Biocontrol in Integrated Pest Management in Fruit and Vegetable Field Production

Abstract

The Farm-to-Fork strategy, an essential component of the European Green Deal, aims to establish a sustainable and healthy food system. A crucial aspect of this strategy is reducing synthetic pesticide use by 50% by 2030. In this context, biocontrol is seen as a vital tool for achieving this goal. However, the upscaling of biocontrol faces several challenges, including technical and socio-economic issues and concerns regarding the legal status of biocontrol products. This article focuses on the Positive List, which includes indigenous and introduced species that have been established for use in EPPO countries and approved biological agents in some OECD countries. This article discusses microbial control agents and active substances derived from microbial metabolites, macro-agents, semi-chemicals, and plant-based compounds. It covers their origins, active substances, mechanisms of action against target pests, application methods, market availability, benefits, and potential environmental side effects. Additionally, it discusses the role of beneficial insects and mites as natural enemies in Integrated Pest Management (IPM) within the context of conservation methods. This article addresses the future of biological control, which largely relies on advancements in science to tackle two critical challenges: enhancing the reliability and effectiveness of biopreparations in field conditions and developing suitable formulations of biopesticides tailored to large-scale cultivation technologies for key crops.

1. Introduction

The concept of Integrated Pest Management (IPM) originated in the late 1950s with the publication of a paper entitled ‘Integrated Management Concepts’ by Stern et al. [1] in the United States (US). Public concern over the harmful effects of pesticides on humans, mammals, birds, fish, and other non-harmful environmental organisms was sparked by Rachel Carson’s book, ‘Silent Spring’, released in 1962 [2]. However, despite these warnings, many highly toxic and persistent insecticides continued to be used widely without regulation or proper application methods until the 1980s. This resulted in various human health issues, environmental pollution, the development of pesticide-resistant insect populations, and the emergence of secondary pests. In response to these challenges, agencies focused on protecting human and animal health and the environment from pesticide-related hazards, and pesticide-related hazard mitigation measures were established.

The United States Environmental Protection Agency (USEPA) was created in 1970, followed by the creation of the European Food Safety Authority (EFSA) in 2002. In 1999, the Organization for Economic and Co-operative Development (OECD) initiated programs on biological pesticides (biopesticides) to assist member countries in harmonizing the methods and approaches used to assess these products and to enhance the efficiency of regulatory procedures [3].

Balog et al. [4] reported that over 1400 biopesticides (about 1000 active ingredients) have been registered worldwide. However, the European Union is currently at a disadvantage compared to the United States, India, Brazil, and China, considering the number of registered biopesticide active substances [3,4]. This disparity can be attributed to the complexities inherent in its regulatory processes [4].

1.1. Biopesticide Legislation in the European Union (EU)

In 2009, several legal acts were published in the EU that outlined statutory provisions related to the objectives of the Thematic Strategy. This set of regulations is commonly called the ‘Pesticide package’. The text includes Directive 2009/128/EC of the European Parliament and of the Council, which establishes a framework for community action promoting the sustainable use of pesticides. It also references Regulation (EC) No 1107/2009, which governs the marketing authorization of plant protection products. The directive highlights the importance of using non-synthetic chemical measures that pose a low risk of environmental pollution [3,5]. As of 1 January 2014, legal regulations in all EU Member States require plant producers to follow the principles of IPM. These regulations mandate that farmers explore all available natural methods of plant protection before turning to chemical solutions [6,7]. The European and Mediterranean Plant Protection Organization (EPPO) is an intergovernmental organization dedicated to protecting plants [6,8]. It achieves this by developing international strategies to prevent the introduction and spread of pests that threaten agriculture, forestry, and the environment. Additionally, the EPPO promotes the use of safe and effective pest control methods. One of its key responsibilities is to develop the EPPO Positive List, which contains a list of active substances approved for use in the EU [6,7]. There is a growing emphasis on reducing pesticide use as part of the European Green Deal, which aims for a 50% reduction in pesticide use by 2030 [6,7]. It is recommended that biological pest control methods be more widely publicized, as increasing awareness of their potential applications is essential.

The approval of microbiological biopesticides and other biologically active substances in the EU follows the same regulations as conventional synthetic pesticides under Regulation (EC) No 1107/2009 [4,6,9]. The data requirements for the approval of active substances, outlined in Commission Regulation (EU) No 283/2013, and for plant protection products, as specified in Commission Regulation (EU) No 284/2013, include a dedicated section (Part B) concerning microorganisms. This regulation mandates that data on the effects of biopesticides on bees must include information on their toxicity, infectivity, and pathogenicity. Additionally, it requires an assessment of the risks posed by metabolites produced by microorganisms, which often necessitates further specialized expertise and can be quite costly [6,7,9].

