Environmentally Friendly and Effective Alternative Approaches to Pest Management: Recent Advances and Challenges

Abstract

The most important requirement in sustainable agriculture is to significantly reduce the application of chemical pesticides, and environmentally friendly and effective approaches to pest management should be established to control the population size of dominant pests. To promote the development of promising plant protection measures, substantial efforts have been made regarding the identification of secondary botanical chemicals, pheromones, and RNA pesticides, as well as the optimization of the feeding conditions of biocontrol agents and the treatment methods of defensive phytohormones. Advances in these areas have revealed effective strategies for pest management, some of which have been widely implemented in agricultural practices. Although the effectiveness of some of these attempts is evidenced by their success in combating herbivore insects, significant challenges remain. Thus, this review summarizes the potential applications and challenges associated with the environmentally friendly and effective alternative strategies currently implemented in pest management. It is revealed that a combination of these approaches will significantly impede the evolution of pests, leading to maximum efficiency in pest management.

1. Introduction

The exploding growth of the global population has placed a heavy burden on agriculture, with estimations indicating that it will reach approximately 10 billion by the mid-21st century [1]. Additionally, rapid urbanization and industrialization across the globe have led to a significant decrease in the total area of arable land and have posed challenges to agricultural production. FAOstat reports indicate that up to 40% of crops are lost to pests every year [2], which can cause direct damage to plants, and in some cases, the severity of the damage is exacerbated by related pests and microbes. For instance, there is always a “synergistic” damage effect on plant seedlings when the wheat aphid, one of the dominant pest species often threatening wheat production globally, coexists with wheat spikes’ fungi or their transmitted plant virus, the barely yellow dwarf virus [3,4,5]. In addition, it has been demonstrated that climate change, especially extreme weather conditions, has led to a significant outbreak of herbivore insects, further contributing to severe damage to the yield and quality of agricultural products [2]. Furthermore, growing concerns about food safety and continuous improvements in living conditions have significantly increased the demand and production of organic and green products. Therefore, to meet the demand of the world’s population regarding agricultural production, appropriate and effective plant protection measures should be developed.

According to FAOstat reports, in China, pesticide consumption decreased from 328,540 tons (T) in 2016 to 224,717 T in 2022, while insecticide consumption decreased from 88,550 T to 60,567 T [6]. Although the use of chemicals for plant protection has gradually decreased in China in recent years, it is still one of the leading countries in terms of pesticide consumption [6]. In 2019, approximately 40% of pesticides in China were used for pest control in cereal crop production [7]. Meanwhile, the Chinese National Agro-Tech Extension and Service Center has also issued guidance and emphasized that chemical spraying is still the dominant method of plant protection in agriculture, likely due to its effectiveness in suppressing pest populations and rapidly controlling the damage caused by pathogens and pests at the lowest cost. However, to achieve maximum control efficiency, farmers often spray several limited chemical pesticides with no management plan in place [8,9], which may cause pests to rapidly develop insecticidal resistance. Consequently, farmers will have to increase the concentrations of chemicals to control further damage due to insecticidal resistance. This has become a serious and continuous problem in most farming regions of the world. Additionally, the extensive use of chemicals may pose various long-term risks to agroecosystems, including the eradication of the natural enemies of dominant pests, the disruption of biodiversity, etc. These drawbacks and challenges in chemical control have significantly promoted the development of alternative plant control measures in agricultural production, thus accelerating sustainable agricultural development and ensuring global food safety. For instance, continuous technological advances for the identification of secondary botanical chemicals, pheromones, RNA pesticides, and phytohormone signaling cascades, as well as the optimization of the feeding conditions of biocontrol agents, have contributed to their widespread use for crop and fruit protection. Furthermore, in 2022, the Ministry of Agriculture and Rural Affairs of the People’s Republic of China implemented a new round of action plans for reducing the use of chemical fertilizers and pesticides [10]. Thus, this review will discuss the recent advances and ongoing research in alternative pest control strategies with the main aim of highlighting environmentally friendly and effective measures for managing the population dynamics of diverse pests without the use of prevalent pesticide control methods.

2. The Potential Application of Secondary Metabolites for Green Plant Protection

Secondary metabolites derived from bacteria, fungi, or plants, including naturally occurring microbiological, biochemical, and macrobiological compounds, can be used for the control of pests, weeds, and phytopathogens [11]. As a well-known example, the bacteriotoxins secreted by Bacillus thuringiensis (Bt) have been widely applied to protect cotton, maize, rice, and wheat from the larval herbivory of major Coleopteran or Lepidopteran pests [12]. Meanwhile, the encoding genes of Bt-derived toxins have been integrated into diverse plants to strengthen their resistance by eradicating susceptible pests or hindering their development [13]. However, similar to some chemical pesticides, Bt-derived toxins subject pests to strong selective pressure, thus rapidly triggering their resurgence. In comparison, botanical secondary metabolites induce moderate selective pressure on herbivore insects, and their application is not often associated with health, environmental, or ecological problems; thus, they have received increasing attention regarding the screening and characterization of botanical chemicals [14]. In recent decades, a broad range of botanical chemicals, including plant extracts and essential oils, i.e., alkaloids, phenols, quinones, terpenoids, flavonoids, tannins, and other plant derivatives, have been isolated from various plants, and they constitute the primary source of biopesticides for protecting crops against pests [11]. Botanical chemicals are commonly classified into four main genres: nitrogen-containing compounds, phenolic compounds, terpenoids, and polyacetates.

