Key message

  • Several commonly found native plants in the Mediterranean basin exhibit a valuable insecticidal activity against several insects of vegetable crops.

  • The development of suitable formulations of biopesticides, such as capsule suspensions, will be crucial in terms of increasing the effectiveness of natural-based insecticides in conjunction with their increased residual effect.

  • The application of natural resource-based biopesticides such as plant extracts can be further exploited for insect control, but many steps need to be made toward their wide use by farmers.

Introduction

The use of conventional insecticides is currently the main strategy for insect control in crop protection. This strategy gradually shifted to an integrated pest management (IPM) approach, which includes the simultaneous use of other means of control as well, and partially alleviates the risks that are related to resistance development of various insects to insecticides and the adverse effects that many insecticides have for human health and the environment (Alyokhin et al. 2015; Pretty and Bharucha 2015; Allahyari et al. 2016). In this regard, in IPM-based programs, high levels of insect control are still required, but in this case through the reduced use of conventional pesticides. In comparison with synthetic insecticides, many natural insecticides or biopesticides are less toxic for mammals and safer for both consumers and non-target beneficial organisms, such as predators and parasitoids (Gaspari et al. 2007; Walia et al. 2017). However, the number of commercial biopesticides remains extremely low (Pavela and Benelli 2016). In this regard, the use of natural insecticides is an eco-friendly approach for insect control and for this reason these compounds should be the target of research in the coming decades, in conjunction with more intensive farmers’ training. This effort starts from the production of standardized natural insecticides (Walia et al. 2017). At the same time, the insecticidal activity of these compounds should be increased through the development of suitable formulations. Furthermore, it is important to optimize the extraction methods, for which there are still disproportionally few data (Pavela and Benelli 2016). Finally, it is important to select genotypes with high content of compounds with insecticidal activity.

Based on the above, this article aims to provide an up-to-date overview for the most important plant species commonly found in the Mediterranean region with insecticidal activity against the main insects of vegetable crops in order to expand the available knowledge regarding the potential spectrum of natural insecticides. In the recent years, several review papers have been published covering similar topics (Pavela and Benelli 2016; Pavela 2016; Isman 2020). In parallel with other studies, this review mainly focuses on native plants of the Mediterranean basin, which, according to the results of various experiments, exhibits a remarkable insecticidal activity against serious pests of vegetable crops. Given its unique complex of ecosystems and the remarkably high number of indigenous plants, the Mediterranean region is considered as an ideal target area for selecting plant species that have a noticeable insecticidal value. Moreover, indigenous plant use for different purposes, such as food, feed, medicine and crop protection, has been followed for thousands of years in this area, and it seems, historically, much more developed than any other eco-zone in earth. In the last years, several commercial botanical insecticides based on plant essential oils or other compounds such as azadirachtin, rotenone, nicotine, pyrethrins have been developed and registered in several countries (Siegwart et al. 2015; Pavela 2016; Grieneisen and Isman 2018; Isman 2020).

An extremely large variety of extracts or essential oils from native plants of the Mediterranean region have a considerable insecticidal value against important pests of vegetable crops (Table 1), and thus, their evaluation toward this direction should be investigated more thoroughly, in order to draw the inferences necessary for the development of new natural-based insecticides. It is important to point out that natural insecticides possess a wide spectrum of biological activity against insects (Table 2); this activity includes antifeedant, deterrent, repellent, effects, as well as growth inhibition, and negative effects on both fecundity and longevity of the target species. In addition, many of these compounds pose combined mode of action in different sites, which are often different than those of the conventional insecticides and, thus, could be used with success for the control of species that are resistant to certain chemicals. Moreover, some of these compounds are able to control multiple life stages of certain pests, i.e., eggs, larvae, pupae and adults, which consist an additional indication of their multiple biological activity. Indicatively, multiple targeted activity may be directly linked with multiple mode of action, given that different life stages may be affected in a different way, e.g., egg hatch may be affected in a different way than larval growth.

Table 1 Natural insecticides from plants commonly found in the Mediterranean region against pests of vegetable crops
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Table 2 Effects of natural insecticides from native plants of the Mediterranean basin on pests of vegetable crops
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Therefore, extracts or compounds from some native plants of the Mediterranean region, alone or in mixtures with other substances that are already used as active ingredients in commercial botanical insecticides, could be used for the development of new products which can be applied for crop protection in both organic and conventional agriculture. The review concludes by suggesting future requirements and perspectives for increasing the effectiveness and consequently the use of natural insecticides in crop protection. To our knowledge, this is the first review article toward this direction that aims to collect different scattered information on the subject.