1.2. Biopesticide Legislation in the United States (US)

In turn, in the US, various laws regulate the use of pesticides, with the EPA serving as the primary federal agency responsible for overseeing pesticides sold or distributed in the country. The main federal law governing pesticides is the Federal Insecticide, Fungicide, and Rodenticide Act (FIFRA), which authorizes the EPA to grant licenses (registrations) for the sale and distribution of these products [10]. Under the FIFRA, these registrations must comply with the regulatory standard that ensures that their use does not result in unreasonable adverse effects on human health or the environment. The EPA has the flexibility to specify data requirements and can adjust these requirements on a case-by-case basis. Recognizing that some microbial and naturally derived biopesticides present a lower risk to human health and the environment than synthetic pesticides, the data requirements are tiered, starting with Tier I testing; further testing at higher tiers is only required if adverse effects are observed at lower levels [4,10]. This flexibility also includes considerations regarding the impact of biopesticides on bees [4,9]. Overall, these factors contribute to a quicker registration process for biopesticides.

This paper offers up-to-date information on significant biopesticides and living organisms mainly available in OECD member states and approved in the EU and the US, detailing their types, sources, and mechanisms of action against target pests and their effects on non-target organisms and pollinators. It evaluates their effectiveness in controlling pests affecting fruits and crops, ultimately highlighting the advantages of biopesticides and their growing acceptance among producers.

2. Biological Control

Biological control involves the use of natural enemies (biological agents), i.e., microorganisms (microbial control agents, MCAs) and macroorganisms (macro-agents—nematodes, parasitic and predatory insects, and mites), to reduce the population of plant pests [11,12]. According to Kumar et al. [13], the commercial use of beneficial organisms in biocontrol has rapidly developed over the past 40 years. Biological products (biopesticides) containing various biologically active substances of microbial metabolites, plant and animal-derived compounds, natural minerals, and semi-chemicals can also be used for pest control [14,15]. As highlighted by many authors, the main advantages of biopesticides as natural compounds compared to traditional pesticides are as follows: (i) lower toxicity to organisms that are harmless or beneficial; (ii) high specificity, i.e., their action is limited mainly to a given pest and/or species closely related to it; (iii) less susceptibility to the development of resistance in the pests being controlled; (iv) high potency at low doses; (v) rapid decomposition and biodegradation; (vi) low exposure and almost no emission problems; and (vii) lower risk to the biodiversity of plants, animals, aquatic and terrestrial organisms, and food chains [13,16,17]. The main difference between biopesticides and synthetic pesticides is their mode of action. The vast majority of synthetic insecticides have neurotoxic effects on pests (organophosphates, carbamates, pyrethroids, and neonicotinoids). Only some insecticides imitate juvenile hormones, for example, fenoxycarb, pyriproxyfen, and methoprene, which are ecdysone antagonists and chitin synthesis inhibitors (diflubenzuron), hindering reproduction and development and thus preventing the emergence of a new generation [17,18]. Biopesticides typically work by repelling or discouraging organisms from feeding. They can interfere with reproduction and metamorphosis, dehydrate pests, and lead to their suffocation [19]. Some biopesticides cause the death of insects through food poisoning or neurotoxic effects [13,20].

3. Types of Biopesticides

Biopesticides encompass various types, classified by their extraction sources and the specific molecules or compounds used for preparation. The categories are listed below.

3.1. Microbial Biopesticides and Their Metabolites

Frederiks and Wesseler [21] reported that 47 microbial biopesticide active substances (MBCAs) were registered in the EU and 73 in the USA between 2000 and 2018. There are currently 75 registered MBCAs in the EU [5]. Microbial biopesticides to control pests in fruit and vegetable field crops consist mainly of bacteria from Bacillus [22], baculoviruses [23], entomopathogenic fungi (EPFs) from Beauveria sp., Metarhizium sp., and Isaria sp. [19], and entomophagous nematodes from Steinernema sp. and Heterorhabditis sp. and also include the metabolites that the bacteria or fungi produce [24,25].

