymus vulgaris L. causing 97% mortality or seeds of Ricinus communis L. inducing 80% mortality (Ait Taadaouit et al. 2012). Increased doses of essential oils extracted from peels of Citrus aurantium L. significantly increased mortality percentage of T. absoluta third instar larvae; thereby applying such natural active substances as botanical insecticide could enhance T. absoluta management programs in greenhouse tomatoes in Tunisia (Zarrad et al. 2013). Moreover, under field conditions in Minia Governorate (Upper Egypt), foliar application of either garlic extract (Allium sativum L.) at 5 mL L− 1, lemon grass extract (Cymbopogon citratus Stapf) at 25 gm L− 1 or Basil (Ocimum basilicum L.) essential oil at 0.5% significantly reduced numbers of T. absoluta mines per plant and tomato foliar damage, which significantly improved the quality of fruit yield (Hussein et al. 2015). Laboratory bioassays showed that azadirachtin applied at 1 mL L− 1 generated promising efficacy against T. absoluta larvae inside tomato leaf mines, causing 92% insect mortality, hence farmers are encouraged to use this botanical insecticide in IPM programs against T. absoluta in Egypt (Abd El-Ghany et al. 2016). More recently, field experiments in Bani Sweif Governorate (Upper Egypt) spraying infested tomatoes with either rosemary oil (Rosmarinus officinalis L.) or thyme oil (T. vulgaris) reduced T. absoluta larval populations by more than 80%. Consequently, these plant extract active substances could be applied for controlling T. absoluta in Egypt as alternative to treatments with conventional chemical pesticides (Sammour et al. 2018). In the same country, the botanical extract azadirachtin applied 5 mL L− 1 ha− 1 showed 70–83% reduction in T. absoluta larval densities and improved crop yield in greenhouse conditions in northern Egypt (Abdel-Ghany et al. 2018).

In addition to North African countries of the MENA region, plant extracts acting as insecticides have also been tested and, whenever appropriate, implemented in Asian tomato-producing areas of this region. Field application of Melia azedarach L. plant extracts at 3 mL L− 1 in Homs region (Syria) resulted in 84.48% efficacy on T. absoluta larvae in tomatoes (Ibrahim et al. 2011). Likewise, aqueous extracts of indigenous M. azedarach applied as a powder formulation caused significant decrease of eggs, larvae, pupae and newly emerging T. absoluta moths under laboratory conditions. Therefore, this botanical formulation could be recommended to be used, at field rate of 2/3 kg in 1,000 ppm per 1,500 L ha− 1 in consecutive applications on plants infested with T. absoluta in Lebanon (Hammad et al. 2019). Applying azadirachtin, registered as an emulsifiable concentrate or wettable powder, every week after detection of infestation and < 10 moths per pheromone trap per week is an IPM tactic proposed to control T. absoluta in Iran (Baniameri and Cheraghian 2012). As such, azadirachtin applied at 3 g L− 1 reduced numbers of first instar larvae by 70–86% under laboratory conditions (Jallow et al. 2018). Simmondsin extracted from jojoba seeds by acetone and water signifcantly reduced T. absoluta second instar larvae in laboratory conditions, and accordingly they could be integrated in programs for controlling T. absoluta in organic farming in Saudi Arabia (Abdel-Baky and Al-Soqeer 2017). Besides, seed essential oils extracted from cardamom (Elettaria cardamomum (L.)) and applied at 3 (outside leaf) or 10 (inside leaf) µL L− 1 of air exhibited high toxicity potential against second instar larvae of T. absoluta; therefore they could be used in sustainable management of this pest in Iranian greenhouse tomato crops (Chegini and Abbasipour 2017). Applying NeemAzal® (azadirachtin) at 3 mL L− 1 in a 15-day frequency proved to be an effective biorational control option against T. absoluta in Lebanese tomato greenhouses where it induced significant reduction in numbers of mines on leaves, larvae and percent of damaged fruits (El Hajj et al. 2017). Lately, based on laboratory bioassays, Piri et al. (2020) demonstrated that application of Ajwain (Carum copticum L.) essential oil exhibited a significant poential in controlling fourth instar larvae of T. absoluta, which might constitute a future promising biorational option to control this pest in Iran.

Application of microbial insecticides

Over the last decades, applying biopesticides that are issued from different microbials such as fungi, bacteria and viruses has been regarded as a powerful effective and environmentally sound control option against a wide range of insect pest species (Van Driesche et al. 2008; Chandler et al. 2011; Czaja et al. 2015; Arthurs and Dara 2019; De la Cruz Quiroz et al. 2019; Tahir et al. 2019) including the pinworm T. absoluta (Biondi et al. 2018). Overall, among several active organisms used, the most applied and successful microbial pesticide in the MENA region was that based on various Bacillus thuringiensis strains (Table 3).