Plant-derived alkaloids are the largest class of nitrogen-containing compounds of plant origin and are widely used for pest control. Most species exhibit potent contact-killing or stomach toxicity effects and act as repellents or antifeedants against insects. They also may disrupt the activity of the crucial enzymes involved in insects’ respiratory, nervous, and digestive systems and significantly suppress diverse insect populations. To date, more than 30 plant-derived alkaloids have been established, along with their source plants and modes of action, and some have been registered as botanical insecticides and introduced into agricultural production [15]. For instance, veratrine (isolated from Veratrum nigrum or V. album), berberine (isolated from Coptis chinensis), and matrine (isolated from Sophora flavescens or S. alopecuroides) have been broadly applied for pest control in China [16]. Nicotine is a promising and well-known alkaloid pesticide obtained from tobacco leaves, which exhibits toxic effects on many herbivore insects while being highly effective and environmentally friendly [17]. Glucosinolate (also known as mustard oil glucosides) is another nitrogen-containing compound, which is isolated from agriculturally significant vegetables, especially in the genus Brassica, such as Brassica nigra L., B. rapa L., B. napus, etc., and its content is always low in foliage and high in root and seed [18,19]. Although glucosinolates are generally present in plant cells as non-toxic compounds, once plant seedlings are damaged by pests, glucosinolates break down as β-D-glucose and unstable aglucone (thiohydroximate-O-sulfonate) through hydrolysis by myrosinases. Subsequently, aglucone may transform into toxic molecules and thus exert adverse effects on soil-borne plant pests as well as the larvae of numerous Lepidoptera pests [20,21].

Plant phenolic compounds, including simple phenols, quinones, lignins, flavonoids, tannins, etc., are not only involved in the regulation of plant development and pigmentation, but also play a major role in protecting plants against biotic and abiotic stresses. Simple phenols can directly trigger the defense responses that enable plants to combat microorganisms, while their oxidation by polyphenoloxidase (PPO) leads to the formation of quinones in plants after microorganism infection [22,23]. Quinones participate in the synthesis and metabolism of plant cell wall components and stimulate the strengthening properties and lignification of cell walls while exhibiting direct toxicity to insects and inhibiting protein digestion in herbivores [24,25,26,27]. In addition, lignin, a phenolic heteropolymer, is one of the crucial components for cell wall strengthening and lignification [28], and its biosynthesis has been induced after a herbivory or pathogen attack. For instance, pest and pathogen attacks lead to the significant upregulation of the transcripts of lignin biosynthesis-associated genes (CAD/CAD-like genes) in plants [29]. Subsequently, its rapid deposition in wound plant tissue prevents entry by physically blocking pathogens’ access or increasing leaf resistance, which reduces feeding by herbivores and decreases the nutritional content of the leaf tissue, thus suppressing further pathogen growth in plant tissue or having a detrimental effect on pest fecundity [28].

Flavonoids are the most abundant phenolic botanical chemicals found in almost all plant species, and they are commonly reported as antifeedants against insects [30,31,32]. For instance, observations of electrical penetration graphs revealed that the addition of flavonoid compounds, including luteolin and genistein, to the artificial diets of pea aphids (Acyrthosiphon pisum Harris) had a detrimental effect on the feeding behavior of pea aphids [33]. In addition, it has been demonstrated that their antifeeding effects can delay development and growth, induce malformations, and affect the reproductive parameters of insects [32]. By contrast, the flavonoids in soy leaves exhibit positive effects on their feeding behavior [34]. Moreover, at low concentrations, some flavonoids, i.e., pinocembrin and quercetin, could act as phagostimulants for the Cucurbitaceae pest Epilachna paenulata and fall armyworm Spodoptera frugiperda J.E. (Smith) [35,36]. These results suggest that the antifeeding activity of flavonoids is likely concentration dependent. Meanwhile, the direct administration of flavonoid compounds for pest control can decrease the activities of detoxifying enzymes, including superoxide dismutase, catalase, ascorbate peroxidase, and glutathione S-transferase, which may trigger oxidative stress and subsequently disrupt the detoxification system of insects [37]. Moreover, flavonoids can disrupt the nervous system of insects by affecting crucial neuronal enzymes such as AChE or neuronal channels [32,38]. Benzoxazinoids are shikimic acid-derived phenolic compounds that are biosynthesized in high abundance by Poaceae crops such as wheat and maize, and they are also found in various dicot families [39,40]. Initially, benzoxazinoids have been described as antifeedants or toxic compounds that suppress the feeding behavior of pests [41]. For instance, most studies have reported positive effects, while some have revealed that none of these benzoxazinoids in wheat cultivars contribute to their resistance to aphids, even leading to the enhanced activity of some aphids with higher levels of benzoxazinoids [42,43]. Therefore, the relationship between the levels of constitutive benzoxazinoids in host plants and their resistance to cereal aphids remains controversial. Furthermore, genetic evidence has revealed that benzoxazinoids also act synergistically with plant signaling compounds by initiating callose deposition in maize plants damaged by pathogens or aphids [44,45]. For instance, the preinfestation levels of aphids significantly alternated the dynamic level of benzoxazinoids, especially in aphid-resistant wheat cultivars, inducing a noticeable increase in the number of aphid-induced callose deposition spots [42].