3.1.1. Bacterial Biopesticides

The most important bacterial pathogen used as a biological control agent is Bacillus thuringiensis (Berliner) (Bt). Toxins produced by a given subspecies and strain of Bt affect only a narrow group of hosts. It has been shown that insects belonging to the order Lepidoptera are highly sensitive to strains of the Bt ssp. kurstaki and Bt ssp. aizawai, while flies and beetles are sensitive to Bt ssp. israelensis and Bt ssp. tenebrionis, respectively [26]. Bt is a naturally occurring Gram-positive spore-forming bacterium that produces crystalline, proteinaceous insect δ-endotoxin with crystal proteins (Cry) and cytolytic (Cyt) toxins. The crystal breaks down into smaller fragments under the alkaline pH conditions in the digestive tract of larvae. Toxic protein molecules attach to receptors in the caterpillar’s midgut, causing intestinal perforation [26]. The effect of the toxins is a rapid cessation of feeding, illness, and then death of the larvae. The pests stop feeding after ingesting the bacteria (after about 30 min), and death usually occurs after 2–3 days [27]. Due to documented cases of some pests becoming resistant to Bt toxin, some new products are based on genetically modified Bt strains [28,29].

The most commonly used in apple and pear IPM programs are Bt ssp. aizawai and Bt ssp. kurtsaki, mainly for controlling caterpillars of moth species such as leafrollers from Tortricidae, i.e., summer fruit tortrix Adoxophyes orana, apple brown tortrix Pandemis heparana, barred fruit-tree tortrix Pandemis cesarana, and pests of apple fruit codling moth Cydia pomnella [30,31,32,33]. They can also be used to control leafrollers feeding on grapes, i.e., vine moth Eupoecilia ambiguella and European grapevine moth Lobesia botrana, and on stone and pome trees, such as peach moth Grapholita molesta and winter moth Operophtera brumata [34,35]. The application of Bt in an apple orchard reduced the degree of fruit damage to 9.7%, while in the unsprayed part, the rate was 34.0% or 12.0% [36] and 12.66% for treated trees, compared to 26.3% and 30.7% for the control [37].

In vegetable IPM, Bt biopesticides are efficient in controlling many cabbage vegetable pests like cabbage moth Mamestra brassicae, silver Y Autographa gamma, small white Pieris rapae, and tomato leafminer Tuta absoluta in tomatoes [38]. Also, Bt treatments led to a reduction of 85.7–94.6% in caterpillars of the diamondback moth [39], 23.4–70.1% in small white on cabbage [40], and 74.4–95.5% in pea moth in peas [41]. Some commercial products based on Bt and approved in most OECD countries are given in

Table 1. Entomopathogenic microorganisms and nematodes with trade names against fruit and vegetable pests.