Table 3 Effective microbial insecticides tested, recommended or implemented alone in integrated pest management programs against Tuta absoluta in the MENA region
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Either microbial biopesticide B. thuringiensis applied at 4.5 g L− 1 or spinosad, a product based on the soil actinomycete Saccharopolyspora spinosa (Metz and Yao), applied at 1 mL L− 1 generated satisfactory control of T. absoluta larvae infesting leaves in greenhouse tomatoes of northeastern Tunisia (Grissa-Lebdi et al. 2011). However, in Tunisian semi-natural conditions, B. thuringiensis var. kurstaki applied at 2.5 g L− 1 provided promising control performance (mortality > 70%) on first, second and third instar larvae of T. absoluta (Hafsi et al. 2012). Culture filtrate of B. thuringiensis (500 ppm) applied under northern Egyptian greenhouse conditions was effective against T. absoluta in tomatoes where it decreased numbers of larvae and mine blotches (Derbalah et al. 2012). Satisfactory efficacy against T. absoluta larvae was observed in tomato greenhouses in Esfahan (Iran) after application of B. thuringiensis var. kurstaki (Baniameri and Cheraghian 2012). The biosurfactant Bacillus amyloliquefaciens AG1, causing serious histological damages in the larval midgut of T. absoluta (Ben Kheder et al. 2015) and the vegetative insecticidal protein B. thuringiensis Vip3Aa16, inducing a microvillus damage and an epithelial cell rupture in T. absoluta third instar larva midguts, cessation of feeding, body retraction, overall paralysis, and death of several larvae (Sellami et al. 2015) are further promising active substances that could be incorporated in IPM programs of T. absoluta in Tunisia. Applying B. thuringiensis or the entomophatogenic fungus Metarhizium anisopliae at 2 g L− 1, and spinosad at 0.75 mL L− 1 provided promising control of T. absoluta larvae and reduced their damage in open-field tomatoes in Menoufia Governorate, northern Egypt (El-Aassar et al. 2015). As such, application of B. thuringiensis (1 g L− 1) at 10-day frequency generated promising results in limiting damage caused by T. absoluta larvae on leaves and fruits in tomato greenhouses in Lebanon (El Hajj et al. 2017). Lately, B. thuringiensis var. kurstaki at 0.5 g L− 1 and Beauveria bassiana at 1.5 g L− 1 induced 55–65% and 45.5–58.5% mortality of T. absoluta second instar larvae, respectively, based on laboratory bioassays (Jallow et al. 2018). A commercial formulation of B. thuringiensis var. kurstaki (IAB Bt), a bioinsecticide available as a wettable powder with a concentration of 32000 IU g− 1, and registered against some lepidopteran pests in Algeria showed a high efficacy in controlling T. absoluta larval stages (particularly the youngest ones) under laboratory conditions, when applied at either concentration 500, 650 or 800 ppm (Harizia et al. 2019).

According to Baniameri and Cheraghian (2012), applying the biopesticide spinosad at 200–250 mL ha− 1 in the case of 10 moths (or more) caught per trap per week is a recommended control tool of T. absoluta in Iran. In greenhouse tomatoes of Center-East Tunisia, either microbial spinosad applied at 0.6 mL L− 1 or commercial formulation of Verticillium lecanii (Biocatch®) applied at 1 mL L− 1 was effective in controlling T. absoluta larvae (Braham et al. 2012). Laboratory bioassays showed that spinosad applied at its recommended dose in Turkey (120 mg L− 1) resulted in 100% larval mortality (Dağlı et al. 2012). Under open-field tomatoes in Kalyobiya Governorate (northern Egypt), spinosad applied at either 238 or 285 mL ha− 1 for controlling T. absoluta was more effective in decreasing infestations on tomato leaves than some chemical insecticides such as pyridalyl, indoxcarb, chlorantraniliprole and chlorfenapyr (Hanafy and El-Sayed 2013). Based on field studies in Sharkia governorate (northern Egypt), spinosad sprayed every 10 days during two months at 0.2 mL L− 1 was effective in controlling T. absoluta larvae on leaves, which consequently reduced the percentage of infested tomato fruits (Soliman 2015).