Tannins are astringent bitter polyphenols and commonly act as feeding deterrents to many insect pests. In comparison with other phenolic compounds, tannins have a strong deleterious effect on pests and hinder their growth by binding to proteins, reducing the nutrient absorption efficiency, and even causing midgut lesions.

Terpenoids form the largest group of secondary metabolites of plant origin, and more than 80,000 species have been found in various plants [46]. The main genres of terpenoid botanical chemicals include hemiterpenes (C₅H₈), monoterpenes (C₁₀H₁₆), sesquiterpenes (C₁₅H₂₄), diterpenes (C₂₀H₃₂), triterpenes (C₃₀H₄₈), tetraterpenes (C₄₀H₆₄), and polyterpene (C₅H₈)_n skeletons, with the terpenoid carbon skeleton undergoing further modification resulting in different terpenoid compounds through redox reaction, methylation, acylation, glycosylation, etc. Some terpenoids play an important role in plant photosynthesis by regulating plant development; pollination can release aromatic components into the environment, and tetraterpene compounds such as carotene and lutein can absorb and transmit light energy. Many other species exhibit resistance to the toxic effects induced by external biotic or abiotic stresses [47]. For the prevention of pest attacks, many terpenoids have toxic effects and act as feeding deterrents or growth inhibitors. For instance, polygodial (sesquiterpenoid), azadirachtin, and toosendanin (triterpenoid) exhibit strong antifeedant effects against various insects and have been used in biopesticide development [16]. Due to its intensely bitter taste, cucurbitacin B (triterpenoid) has also been used as an antifeedant against some insect species, i.e., Leptinotarsa decemlineata, Tenebrio molitor, Cerotoma trifurcate, etc., and as a deterrent or repellent affecting the oviposition of insects, including Ostrinia nubilalis, Spodoptera exigua, etc. Additionally, as phagostimulants, they enhance the feeding behaviors of some species such as Acyrthosiphon pisum, Corythucha ciliata, and Diabrotica insects [48]. Moreover, some terpenoids can induce defense responses in adjacent healthy plants, thus strengthening their resistance to pests [49,50].

Furthermore, polyacetylenes are commonly isolated from Asteraceae plants and have the potential to be used as effective insecticides for pest control. For instance, four polyacetylene species were isolated from the traditional edible herb Bidens pilosa (L.), which exhibited resistance to Plutella xylostella (L.), Spodoptera litura, Mythimna separata (Walker), Spodoptera exigua (Hübner), and Helicoverpa armigera and Ostrinia furnacalis (Guene’e), likely due to its toxicity [51].

Apart from that, some other plant insecticidal compounds and proteins, such as plant lectins, α-amylase inhibitors, avidin, Photorhabdus luminescens toxins, and cholesterol oxidase, are promising for the development of biopesticides [52,53]. For instance, as a group of carbohydrate-binding (glyco) proteins derived from Galanthus nivalis or Pinellia ternate agglutinin, lectins have a protective function against various pests, including Homopteran, Lepidopteran, and Coleopteran species, due to their insecticidal activity that affects the absorbance of carbohydrate compounds in these insects [12,54].

Taken together, an increasing number of studies have focused on the isolation of more alternative botanical chemicals and the comprehensive characterization of their biosynthesis pathways to facilitate the development of botanical biopesticides (Figure 1). However, the extent of their inherent biosynthesis in most plants hardly meets the levels required for biopesticide production; thus, the development of microbial production systems would facilitate the large-scale production of botanical chemicals and biopesticides. In addition, the application of some other biopesticides is hardly effective as a control measure against various pests with simultaneous outbreaks. Meanwhile, similar to chemical pesticides and Bt-derived toxins, the toxic effects of some secondary botanical metabolites may pose health and ecological challenges caused by accumulation in food chains.

3. Phytohormone Treatment as a Pest Control Strategy

Over time, plants have coevolved their constitutive and induced defense mechanisms to combat or repel their colonizers either directly or indirectly [22,55,56]. As described previously, secondary botanical metabolites play a crucial role in constitutive defense mechanisms; however, most plant species have moderate levels of these compounds. Empirical studies have revealed that the preinfestation levels of herbivores may significantly upregulate the gene transcripts associated with the biosynthesis of phytohormones and some secondary botanical metabolites, thus suppressing the population densities of diverse pests. Based on most of the existing studies, jasmonic acid (JA) and its derivatives are extensively accumulated in plants damaged by chewing insects [57], while salicylic acid (SA) and its derivatives are extensively accumulated after the damage caused by the feeding of piercing–sucking insects [58]. Although JA and SA, as endogenous growth regulators, hardly exhibit any detrimental effects on plants themselves, their excessive accumulation in plant tissues leads to the subsequent activation of the corresponding signaling pathways and triggers plant defenses to alleviate further damage. Plant defense mechanisms mediated via phytohormone signaling often exhibit distinct responses based on the mouthpart types of their attackers; thus, in the next section, we specifically discuss the physiological alternations induced by direct JA or SA treatment.