Control of important insects of vegetable crops with natural insecticides

In the following section the insecticidal activity and the mode of action of extracts from the native species of the Mediterranean basin (Table 3), against the most important pests of vegetable crops, will be presented in order to reveal their potentials in vegetable protection. For this purpose, we have divided the species that are to be presented according to their target insect species, which are grouped in orders, by using paradigms of insects that have high economic importance for vegetables, separately for each order.

Table 3 Important weeds and other native plants of the Mediterranean basin with insecticidal properties
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Coleoptera

The Colorado potato beetle, Leptinotarsa decemlineata (Say), is one of the most destructive pests in several horticultural crops, such as potato, eggplant and tomato (Tajmiri et al. 2017; Wang et al. 2017). Its control is mainly based on application of synthetic insecticides such as chlorantraniliprole, imidacloprid, metaflumizone, lambda-cyhalothrin and thiamethoxam (Hitchner et al. 2012; Jiang et al. 2012; Ropek and Kołodziejczyk 2019), while there are numerous cases of resistance development (Mota-Sanchez et al. 2006; Szendrei et al. 2012). Biopesticides such as plant extracts from the native species [white false hellebore, Veratrum album L. (Melanthiaceae), common hop, Humulus lupulus L. (Cannabaceae) and common nettle, Urtica dioica L. (Urticaceae)] of the Mediterranean region possess antifeedant, larvicidal and adulticidal properties against this species, for both larval and adult stage (Gökçe et al. 2006; Aydin et al. 2014; Ertürk and Sarikaya 2017). Veratrum album is a toxic plant containing steroidal alkaloids that cause poisoning in humans, while it is easily mistaken for yellow gentian, Gentiana lutea L. and wild garlic, Allium ursinum L. (Zagler et al. 2005; Gilotta and Brvar 2010; Dumlu et al. 2019; Kikkawa et al. 2019). Aydin et al. (2014) observed that extracts of V. album rhizomes exhibited 100% mortality against adults of L. decemlineata in just 24 h, while these extracts were more toxic than those of their compounds jervinem, oxyresveratrol and β-sitosterol 3-O-β-D-glucopyranoside alone. Due to its toxicity to humans, it is important to check whether the vegetables that are sprayed with extracts of this plant will cause poisoning or serious health disorders.

Humulus lupulus is perennial species native in Mediterranean basin. The female inflorescences of H. lupulus have been used in traditional folk medicine and contain several compounds such as xanthohumol and 8-prenylnaringenin (Zanoli and Zavatti 2008), while according to Gökçe et al. (2006) and Alkan et al. (2015) extracts from this plant part exhibited insecticidal effects against L. decemlineata. Specifically, Gökçe et al. (2006) found that first- to third-instar larvae of L. decemlineata were very susceptible to H. lupulus extracts. The insecticidal activity of this species may be due to the compounds xanthohumol and isoxanthohumol (Aydin et al. 2017; Stompor et al. 2015). Aydin et al. (2017) reported that the compound xanthohumol was more toxic against stored pests than the extracts from inflorescences, while Stompor et al. (2015) reported that isoxanthohumol and prenylflavonoid isolated from this species also exhibited considerable insecticidal activity. Regarding the insecticidal activity of U. dioica Mateeva-Radeva (1997) reported that extracts from this species caused mortality between 75 and 85% on young larvae of L. decemlineata.

Other plant species that possess insecticidal activity against L. decemlineata are the oriental sweetgum, Liquidambar orientalis L. (Altingiaceae) and the common box, Buxus sempervirens L. (Buxaceae). Liquidambar orientalis is a tree native in the eastern Mediterranean zone and has significant antioxidant properties, since it contains several phenolic compounds such as protocatechuic acid, (−)-epicatechin and gallic acid (Saraç and Şen 2014). Moreover, the essential oil from this species presents a wide variety of compounds such as trans-cinnamyl alcohol, hydrocinnamyl alcohol, β-caryophyllene, styrene, benzyl alcohol and α-pinene (Park 2014). Recently, Ertürk and Sarikaya (2017) found that extracts from L. orientalis were both toxic and antifeedant on L. decemlineata. This activity may be due to the compounds trans-cinnamyl alcohol and hydrocinnamyl alcohol, since according to Park (2014) both compounds exhibited insecticidal effects against the Japanese termite, Reticulitermes spearatus (Kolbe).