Laboratory experiments demonstrated that either entomopathogenic fungus B. bassiana, M. anisopliae or V. lecanii applied at 107 conidia mL− 1 was effective against one or more life stage(s) of T. absoluta: B. bassiana and M. anisopliae being effective on both eggs and first instar larvae, whereas V. lecanii was effective on first and third instar larvae (Abdel-Raheem et al. 2015). Such findings would be useful for incorporating pesticide treatments based on these microbials in IPM programs of T. absoluta in Egypt. As such, either microbial active substance spinosad (0.6 or 0.3 mL L− 1) or B. bassiana (5 × 105 spore per m2) exhibited outstanding efficacy against T. absoluta larvae inside and outside tomato treated leaf mines, thereby applying these substances could be an effective biorational tool for farmers for managing T. absoluta in Egypt (Abd El-Ghany et al. 2016). Laboratory experiments showed that a spontaneous mutant of a local strain of B. bassiana was very effective against T. absoluta larval populations, which could be a strong basis for developing of a bioinsecticide to control controlling T. absoluta in Tunisia (Borgi et al. 2016). Moreover, Ben Tiba et al. (2019) provided evidence that, under laboratory conditions, a local isolate of Phthorimaea operculella granulovirus (PhopGV Tu1.11) exhibited potential toxicity on T. absoluta larvae, which could be developed and incorporated as a biopesticide active substance in IPM programs against T. absoluta in Tunisia. Spinosad sprayed at 0.3 mL L− 1 ha− 1 and B. thuringiensis var. kurstaki applied at 2 g L− 1 ha− 1 were proven to be the most effective microbial pesticides, causing respectively 78–97% and 78–91% reduction in T. absoluta larval population and enhancing crop yield, as compared to either entomopathogenic fungus M. anisopliae at 5 mL L− 1 ha− 1 or B. bassiana at 5 mL L− 1 ha− 1), causing 46–75% reduction in larval densities in northern Egyptian greenhouses (Abdel-Ghany et al. 2018).

Although some microbial-based pesticides proved to be effective against T. absoluta, previous research studies provided evidence that the application of some active substances could exert some serious constraints. Indeed, spinosad for example was shown to present adverse lethal effects on adults and pupae of the ectoparasitoid Bracon nigricans Szépligeti (Hymenoptera: Braconidae), and sublethal effects on the predators Orius laevigatus Fieber (Hemiptera: Antocoridae) and M. pygmaeus (Hemiptera: Miridae), in contrast to the harmless B. thuringiensis (Biondi et al. 2012, 2013; Ricupero et al. 2020), as well as on the egg parasitoid T. brassicae (Parsaeyan et al. 2020). Additionally, spinosad can show high resistance in its target T. absoluta populations (Campos et al. 2014), which could result in control failure, compromising pest management objectives.

Different combinations of biorational control tools

In addition to combining releases of parasitoids with predators, other categories of combinations were also tested against T. absoluta before to be implemented in IPM programs throughout the MENA region. These combinations include (i) « natural enemy release + botanical pesticide », (ii) « natural enemy release + microbial pesticide », (ii) natural enemy release + entomophatogenic nematode », (iv) « natural enemy release + pheromone-based mass trapping », and (v) « microbial pesticide + botanical pesticide » (Table 4).

Table 4 Promising combinations of various biorational control tools tested, recommended or implemented in integrated pest management programs against Tuta absoluta in the MENA region
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Releasing 25 T. achaeae adult parasitoids per m² in combination with release of the predatory mirid M. caliginosus at 1–4 adult(s) per m² and application of the microbial pesticide B. thuringiensis at 1 g L− 1 resulted in notable reduction in T. absoluta larvae and mines on tomato plants in northern Egyptian greenhouse conditions (Kortam et al. 2014). In other cases, applying the microbial insecticide B. thuringiensis in combination with releasing the egg parasitoid T. evanescens and pheromone mass trapping generated significant decrease in T. absoluta larval densities and crop damage in northern Egyptian (Kafrel-Sheikh Governorate) open-field tomatoes (Khidr et al. 2013). Likewise, four releases of T. evanescens parasitoids at about 190,000 ha− 1 combined with bioinsecticide (Protecto and Spinosad bait) applications against T. absoluta induced a significant reduction in leaf and fruit damages in Egyptian open-field tomatoes (Rizk 2016).

In Iranian greenhouse tomato crops, releases of either egg parasitoid Trichogramma embryophagum (Hartig) (Hymenoptera: Trichogrammatidae) or T. brassicae in combination with applying B. thuringiensis significantly reduced T. absoluta larval densities and leaf mines (Alsaedi et al. 2017). As such, releases of T. brassicae in combination with spinosad treatment, or the biopesticide combination “spinosad + B. thuringiensis” significantly decreased both T. absoluta densities and related leaf mines on tomato crops in Iranian greenhouse conditions (Jamshidnia et al. 2018). On the other hand, in commercial tomato plastic greenhouses in northern Egypt, Adly and Nouh (2019) showed that the combined use of the parasitoid T. euproctidis (weekly releases of 50 parasitoids per m2) and the entomopathogenic nematode Heterorhabditis bacteriophora strain HP88 decreased density of T. absoluta larvae gradually until the end of the season, and accordingly they recommended this combination to be integrated as a main component of pest management against T. absoluta in Egyptian greenhouse tomato crops. Moreover, biweekly releases of Trichogrammatoidea bactrae Nagaraja (Hymenoptera: Trichogrammatidae) (143,000 and 238,000 parasitoids ha− 1) in combination with pheromone-mass trapping significantly reduced infestation levels and resulted in higher yield rates in open-field tomato crops in Egypt (Goda et al. 2015). In this context, Ahmadi and Poorjavad (2018) showed that neither T. evanescens nor T. brassicae prarasitoids (1,000 released individuals for each species) were caught in sticky delta traps baited with T. absoluta sex pheromone in greenhouses in Iran, which apparently indicate a possible compatibility between both pest control tools whenever applied in combination. Based on laboratory experiments, it was proven that using the combination « predator N. pseudoferus + entomopathogenic fungus M. anisopliae » could show promise in pest management programs of T. absoluta in Iran, however experiments in field (natural) conditions are needed to confirm these preliminary laboratory findings (Alikhani et al. 2019).