One of the most important results of direct JA treatment is that it can alter the content of some secondary botanical metabolites, including flavonoids, terpenoids, phenolic compounds, alkaloids, quinone, lignin, etc. [59,60,61]. For instance, the nicotine content in the leaf tissues of Nicotiana tabacum seedlings directly treated with methyl jasmonate (MeJA) was upregulated two-fold compared to control plants, which significantly increased the mortality of Manduca sexta larva [61]. Meanwhile, tobacco seeds soaked with 3 mM JA solutions exhibited the accumulation of defensive metabolites in tobacco plants, including caffeoylputrescine, dicaffeoylspermidine, nicotianoside VII, and diterpene glycosides, with increases of 60%, 79%, 19%, and 29%, respectively, compared to controls [62]. A significant increase in the content of these secondary botanical metabolites subsequently triggered physiological alternations and plant defense mechanisms, leading to the suppression of the feeding behavior of Spodoptera litura larva [62]. Meanwhile, JA treatment could positively affect the morphological traits of plants associated with constitutive defenses. For instance, directly spraying 7.5 mM of MeJA on tomato plantlets at the two-leaf growth stage resulted in a 60% increase in the type-IV glandular trichome density on the leaf surface, highlighting its significance for acylsucrose production [60]. Plants subjected to MeJA treatment exhibited resistance to whiteflies, leading to a decrease of 50% in the incidence of its transmitted virus relative to the controls [60].

In addition, JAs can induce the expression of the enzymes involved in antibiosis, i.e., proteinase inhibitors (PIs), PPO, lipoxygenase (LOX), peroxidase (POD), phenylalanine ammonia lyase (PAL), etc., or enhance their activities in plant tissues [63]. For instance, MeJA treatment induced the upregulation of PI activity in various plant tissues while significantly reducing the activities of strong alkaline trypsins and chymotrypsins in Lepidopteran insects, leading to detrimental effects on their feeding behavior and digestive system [64]. As described previously, the activities of trypsin proteinase inhibitors in tobacco plants grown from seeds treated with 3 mM of JA increased to 80% compared to the control plants [62]. Moreover, JA treatments could suppress the colonization rate of insects through the development of a blend of volatile compounds and an alteration in the content and composition of induced plant volatiles, which either act as feeding and/or oviposition deterrents or attract the natural enemies of herbivores [65,66]. These findings suggest that the exogenous application of JAs on seedlings or seeds could suppress the pest population density by directly enhancing the plant’s constitutive and induced resistance to herbivores and indirectly attracting native biocontrol agents. Various JA treatment methods have been used in agricultural practices, including spraying, soaking, daubing, exposure, soil injection, etc. [67]. However, the commercial production of JAs poses the greatest obstacle in the application of JA treatments for agricultural production, likely due to their complex biosynthesis pathways and purification process, resulting in low productivity. Moreover, treatment with relatively large concentrations of JAs usually leads to stronger resistance to pests in different cultivars. However, increasing the concentrations of JA treatments significantly increases the cost of agricultural production and may also have a negative effect on plant growth. Thus, seed soaking with a JA solution is a recommended strategy for pest control in crop production.

Similarly, the exogenous application of low concentrations of SA not only facilitates the production of secondary botanical metabolites such as phenolic compounds and anthocyanins but also increases the activities of protective enzymes, including superoxide dismutase (SOD), POD, catalase (CAT), ascorbate peroxidase (APX), glutathioneperoxidase (GPx), etc. [68,69]. For instance, corn plants treated with stabile SA that underwent crosslinking with chitosan nanocarriers exhibited a significant enhancement in the content of benzoxazinoids in their leaves compared to the controls, namely from 36.7% to 179.8%, as well as the upregulation of SOD, POD, and CAT enzymatic activity, which induced stronger resistance to fall armyworm Spodoptera frugiperda and significantly alleviated the oxidative stress triggered by its feeding behavior in maize plants [70]. These findings suggest thar SA–chitosan nanoparticles may be considered eco-friendly biostimulants with the ability to increase pest resistance in crops, and thus may be successfully used in organic farming in the near future [69]. The extensive accumulation of SA after pest damage or treatment with higher concentrations of SA can decrease the activities of antioxidant enzymes [71] and result in the accumulation of reactive oxygen species (ROS), especially H₂O₂ in tissues, subsequently activating the systemically acquired resistance [72,73,74]. Thus, there is often a tradeoff between normal plant growth and the detrimental effects of excessive application on the production of secondary botanical metabolites in various plants. In terms of cost, the application of commercial SA has significantly lower costs compared to JA biosynthesis. As various plants exhibit distinct susceptibility thresholds in SA treatment, the determination of the threshold concentrations of SA treatment in main crops is crucial for the broader application of SA-mediated pest control practices.