Buxus sempervirens is a widespread Mediterranean species (de Jong et al. 2012) that contains several steroidal alkaloids (Loru et al. 2000). Regarding the biological properties of the extracts of this species, Ertürk and Sarikaya (2017) reported that these extracts displayed insecticidal activity against L. decemlineata. Several alkaloids (i.e., cyclobuxine-D, imperialine (−)-cyclomikuranine (3), (−)-cyclobuxophylline-K (4) and (+)-buxaquamarine) have been isolated so far from leaves and roots of this species (Ata et al. 2002; Eshonov et al. 2014), but their insecticidal properties are poorly understood and merit additional investigation. In a recent study, Kimbaris et al. (2017) reported that essential oils from pennyrile, Mentha pulegium L., showed insecticidal activity against L. decemlineata, since its feeding capacity was negatively affected by piperitenone and pulegone, the main components of essential oils of M. pulegium.

Diptera

The American serpentine leafminer, Liriomyza trifolii (Burgess), is a serious pest of several vegetable crops such as tomato and pepper in Europe and many other areas of the world (Stegmaier 1966; Kotze and Dennill 1996; Hernández et al. 2011). Several insecticides, such as abamectin and spinosad, have been tested for the control of this species, often with inconclusive results (Devkota et al. 2016). In addition, yellow sticky traps have been positively evaluated, as a part of IPM programs that could be used for mass trapping, but this technique may not be effective at high population densities (Durairaj et al. 2007).

To our knowledge, there is still inadequate information on the insecticidal activity of natural insecticides against this species. In this regard, extracts of plants from some species (squill, Urginea maritima (L.) Baker (syn. Drimia maritima (L.) Stearn), Asparagaceae) and myrtle spurge, Euphorbia myrsinites L. (Euphorbiaceae)) have been shown to be effective. Aqueous extracts from U. maritima and E. myrsinites exhibited both translaminar and systemic activity against L. trifolii (Civelek and Weintraub 2004). According to Hassid et al. (1976) the plants of U. maritima contain the compound azetidine-2-carboxylic acid, which has a noticeable insecticidal effect (Adeyeyé and Blum 1989). Okot-Kotber and Adeyeye (1997) reported that larvae of the corn earworm, Helicoverpa zea Boddie, treated with this compound have defective β-alanyldopamine synthetase. Recently, Maazoun et al. (2017) observed that the extracts from bulbs of U. maritima inhibited the acetylcholinesterase (AChE) activity, while the main compounds that isolated from bulbs were ferulic acid, vanillic acid and 4-hydroxybenzoic acid.

Hemiptera

Aphids and whiteflies are among the most important pests of several vegetable crops causing serious direct and indirect infestations. The peach-potato aphid, Myzus persicae (Sulzer), the cabbage aphid, Brevicoryne brassicae (L.), and the silverleaf whitefly, Bemisia tabaci (Gennadius) are three major pests that seriously infest several vegetable crops worldwide (Baysal and Çinar 2007; Jahan et al. 2013; Lima et al. 2017). In conventional agriculture, their control is mainly based on application of synthetic insecticides, while there are numerous cases of resistance development. In contrast, in organic agriculture the means available for the control of these species are rather limited.

Regarding the insecticidal capacity of plant-based insecticides, Jiang et al. (2018) observed that seed extracts from black locust (Fig. 1), Robinia pseudoacacia L. (Fabaceae), exhibited significant insecticidal activity against aphids (cotton aphid, Aphis gossypii Glover and B. brassicae) under both laboratory and field conditions. According to these researchers the main components in seeds of this species were 9,12-octadecadienoic acid (20.9%), followed by 9,12,15-octadecatrienoic acid methyl ester (14.3%) and 9,12-octadecadienoic acid methyl ester (10.9%). In another study, Soliman et al. (2005) reported that the leaf extracts from wavyleaf mullein, Verbascum sinuatum L. (Scrophulariaceae) were able to control A. gossypii. Similarly, Demnati and Allache (2014) tested powder from stems of this species and found a satisfactory level of efficacy against the cowpea weevil, Callosobruchus maculatus (F.).