Regarding combinations involving microbial and botanical insecticides, field studies in Iran demonstrated that using of B. thuringiensis var. kurstaki in combination with the botanical active substance azadirachtin generated the highest long term effect on T. absoluta larval abundance as well as on induced leaf and fruit damage (with 100% reduction), as compared to applying each biopesticide alone (Nazarpour et al. 2016). Spraying the botanical neem Azal (3 mL L− 1) in combination with the microbial B. thuringiensis (1 g L− 1) significantly reduced T. absoluta larval populations as well as damage on leaves (mines) and fruits in Lebanese greenhouse tomatoes (El Hajj et al. 2017).

Likewise, in the absence of any releases of natual enemies, applying of the combination «azadirachtin (6.857 L ha− 1) + B. thuringiensis var. kurstaki (11.428 L ha− 1)» showed potential control effect since it significantantly reduced T. absoluta larval densities and improved healthy yield production in northern Egyptian open-field tomato crops (Khidr et al. 2013). In commercial polycarbonate greenhouses in Waffra (southern Kuwait), either combination « azadirachtin (3 g L− 1) + B. thuringiensis (0.5 g L− 1) » or « azadirachtin (3 g L− 1) + B. bassiana (1.5 g L− 1) » induced significant decrease in T. absoluta larval mines on leaves and significantly reduced the number of damaged fruits, thereby improved tomato crop yield. These findings represent a strong indication that such microbial-based combinations could be sucessfully incorporated in IPM programs against T. absoluta in greenhouses tomatoes in Kuwait as well as in other Middle Eastern countries (Jallow et al. 2018).

Conclusion and future directions

Since its first detection in 2008 in the MENA region, more specifically in North Africa, and its further spread to Middle Eastern Asian countries, farmers have been facing serious tomato crop health problems coupled with substantial annual economic losses posed by the destructive pest T. absoluta. In an attempt to effectively manage this new threat to tomato industry, various control tools were tested, and whenever possible implemented in IPM programs, in different MENA countries located either in northern Africa or south-western Asia. In general, IPM programs against T. absoluta in the MENA region have been relied heavily on applying effective but hazardous synthetic chemical pesticides that could exert adverse side effects on beneficial arthropods, coupled with the pest’s high potential for developing insect resistance to a number of chemical substances. However, fortunately, in the few last years, it has become evident due to growing awareness linked to these alarming realities, that using biorational approaches as alternative to the the injudicious use of such synthetic pesticides is of foremost importance for ensuring sustainable management of this pest. Among biorational tactics considered as alternative to hazardous chemicals, biological control using egg and/or larval parasitoids has always been considered as sustainable component of IPM programs against T. absoluta in the MENA region. Importantly, it is necessary to know which are the parasitoid species that have great potential in reducing T. absoluta densities in tomatoes, in which conditions these species could be released, and which are the most recommended release rates of the species to be used for optimizing their field effectiveness. Additionally, notable advances in efforts focused on environmentally-sound management of T. absoluta based on either microbial or botanical (plant extract) pesticides have been at the forefront since the first report of the pest in the MENA region. In this context, different control scenarios have been adopted alone or combined with other ecofriendly options (natural enemy release and/or pheromone-mass trapping), depending on the agro-ecosystem nature and conditions in each concerned tomato-producing region. However, in some cases, such biorational approaches might have serious weaknesses such as failures in controlling the pest or detrimental side effects on human health, environment and non-target beneficial organisms. Accordingly, special attention should be paid to such possible serious constraints when developing and implementing IPM programs against this pest in the MENA region, and it is necessary to remain as vigilant as possible regarding this issue. Ideally, the performance of further novel biorational options should be carefully and thoroughly investigated by scientists belonging to the MENA region in the near future, in strong collaboration with farmers as well as with decision-making and policy-maker professionals.