Based on these attempts, although both JA and SA treatments could induce secondary botanical metabolites and antibiosis enzymatically mediated defense responses in plant tissues to combat pests, their exogenous application hardly exerts additive effects on pest control. Our previous studies comprehensively summarized their antagonistic effects triggered by aphids or pathogenic fungi [75,76]. In another study, we provided experimental evidence supporting the conclusion that the direct foliage spraying of MeJA has a multifunctional role in altering the physiological traits of plants that suppress the SA-mediated plant defenses in wheat cultivar XN979 [77]. In addition, some other challenges should be overcome before the application of phytohormone treatments for plant protection, i.e., their high cost, susceptibility to degradation, uncontrollable permeability, unstable control efficiency, short duration of effect, uncontrolled application leading to detrimental effects on plant growth, etc. Therefore, to address these problems, future efforts are expected to continue to focus on advances in the organic chemical synthesis of phytohormones, especially JAs, and nanomolecular packaging technology.

4. The Introduction of Biocontrol Agents into Pest Management

The growing interest in sustainable agriculture has led to the introduction of biocontrol agents into herbivore insect control, which is commonly referred to as the application of natural enemies, including parasitoids, predators, or herbivorous arthropods, to suppress the pest population density; most of them are harmless to human and vertebrates. Depending on the intensity of human intervention, biocontrol strategies include augmentative, classical, and conservation biological control methods. Among them, classical and augmentative biological control methods involve the release of the natural enemies of target pests, with the classical approach focused on the prevention of invasive pests by establishing high-density populations and introducing local natural enemies that are not already present at new locations. By contrast, the augmentative approach involves pest suppression in greenhouses or outdoor crops through the release of commercially reared natural enemies. As this approach significantly contributes to reducing the detrimental effects of pests in agricultural production, in this section, we discuss augmentative biological controls in more detail.

Augmentative biological controls often require the massive release of predatory or parasitic natural enemies and could temporarily suppress the population density of target pests. Their cost in comparison to other approaches usually depends on the cost of natural enemy production by commercial insectaries. In addition, most control projects require annual release to sustain the control efficiency. The most common predatory natural enemies used in biological controls are lady beetles (Coleoptera: Coccinellidae), which are considered beneficial and cost-effective species because, in their larval or adult stages, they can feed on most Homoptera or Acarina pests, i.e., whiteflies, cottony cushion scale, mealybugs, armored scale insects, scale insects, aphids, and even mites [78,79]. Nearly 6000 lady beetle species have already been identified worldwide. Apart from the species in the subfamily Epilachninae (always feed on plants) and the tribe Halyziini (feed on mildews), almost 80% of the species in the Coccinellidae family could be potential biocontrol agents in agricultural production, either outdoors or in greenhouses [80]. Four species, namely the harlequin lady beetle (Harmonia axyridis Pallas), Japanese lady beetle (Propylaea japonica Thunberg), variegated lady beetle (Hippodamia variegate Goeze), and seven spotted ladybird beetle (Coccinella septempunctata L.), are the most specialized predatory natural enemies that have been widely applied in augmentative biocontrol projects in China [81,82,83,84]. For instance, the aphidophagous lady beetle H. variegate has been used to suppress the population density of aphid species, including the cotton and pea aphids in cereal, fruit, or vegetable crops, and their related cropping systems [85]. Meanwhile, many patents focused on optimizing the feeding conditions of lady beetles to rapidly aggregate their populations have been issued in recent decades, significantly facilitating the commercial production of lady beetles with a low cost in insectaries [83]. These findings suggest that the release of predatory lady beetles could contribute to the regulation of populations of their prey; however, accumulating experimental evidence has revealed that a high aphid reproductive rate is barely achieved with strategies involving the release of aphidophagous lady beetles, which is likely due to the disparities in life history between lady beetles and aphids, with the predator lagging behind the prey in terms of population growth, thus inducing its response. Meanwhile, some aphidophagous lady beetles exhibit a functional type II response, indicating that their predation ability increases with prey density but gradually decelerates until a plateau with the increasing densities of diverse aphid populations [85]. Therefore, the release of predatory lady beetles as an augmentative biological control strategy may be successful on its own for pests with slow development and low voracity and fecundity; however, the release of a combination of other predatory or parasitic natural enemies is required for controlling R-strategist pests, especially aphids.