Fig. 1
figure 1

Herbaceous and woody native plants with insecticidal properties commonly found in the Mediterranean basin: 1. Cyperus rotundus, 2. Ecballium elaterium, 3. Solanum elaeagnifolium, 4. Rosmarinus officinalis, 5. Silybum marianum, 6. Pallenis spinosa, 7. Echium italicum, 8. Robinia pseudoacacia and 9. Cercis siliquastrum

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The essential oils from several plant species belonging to Lamiaceae were particularly toxic on aphids. For example, essential oils from rosemary, Rosmarinus officinalis L., were antifeedant on M. persicae (Santana et al. 2014), while the essential oils from lemon balm, Melissa officinalis L., oregano, Origanum vulgare L., common thyme, Thymus vulgaris L. (Lamiaceae), fennel, Foeniculum vulgare Mill. anise, Pimpinella anisum L. (Apiaceae), and common vervain, Verbena officinalis L. (Verbenaceae) exhibited high mortality (> 90%) on M. persicae (Digilio et al. 2008). Similarly, Behi et al. (2019) reported that the essential oil from aerial parts of M. pulegium (Lamiaceae) and lentisk, Pistacia lentiscus L. (Anacardiaceae) caused mortality 94% and 74%, respectively, on A. gossypi. The main compounds of essential oil from leaves of M. pulegium and P. lentiscus were pulegone (45.89%), cis-menthone (23.25%) and α-pinene (2857%), β-myrcene (21.03%), respectively. Moreover, Gaspari et al. (2007) observed significant adverse effects of small nettle, Urtica urens L., extracts on aphid fecundity of the same insect species. At the same time, Stompor et al. (2015) reported that isoxanthohumol which is derived from H. lupulus is a strong deterrent against M. persicae. Similarly, the essential oil from Southern blue gum, Eucalyptus globulus Labill. (Myrtaceae) exhibit a valuable insecticidal activity against M. persicae (Castresan et al. 2013). This species is not native to Mediterranean zone, has been introduced to this area since the eighteenth century and is currently widely expanded in various regions (Silva-Pando and Pino-Pérez 2016; Badalamenti et al. 2018). Eucalyptus globulus can be a valuable source for the development of natural insecticides due to its high biomass production. Zewdie et al. (2009) reported that the dry leaves yield in a 9-year old plantation of E. globulus was 28 t ha−1.

In another study, Abou-Fakhr Hammad et al. (2014) found that extracts of mayweed, Anthemis scariosa Boiss., stems and leaves were both repellent and toxic against the adults and second nymphal instars of B. tabaci. Regarding the mode of action of essential oils from Asteraceace species such as absinthe, Artemisia absinthium L., Czerniewicz et al. (2018) noted that these essential oils decreased the activity of the enzymes acetylcholinesterase and Na+/K+-ATPase within the tissues of M. persicae. Artemisia absinthium contains a wide variety of terpenes such as camphor, B-Τhujone, camphene, 1,8-cineole, borneol, sabinene, b-Pinene, β-Myrcene, linalool (Bachrouch et al. 2015). Furthermore, Al-mazra’awi and Ateyyat (2009) reported that the plant extracts of fringed rue, Ruta chalepensis L. (Rutaceae), were lethal for B. tabaci. The insecticidal activity of this species could be attributed to essential oils constituents. Bedini et al. (2018) reported that the essential oil from R. chalepensis contains several ketones [i.e., 2-undecanone (12.7%) and 2-nonanone (56.7%)]. These researchers also reported that R. chalepensis essential oil exhibited larvicidal activity against the Asian tiger mosquito Aedes albopictus (Skuse). Finally, Al-mazra’awi and Ateyyat (2009) observed that the extracts from stems and leaves of spiny alkanet, Alkanna strigosa Boiss. & Hohen (Boraginaceae), were effective for the control of the B. tabaci. To our knowledge, there are no reports concerning the compounds from A. strigosa that exhibit insecticidal activity.

Thysanoptera

The onion thrips, Thrips tabaci (Lindeman) and the western flower thrips, Frankliniella occidentalis (Pergande), are very important pests of several vegetable crops worldwide causing serious infestations, while at the same time these species are vectors of important viruses, such as the Tomato Spotted Wilt Virus (van Rijn et al. 1995; Badillo-Vargas et al. 2012; Westmore et al. 2013). There are some studies that have examined the potential of extracts from plants, native in the Mediterranean basin, for the control of these species. For instance, Najmizadeh et al. (2013) observed that the plant extracts from seeds of wild rue, Peganum harmala L. (Nitrariaceae), pot marigold, Calendula officinalis L. (Asteraceae) and Judas tree, Cercis siliquastrum L. (Fabaceae) were very effective for the control of T. tabaci. Similarly, Razavi and Ahmadi (2016) found that plant extracts from P. harmala could be used with success against F. occidentalis. According to Nenaah (2011) the seeds of this species contain β-carbolines alkaloids (i.e., harmane, harmine and harmaline). Regarding the insecticidal activity of these compounds, Bouayad et al. (2012) reported that harmine caused a decrease in larval weight of the Indian meal moth, Plodia interpunctella (Hübner), as well as a dramatic reduction of α-amylase activity. The insecticidal activity of C. officinalis could be attributed to essential oils constituents. According to Khalid and Teixeira da Silva (2010) this species contains a wide variety of terpenes such as a-Cadinol, Δ-Cadinene, α-Eudesmol, a-Pinene and guaiol. The insecticidal activity of guaiol and several other terpenes such as camphor, 1,8-cineole, β-Pinene, linalool has been reported by several research groups (Rodilla et al. 2011; Gupta et al. 2017; Ortiz de Elguea-Culebras et al. 2017; Seixas et al. 2018), while regarding the mode of action of these compounds López and Pascual-Villalobos (2010) observed that the monoterpenoids fenchone, S-carvone and linalool inhibited the enzyme acetylcholinesterase.

Lepidoptera

The tomato leafminer, Tuta absoluta (Meyrick), the Egyptian cotton leafworm, Spodoptera littoralis (Boisduval), the cabbage butterfly, Pieris brassicae (L.), and the small white butterfly, Pieris rapae (L.), are among the most important pests causing severe damage to several types of vegetable crops. Tuta absoluta is a serious threat for Solanaceae crops in the Mediterranean basin, attacking both outdoor and greenhouse crops, and can cause yield losses that may exceed 60% (Braham et al. 2012; Abd El-Ghany et al. 2016). Like other pests, its control is based on application of synthetic insecticides. Regarding its control with botanical-based insecticides, the data that are available are rather limited. Ait Taadaouit et al. (2012) observed that the extracts from T. vulgaris, castor bean, Ricinus communis L., P. harmala and U. dioica caused mortality on second instar larvae of T. absoluta. In fact, among the above plant species, T. vulgaris was the most effective (Ait Taadaouit et al. 2012). The insecticidal activity of these species is also reported in other studies. For example, Jovanović et al. (2007) found that extracts from U. dioica could be used with success against the bean weevil, Acanthoscelides obtectus (Say).

Hasheminia et al. (2013) reported that the extracts of milk thistle, Silybum marianum (L.) Gaertn. seeds, were toxic, deterrent and antifeedant on P. rapae. Similarly, Chandel et al. (2012) found that R. communis extracts were lethal on nymphs and adults of P. brassicae. Regarding the mode of action of R. communis extracts, Tatun et al. (2014) reported that these extracts contain compounds that block the α-amylase activity. This insecticidal activity was demonstrated from experiments performed on the red flour beetle, Tribolium castaneum (Herbst) (Tatun et al. 2014). The insecticidal activity of R. communis has been attributed to the compounds Ric c 1 and Ric c 3. Do Nascimento et al. (2011) reported that the 2S albumins Ric c 1 and Ric c 3 inhibited the α-amylase activity on larvae of C maculatus, the Mexican bean weevil, Zabrotes subfasciatus (Boheman), and the yellow mealworm, Tenebrio molitor L. According to Sayed et al. (2007) the natural compounds khellin and visnagin (Fig. 2) which were isolated from aerial parts of purple nutsedge, Cyperus rotundus L., caused strong inhibition of larval growth of S. littoralis. The insecticidal activity of C. rotundus is also reported by other research groups. For example, Liu et al. (2016) observed that the sesquiterpenes α-Cyperone and cyperene which isolated from rhizomes of C. rotundus caused contact toxicity against the psocid Liposcelis bostrychophila Badonnel. Cyperus rotundus is a perennial weed widely distributed in agricultural regions around the world and very common in the Mediterranean basin (Hershenhorn et al. 2015; Du et al. 2019). The foliage of the plant U. maritima contains the non-protein-based amino acid l-azetidine-2-carboxylic acid (1.7% of fresh weight), which was lethal for S. littoralis larvae (Hassid et al. 1976). According to Huang et al. (2011) non-protein amino acids have been associated with plant defense against insect pests, while Adeyeyé and Blum (1989) reported that the compound l-azetidine-2-carboxylic acid caused retardation of larval development and lethal effects resulting from exuvial ligature on the H. zea larvae.