The green lacewing (Neuroptera: Chrysopidae) is another important species involved in the release of predatory natural enemies. During its larval stage, the larvae lacewing (often known as aphidlion) has similar praying habits to lady beetles and feeds on a wide range of small soft-bodied insects, i.e., aphids, whiteflies, scales, thrips, leafhoppers, mites, and even the eggs of some Lepidoptera pests [86], probably because it has prominent sucking mouthparts and well-developed legs, whereas most adults are not predaceous and only feed on pollen, plant nectar, and insect honeydew. Thus, lacewing larvae are highly effective agents in augmentative biological control programs [87]. Among the over 1200 chrysopid species known to date, several lacewing species have been primarily used in biological control programs in China, including Chrysoperla sinica Tjeder, Chrysopa septempunctata Wesmael, Chrysopa formosa Brauer, etc. [84]. As lacewing populations often lag behind their prey, directly releasing their eggs may not be effective in reducing the high infestation of target pests. Meanwhile, differences in the predaceous ability between different ages of lacewing larvae facilitate the rearing and release of the third instar lacewing larvae to attain maximum control efficiency. Similarly, most cases have reported that lacewing larvae often exhibit a functional type II response [88]. However, in comparison, the frequent release of commercially purchased lacewing larvae from insectaries can significantly increase the costs of agricultural production, likely because lacewing larvae have cannibalistic traits.

In addition, omnivorous insect predators, such as Nesidiocoris tenuis Reuter (Hemiptera: Miridae) and Arma chinensis Fallou (Hemiptera: Pentatomidae), could be alternative agents for the biological control of mites, thrips, whiteflies, aphids, and some moths in diverse crop systems used in augmentative biological control programs [89,90]. In recent decades, these two bugs have been successfully released to control target and invasive pests in China and other countries. Besides insect predators, some predacious mites (Acari: Phytoseiidae) are important agents used in the augmentative biological management of phytophagous mites and some agricultural, forest, and horticultural pests, including thrips, whiteflies, mealybugs, etc. For instance, native mite species, including Amblyseius brientalis Ehara, A. tsugawai Ehara and A. pseudolongispinosus Xin, Liang & Ke, and adventive species, including Neoseiulus barkeri Hughes, N. californicus McGregor, and Phytoseiulus persimilis Athias-Henriot, have been established as the most important beneficial arthropods used in augmentative biological control programs in China [84].

Although the abovementioned predatory natural enemies could effectively suppress the population density of target pests, the release of a combination of parasitoid insects during different periods of pest occurrence could further improve the effectiveness of pest regulation in augmentative biological control programs. Most of the identified insect parasitoids originate from the Hymenoptera order, with estimations indicating that 95,000 species of Hymenoptera parasitoids account for about 78% of the described species of insect parasitoids [91]. Among them, almost all species of Trichogrammatidae are egg parasitoids. Trichogrammatids have a broad host range, and more than 400 species, distributed into 11 orders of insects, are targets for trichogrammatids, including Homoptera, Coleoptera, Lepidoptera, Hemiptera, Orthoptera, Diptera, Odonata, Hymenoptera, Thysanoptera, and Neuroptera, most of which are agricultural and forest pests [92]. Only 20 out of the 800 species of trichogrammatids are mass-reared for the suppression of pest populations in cotton, corn, rice, vegetables, and other agroecosystems. Parasitic wasps from Chalcidoidea and Ichneumonoidea are the main biological control agents of Coleopterous, Lepidopterous, Hemipterous, and Dipterous pests, including some storage pests [92]. For instance, Encarsia formosa Gahan from Chalcidoidea has been widely used in whitefly biological control programs worldwide [93]. Platygastroidea parasitoids could be the potential parasitic natural enemies of true bugs, moths, and other insects [94]. These findings suggest that parasitoid wasps provide sufficient resources for developing and introducing valuable parasitoids that, together with more intensive parasitoid assemblages of pests, can be used in successful biological control programs under diverse environmental conditions. Moreover, microbial control agents, including entomopathogenic bacteria and fungi from the Hypocreales order, such as Beauveria bassiana, Akanthomyces attenuates, and Trichoderma spp., or Bacillus subtilis, etc., could attack a wide range of insect and mite species, and some of them are promising as potential biological agents [95,96].

Predators, parasitoids, and microbial control agents can complementarily attack a pest during different periods of its occurrence in agroecosystems, resulting in stronger pest suppression than a single-enemy species. Thus, the combined release of predators, parasitoids, and/or fungal pathogens in augmentative biological control practices can better prevent these detrimental effects in most agricultural practices. However, diverse natural enemy assemblages in natural communities may result in antagonistic effects on pest control, likely due to intraguild predation, mutual damage between predators and parasitoids, etc.

In comparison, conservation biological control is a moderate type of pest control because it does not release natural enemies and uses agronomic-based methods to alter the habitats and trophic conditions of biocontrol agents in order to aggravate their population densities in local agricultural ecosystems [97,98]. For instance, our previous review provided a comprehensive overview of current knowledge and advances in the role of intercropping systems in the conservation, attraction, or aggravation of the population densities of native predatory natural enemies to suppress pest population dynamics [75]. Thus, for cases in which the release of biological control agents is not possible, the conservation of its native biological control agents should be more considered.

5. Insect Pheromones and Their Potential Use in Pest Management

Insect pheromones are the most essential semiochemicals for insect survival and conspecific communication, and they present advantages for application in pest management, as pheromones commonly exhibit species-specific effects and are less toxic to the environment [99]. They can be divided into sex pheromones, aggregation pheromones, alarm pheromones, trail pheromones, etc., according to their mediatory intraspecific interactions [100]. In recent decades, advances in chemical ecology, especially with the rapid development of detection and sensitive analytical techniques, have significantly facilitated the isolation and identification of various insect pheromones. Meanwhile, considerable progress in synthetic biology has significantly promoted the large-scale production of artificial synthetic pheromones or parapheromones. These efforts have greatly contributed to establishing pheromone-based pest control measures, and various insect pheromones have been widely applied in cost-effective pest control.