Fig. 2
figure 2

Chemical structure of some active constituents of native plants of the Mediterranean basin with insecticidal activity: a khellin (C14H12O5), b visnagin (C13H10O4), c linalool (C10H18O), d a-Cyperone (C15H22O), e l-azetidine-2-carboxylic acid (C4H7NO2), f S-carvone (C10H10O) and g pulegone (C10H16O)

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Efficacy of natural insecticides under field conditions

Usually, the extracts or the essential oils of plants are evaluated regarding their insecticidal activity under laboratory conditions. In this regard, the evaluation of these insecticides at the field scale is essential, since the environmental conditions (e.g., temperature, light and rainfall) can greatly affect their efficacy. Regarding the insecticidal activity of the abovementioned natural insecticides under field conditions there are disproportionally few data, as compared with the laboratory bioassay-based reports. For example, Civelek and Weintraub (2004) examined the efficacy of the extracts from U. maritima and E. myrsinites against L. trifolii in greenhouses, when applied at the foliage of tomato plants. The results indicated that the extracts from these plants, which applied at different concentrations, significantly reduced the number of larvae and adults of L. trifolii on tomato leaves, while the efficacy of the extracts from both species was comparable with that of cyromazine treatment. Similarly, Jiang et al. (2018) evaluated the efficacy of 10% seed extract of R. pseudoacacia against B. brassicae in an oilseed rape crop (Brassica napus L.). The 10% EW (emulsion in water) formulation of this extract was applied at three different doses (300, 600 and 900 g/ha). The results of this field experiment revealed that this formulated bioinsecticide at the dose of 900 g/ha exhibited high efficacy (> 95%) against B. brassicae, which was comparable with that of the neonicotinoid insecticide imidacloprid.

Tembo et al. (2018) reported that the extracts (10% w/v) from leaves of Tithonia diversifolia (Hemsl.) A. Gray, Lippia javanica (Burm.f.) Spreng, and Tephrosia vogelii Hook.f. reduced the number of various insect pests in bean and cowpea crops, while the extracts provided similar results with that of the pyrethroid lambda-cyhalothrin. Similarly, Smith et al. (2018) observed that three different biopesticides based on orange oil (60 g/L of the active ingredient), neem oil (1% azadirachtin-A) and the essential oil from Chenopodium ambrosioides (16.75% of the essential oil) provided high efficacy against M. persicae on pansy (Viola x wittrockiana) which was comparable with that of the synthetic pesticides spirotetramat and flonicamid.

Probably the most well-demonstrated botanical insecticides under field conditions are those that are based on the neem tree (Azadirachta indica, A.Juss., Meliaceae). Recently, Shah et al. (2019) conducted field trials in order to evaluate the efficacy of the neem seed extract in comparison with synthetic insecticides. Their results show that the neem seed extract was less effective against cauliflower pests in comparison with a commercial product based on neem tree [NeemAzal; active ingredient: azadirachtin-A (10 g/L)] or to chlorantraniliprole plus thiamethoxam.

The above paradigms clearly reveal that certain insecticides from native species of the Mediterranean region can be effective under field conditions, at least at the same level with commercially available synthetic insecticides. This underlines the importance to boost further for the development of commercial natural resource products that can, in certain scenarios, replace conventional pesticides. It is an encouraging statistic that the number of registered natural insecticides has been increased in recent years (Grieneisen and Isman 2018), while the prospects for the future appear to be positive. As mentioned above, the Mediterranean thrive in native plant species with considerable insecticidal activity and, thus, the extracts and/or the essential oils from some of the above species can be used in order to develop new commercial products. Finally, it is very important to develop broad-spectrum natural insecticides that contain extracts or essential oils from more than one plant species in order to (a) provide increased efficacy and broader target spectrum and (b) reduce the number of applications in the field. These goals can be achieved, since previous studies have shown that the constituents of essential oils can exhibit synergistic action (Pavela 2016; Isman 2020). Moreover, the experiments of Feng and Isman (1995) indicated that M. persicae can develop resistance to azadirachtin. In this regard, it is necessary to reduce the selection pressure of resistance to natural insecticides by (a) developing new products or (b) combining two or more insecticides, although often these products are not compatible (Siegwart et al. 2015). In this regard, the compatibility between two natural insecticides or between natural and synthetic insecticides should be also evaluated. Moreover, in order to improve the efficacy of natural insecticides in the field, it is important to conduct more field experiments in which the application time and strategy of these products should be examined in “real-world” application scenarios (Isman 2017).

It is also important to note that natural insecticides can be integrated with other control techniques such as the release of predators or parasitoids. The fact that natural insecticides had no considerable effect on natural enemies has been reported by several research groups (Gaspari et al. 2007; Gupta et al. 2017). For example, Gaspari et al. (2007) reported that U. urens extracts had no effects on the polyphagous predator of M. persicae, Macrolophus pygmaeus (Rambur), indicating that these extracts could be used successfully in conjunction with “macro-biological” control. In a recent study, Gupta et al. (2017) also observed that that lemon extracts had no effects on the polyphagous predator the seven-spot ladybird, Coccinella septempunctata L. Moreover, the neem oil, a natural insecticide that is available in several countries, presented a low toxicity to larvae of the predator Eriopis connexa (Germar) (Tavares et al. 2010).

The increase of natural enemies of pests in vegetable crops in combination with the application of natural insecticides should be a part of integrated pest management system in these crops. The planting of flowering plants (i.e., marigolds, Tagetes spp., and cosmos, Cosmos spp., sesame, Sesamum indicum L., okra, Abelmoschus esculentus (L.) Moench, and sunflower, Helianthus annuus L.) on the bunds (also known as vegetation or flower strips) in several crops is a useful field technique in order to increase the natural enemy populations (predators, parasitoids) and, thus, enhance the biological control of pests (Balzan and Moonen 2014; Ali et al. 2019; Cahenzli et al. 2019; Gontijo 2019; Horgan et al. 2019). Finally, intercropping vegetables with other plants can also contribute toward the increased occurrence of natural enemies. In a recent study, Zheng et al. (2020) reported that the infestation of potato crop by the potato tuber moth (PTM), Phthorimaea operculella (Zeller) was significantly reduced in the intercropping potato-maize system, through a simultaneous increase in the number of parasitoids.

Insect control in vegetable crop production with natural insecticides: sustainability in practice

Many of the compounds mentioned earlier in this review are usually non-persistent under field conditions and can be easily transformed by light and oxygen into less effective compounds (Ujváry 2010). However, reduced persistence is not necessarily always a shortcoming, as some botanicals may leave residues at the postharvest stages of agricultural commodities, which have not been thoroughly investigated for their effects on mammals. The same holds for environmental concerns on certain compounds. Still, while theoretically, persistence is a “red flag” in the case of conventional insecticides, the use of plant extracts and derivatives that can retain their insecticidal effects for long periods and have low (or no) mammalian toxicity, is desirable and compatible with IPM-based strategies. While the efficacy studies are numerous, the effects of most of these compounds on both mammals and the environment are poorly understood. The development of commercially available botanical formulations should essentially pass through this channel of evaluation, for which, unfortunately, there are not that many data available. Hence, while it appears that we have an enormous amount of data for the insecticidal value of some of these compounds, we practically know little about their exact effects on mammals and the environment. For example, the compound ricinine from R. communis exhibited toxic effects on the workers of European honey bee, Apis melifera L. (Rother et al. 2009). Similarly, Xavier et al. (2015) observed that the garlic extracts and neem oil exhibited toxic effects on A. melifera larvae. In another recent study, Benelli et al. (2020) reported that the essential oil from marsh rosemary, Ledum palustre L. exhibited insecticidal activity against S. littoralis and other insects, while had no toxic effects against the redworm, Eisenia fetida (Savigny), which is an good indicator of reduced toxicity on non-target organisms. In contrast, it was observed that this essential oil had toxic effects on aquatic microcrustaceans, Daphnia magna Straus, while had exhibited cytotoxic effects on two human cell lines (HaCaT and NHF A12).