Pheromone-based pest control techniques involve the application of artificial synthetic pheromones or parapheromones to simulate insect pheromones and selectively lure agricultural, horticultural, and silvicultural pests, thus manipulating their behavior to reduce pest populations. Several strategies have been implemented using this technique, such as attract and kill (A&K), mating disruption, mass trapping, repellents, etc. [100]. The “pulling” approaches, including A&K and mass trapping, involve the release of attractants (sex and aggregation pheromones) and guiding the pests toward an external location with a killing trap, while the “pushing” approach requires the release of alarm pheromones or a high concentration of sex and aggregation pheromones as repellents to push target pests away from their hosts [101,102]. Empirical studies have demonstrated that the push–pull approach mediated with different pheromones is an effective strategy for managing the population dynamics of pests in cropping systems [103]. Besides these passive tactics, sex-pheromone-mediated mating disruption is the most commonly used active strategy, which involves interference with mate finding and the reproduction of target pests through competitive and non-competitive mechanisms [104].

For developing more pheromone traps with synthetic lures, considerable efforts have focused on the determination of the chemical composition of economic pests. To date, thousands of pheromone compounds have been established, with most derived from the orders Lepidoptera and Coleoptera [105]. According to the existing literature, the sex pheromones of moths in the Lepidoptera order are the most studied, while the aggregation pheromones of bark beetles (Coleoptera: Scolytinae), a species considered the most destructive pests settled on sawtimber and pulpwood trees in North America, have been widely studied [105,106]. In comparison to sex pheromones, aggregation pheromones are employed by pioneer beetles to attract both sexes of conspecifics to their host trees for mate selection, to coordinate resource exploitation, and to perform gallery construction [106,107]. Significant successful cases regarding the control of some destructive Coleoptera pests using aggregation pheromones have been reported, especially in combination with plant volatile attractants. As the current study focused on highlighting the dominant pest management measures used for agricultural and horticultural crops, in this section, we only discuss the composition traits of sex pheromones and their potential use in the management of Lepidoptera pests.

As described previously, sex pheromones are considered the most important semiochemicals used in agricultural pest management. According to their chemical structures, moth sex pheromones are classified into four major groups: Type I, C₁₀–C₁₈ long-chain mono-unsaturated or di-unsaturated fatty alcohols, aldehydes, and acetates; Type II, C₁₇–C₂₅ polyunsaturated straight-chain hydrocarbons and their corresponding epoxide derivatives; Type III, C₁₇–C₂₅ compounds with one or more methyl branched chains; and Type 0 compounds, which are short-chain methylcarbinols and methyl ketones [108,109]. The sex pheromones isolated from the most commonly occurring moths in agricultural production belong to Type I compounds, accounting for approximately 75% of the total identified Lepidopteran pheromones. Type II compounds account for about 15%, and the others include Type III and Type 0 compounds [108]. Most of them are biosynthesized and released in sex pheromone glands, which are commonly located at the intersegmental membrane between the eighth and ninth abdominal segments in females [110]. Although sex pheromone components largely differ between species in the Lepidoptera order, some share the same components with distinct combinations [111]. For instance, the sibling species Helicoverpa armigera and H. assulta use Type I compounds, including (Z)-11-hexadecenal (Z11-16:Ald) and (Z)-9-hexadecenal (Z9-16:Ald), as essential sex pheromone components with reverse ratios of 97:3 and 7:93, respectively [112]. In addition, traps prepared with the application of a mixture of the two main sex pheromone components of oriental fruit moths (Grapholita molesta), including (Z)- and (E)-8-dodecenyl acetates (Z8-12:Ac; E8-12:Ac), also attract large populations of its sibling species, the European plum fruit moth (G. funebrana Tr.) [113]. It was demonstrated that the sex pheromones of G. funebrana are composed of Z8-12:Ac, E8-12:Ac, Z8-14:Ac, Z10-14:Ac, and Z8-12:OH at a ratio of 100:1:30:5:2, and that commercial synthetic lures for G. funebrana consist of Z8-12:Ac and E8-12:Ac at a ratio of 100:4, with the addition of other components exhibiting no synergistic effects [114]. Moreover, the major sex pheromone of Cydia pomonella, E8,E10-dodecadien-1-ol (E8,E10-12:OH), had apparent synergistic effects on the sex lure of male G. funebrana and G. molesta [115]. These findings suggest that developing traps with specific synthetic pheromone lures could be an efficient and environmentally sustainable control method for the management of diverse moth populations.