There are numerous data indicating that, in vegetable crops but also in other crop categories, certain botanicals may not be as effective as conventional synthetic insecticides (Walia et al. 2017). Still, as noted above, there are many examples where specific botanicals were more effective than conventional insecticides, especially in the case of resistant insect populations. The most important parameter for improving the effectiveness of natural insecticides is the development of suitable formulations (Fig. 3). The natural insecticides are formulated in several types of formulations such as emulsifiable concentrate (EC), emulsion in water (EW) and oil dispersion (OD) (Smith et al. 2018; Jiang et al. 2018). The stability of natural products can be increased via the process of microencapsulation (Fernandes et al. 2013), since formulation of biopesticides is a key challenge for their wider adoption (Pavela and Benelli 2016). The microencapsulation is an evolving technology to stabilize and control the release of the encapsulated biological compounds (Vinceković et al. 2017). This is extremely important since the residual activity of natural insecticides is generally shorter than that of synthetic insecticides. In this regard, Igrc Barčić et al. (2006) reported that the residual activity of neem extract lasted up to 7 days, while the residual activity of spinosad lasted a for 10 to 20 days. In addition, there are some recent examples where the insecticidal effect and the persistence of some compounds was greatly benefited by encapsulation (Domingues and Santos 2019; Kavetsou et al. 2019). Kavetsou et al. (2019) observed that the encapsulation of essential oil of M. pulegium extended the duration of insecticidal activity of this insecticide for 3 days. Moreover, this technology has been successfully applied for the formulation of neem-based products such as oil or extract (Gahukar and Das 2020; Pascoli et al. 2020). At this point, it is important to mention that the microencapsulation technology has not been widely applied to several commercial insecticides (synthetic or botanical-based), probably due to issues that are associated with cost and technology complexity. Phytochemical pesticides contain several active ingredients, which makes the product standardization a very complicated procedure (Walia et al. 2017). For this purpose, the selection of genotypes with high content in compounds with insecticidal properties is extremely important, while the cultivation of the native plants under optimum conditions could contribute toward this direction. This is supported by the fact that in many native species there is a noticeable seasonal variation in the content of their bioactive compounds. For example, Bennaoum et al. (2017) observed that the composition of essential oils (e.g., concentration of 2-undecanone and 2-nonanone) from Ruta species (e.g., Ruta chalepensis subsp. latifolia and Ruta chalepensis subsp. angustifolia) varied between the two species, among the seasons (winter, spring, summer and autumn), as well as among the various genotypes of different geographical origin. In addition, the combined application of natural insecticides can also help to increase their effectiveness, through the combined mode of action, their multiple effects on different life stages of the target species and their different interactions with abiotic conditions, such as sunlight, temperature and moisture.

Fig. 3
figure 3

The critical points for increasing the use of natural insecticides in vegetable production

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The dose–concentration that these compounds are used, consists one of the key elements in their wider use. It is generally considered that botanicals and plant derivatives are effective at extremely high dose rates, which often exceed 100 or even 1000 ppm, while conventional insecticides are effective at considerably lower rates, which are usually less than 10 ppm. For example, the lethal concentrations (LC95) of essential oils from P. lentiscus and M. pulegium against to A. gossypii were 1343 and 939 ppm, respectively (Behi et al. 2019). This is particularly critical for direct comparisons between botanicals and synthetic pesticides, as apart from the efficacy per se, feasibility and eventually adoption is heavily based upon the dose rates that are effective for insect control. In this regard, the development of formulations that are effective at low dose rates is essential for their feasibility in practice. Moreover, some of these compounds are macromolecules that are very expensive in their synthesis or even extraction and isolation, which is expected to negatively affect the cost-effectiveness of “real-world” applications in vegetable crops. As the cost of botanical-based insecticides is far less industrialized than that of the conventional ones, their cost-effectiveness is expected to be increased under the basis of a “scale-up” production, which lays far beyond initial research and development. These attributes, along with the implementation of potential combinations of botanicals with additional reduced-risk control methods, will eventually set the scene for increased farmers’ acceptance and implementation in realistic area-wide scenarios.

In summary, several commonly found native plants in the Mediterranean basin exhibit a valuable insecticidal activity against several insects of vegetable crops, while there is an increase in global demand for biopesticides, along with the consumers’ demand for reduced use of conventional insecticides. Moreover, the extracts from the evaluated species exhibited multiple mechanisms of action, which can be considered as a positive attribute toward their wide use. In this effort, the development of suitable formulations of biopesticides, such as capsule suspensions, will be crucial in terms of increasing the effectiveness of natural-based insecticides in conjunction with their increase residual effect. Standardization of the chemical composition of these insecticides should be seriously taken into account, as different species, or even different populations of these species, often vary remarkably in the composition and the containment of a given compound. Accordingly, the application of biopesticides such as plant extracts can used for insect control, but many steps need to be made to be acceptable by farmers.

Author contributions

ACK and CGA contributed equally to reviewing the literature and writing the manuscript.