However, the direct release of natural pheromones in cropping systems has obvious drawbacks, including poor stability and a short duration of effect, which significantly hinder the broad application of pheromone-based pest control techniques. By addressing these challenges and guaranteeing control efficacy, aerosol delivery systems have been established and optimized to alter the emission rates and deployment of pheromones and significantly extend the duration of their effect [104]. Meanwhile, many low-rate pheromone-dispensing systems have been developed with the development of new materials in the field of material chemistry [116,117]. In addition, as described previously, the ratio and composition of the major components of natural moth sex pheromones require modification to develop traps in fields. Other factors including the trap design (e.g., type, color, height), trap location, type of dispenser, pheromone dose and purity, and environmental and weather conditions during the trapping period could influence its lure effects [118]. For the effective suppression of pest population densities, commercial firms engaged in pheromone-based pest control have successfully developed many species-specific pheromone-baited products and devices for mass trapping, as well as mating disruption systems in Rosaceae orchards, crops and vegetable fields, and forests, even for food storage. Currently, these pheromone-baited traps have been implemented as a control measure against G. molesta, the diamondback moth (Plutella xylostella) in crucifer crops, the red palm weevil (Rhynchophorus ferrugineus), the rice stem borer (Scirpophaga incertulas), and some other moths [109]. Moreover, new collaborations among academic researchers, industry stakeholders, and government agencies will facilitate the development and popularization of novel pheromone-baited traps in agricultural practice [109].

6. Concluding Remarks and Future Perspectives

This review illustrates and summarizes the potential applications and challenges of alternative environmentally friendly and effective strategies implemented in pest management. Although these pest management strategies could effectively suppress the population of some pests to low levels and prevent economic losses, depending on the measures used, it is hard to successfully control pest damage only through one of these methods, especially for R-strategist pests. Fortunately, significant advances in crop molecular breeding programs enable the large-scale cultivation of elite cultivars with desired pest resistance traits [119], thus prompting the effective control of target R-strategist pests using these pest management measures. This is likely because resistant cultivars can facilitate the long-term suppression of the population density of target pests [52]. Meanwhile, empirical studies have suggested that the combined use of some of these strategies would greatly increase the success rate in pest control and allow maximum efficiency to be achieved (Figure 2).

As diverse attackers are more likely to colonize different or similar niches of the same plant to obtain nutrients in agroecosystems [120], the direct spraying of biopesticides or chemical pesticides could rapidly suppress diverse pest population densities. Similarly, the uncontrolled application of chemical pesticides and the heavy selective pressure posed by the widespread and frequent use of biopesticides can significantly stimulate pest activity, thus increasing insecticide resistance, especially those with short generation times and stronger genetic plasticity. Therefore, sustainable agriculture requires additional efforts to decrease the susceptible thresholds of pests to chemical application. RNA interference (RNAi)-based methods play a crucial role in decreasing the rate of pests developing insecticide resistance, especially for suppressing the transcripts of the genes encoding the detoxifying enzymes of diverse pests [121,122]. For instance, a study investigating transgenic wheat plants expressing the double-stranded RNA (dsRNA) of the carboxylesterase E4 (CbE E4) gene fragment of S. avenae reported decreased transcript levels of the CbE E4 gene and impaired herbivore tolerance to phoxim (O,O-diethyl-Oa-oximinophenyl cyanophosphorothioate) insecticides [123]. Additionally, the direct spraying of the artificial synthetic dsRNA of detoxifying enzymes of diverse pests can also downregulate the transcript of target genes. In addition, recent advances in RNA chemical synthesis technology have enabled the efficient production of synthetic dsRNA, which not only improves the susceptibility of pests to diverse pesticides but also facilitates the development of RNA biopesticides. Meanwhile, nanomaterial-encapsulated dsRNA techniques have significantly increased the duration and stability of RNA biopesticides, which has led to the successful knockdown of the transcript of corresponding genes with artificial spraying [124,125]. For instance, the direct spraying of dsRNA targeting UDP-N-acetylglucosamine pyrophosphorylase with chitosan-modified nanomaterial significantly downregulated the transcript of target genes, resulting in the 48.9% mortality of the brown planthopper Nilaparvata lugens, whereas it did not exert any adverse effect on its important natural enemy Cyrtorhinus lividipennis [124]. Moreover, to prevent pests from acquiring RNAi resistance, the application of diverse alternative sprayable dsRNA products without widespread and frequent application is needed. Thus, the identification of sufficient and suitable candidate genes associated with vital activities, even those exhibiting lethal effects, could be a crucial prerequisite for the development of RNA biopesticides. With the assistance of an effective dsRNA delivery system, an increasing number of molecular target genes derived from diverse pests have been identified and have significantly downregulated the expression of corresponding genes. These findings suggest that RNAi-based pest management may be a promising measure for future crop protection.

In conclusion, the biological traits of pests enable them to rapidly adapt to various control measures, thus presenting an invisible “armament race”. A combination of the approaches highlighted in this review will significantly impede the ability of pests to develop resistance to biopesticides, hormone-triggered defenses, pheromones-based traps, RNAi pesticides, etc., and thus allow the maximum control efficiency to be achieved in agricultural practice (Figure 2 and Figure 3). This can be materialized with the release of biocontrol agents at appropriate times in the field through the large-scale cultivation of pest-resistant cultivars.