Microorganism	Target Pests	Crops	Trade Name	References
Baculoviruses
Adoxophyes orana granulowirus AoGV	Lepidopteran larvae: Adoxophyes orana	Pome and stone fruit trees	Capex Plus	[42,43,44,45]
Anagrapha falcifera multinucleopolyhedrovirus AfMNPV	Lepidopteran larvae: Anagrapha falcifera, Chloridea virescens, and Helicoverpa armigera	Celery, tomatoes, pepper, and vegetables	Unknown name (registered in US)	[43,44]
Autographa californica multinucleopolyhedrovirus AcMNPV strain FV 11	Lepidopteran larvae: Trichoplusia ni	Vegetables	Loopex	[43,44,45]
Cryptophlebia peltastica nucleopolyhedrovirus CrpeNPV strain South Africa	Lepidopteran larvae: Cydia pomonella and Grapholita molesta	Pome and stone fruits and walnuts	CodlMax and MultiMax	[42,43]
Cydia pomnella granulovirus CpGV isolate CpGV-R5	Lepidopteran larvae: Cydia pomonella	Apple and pear trees, quince, and walnut	Carpovirusine, Carpovirusine Plus, Carpovirusine Super, Grandex Max, Granupom, Madex Max, Pavois, and Pomonellix	[39,40,41]
Cydia pomonella granulovirus Mexican isolate CpGV-M	Lepidopteran larvae: Cydia pomonella	Apple and pear trees	Carpostop	[42,43,44]
Cydia pomnella granulovirus CpGV strain CMGv4	Lepidopteran larvae: Cydia pomonella and Grapholita molesta	Apple and pear trees, peaches, nectarines, and apricots	Virosoft CP4 and Virgo	[40,41]
Helicoverpa armigera nucleopolyhedrovirus HearNPV	Lepidopteran larvae: Helicoverpa armigera, Helicoverpa zea, Mamestra brassicae, and Spodoptera frugiperda	Cabbage and other vegetables, lettuce, onion, sweet corn, and tomatoes	Biovirus-H, Biokill-H, Helicowex, and Helistop	[43]
Helicoverpa zea nucleopolyhedrovirus HearNPV	Lepidopteran larvae: Helicoverpa zea	Tomatoes, lettuce, cabbage vegetables, onion, sweet corn, and strawberries	Gemstar	[42,43,44]
Mamestra brassicae multinucleopolyhedrovirus MbMNPV	Lepidopteran larvae: Mamestra brassicae	Cabbage vegetables	Unknown name (registered in China	[43]
Pieris rapae granulovirus PiraGV	Lepidopteran larvae: Pieris rapae	Cabbage vegetables	Unknown name (registered in Korea)	[45,46]
Plutella xylostella granulovirus (PxGV)	Lepidopteran larvae: Plutella xylostella	Cabbage vegetables	Plutellavex (registered in Korea)	[46]
Spodoptera exigua multicapsid nucleopolyhedrovirus SeMNPV, isolate BV-0004	Lepidopteran larvae: Spodoptera exigua	Cabbage and other vegetables	Spod-X	[43,46]
Spodoptera frugiperda nucleopolyhedrovirus (SfMNPV) strain 3AP2	Lepidopteran larvae: Spodoptera exigua and Spodoptera frugiperda	Carrots, celery, legume vegetables, lettuce, and sweet corn	Fawligen	[43,44]
Spodoptera littoralis nucleopolyhedrovirus (SpliNPV)	Lepidopteran larvae: Spodoptera littoralis	Cabbage vegetables, peas, and tomatoes	Multiplex Spodomar and Spodopterin	[43]
Bacteria
Bacillus thuringiensis spp. aizawai strain GC-91	Lepidopteran larvae: Epiphyas postvittana, Platyptilia carduidactyla, Pierris rapae, Plutella xylostella, and Trichoplusia ni	Pome and stone fruit trees, berry bushes, grapes, and cabbage vegetables	Agree	[39,40,44]
Bacillus thuringiensis spp. aizawai strain ABTS-1857	Hymenopteran larvae: Hoplocampa flavum and Hoplocampa minuta Lepidopteran larvae: Adoxoyphyes orana, Agrotis sp., Cydia pomonella, Helicoverpa armigera, Mamestra brassicae, Pieris brassicae, Pieris rapae, Plutella xylostella, and Tuta absoluta	Pome and stone fruit trees, berry bushes, grapes, cabbage, other vegetables, and tomatoes	Florbac and XenTari	[42,43,47]
Bacillus thuringiensis spp. aizawai strain GC-91	Lepidopteran larvae: Spodoptera sp.	Vegetables	Bactercide	[47]
Bacillus thuringiensis spp. kurtsaki strain ABTS 351	Lepidopteran larvae: Autographa gamma, Cydia pomonella, Mamestra brassicae, Pieris brassicae, Pieris rapae, Plutella xylostella, Trichoplusia ni, and Tortricidae leaflorells	Cabbage vegetables, stone and pome fruit trees, grapes, and berries	Biobit, Bonide, Britz Bt, Caterpillar Killer, Dipel, Foray 48F, Ringer Vegetable Insect Attack, and Safer B.T.	[42,43,44,47]
Bacillus thuringiensis spp. kurtsaki strain EG 2348	Lepidopteran larvae: Agrotis sp., Eupoecilia ambiguella, Mamestra brassica, Lobesia botrana, Pieris brassicae, Pieris rapae, Plutella xylostella, and Tuta absoluta	Pome and stone fruit trees, grapes, and cabbage vegetables	Condor, Lepinox Plus, and Rapax AS	[42,44,47]
Bacillus thuringiensis spp. kurtsaki strain SA-11	Lepidopteran larvae: Agrotis sp., Cydia pomonella, and Plutella xylostella	Apple and pear trees and vegetables	Javelin	[47]
Bacillus thuringiensis, spp. kurstaki strain SA-12	Lepidopteran larvae: Duponchelia fovealis, Epiphyas postvittana, Lobesia botrana, Platyptilia carduidactyla, Tortricidae, leafrollers, and Trichplusia ni	Pome and stone fruit trees, grapes, pepper, and vegetables	Btk32, Bt Worm Killer, Deliver, Green Light, San 420 I, and Thuricide	[42,44,47]
Bacillus thuringiensis spp. kurtsaki strain BMP-123	Lepidopteran larvae: Agrotis sp., Eupoecilia ambiguella, Mamestra brassicae, Lobesia botrana, Plutella xylostella, Tortricidae leafrollers, and Tuta absoluta	Pome and stone fruit trees, grapes, and cabbage vegetables	BMP-123	[42,44,47]
Bacillus thuringiensis spp. kurtsaki strain EVB-113-19	Lepidopteran larvae: Agrotis sp., Cydia pomonella, Plutella xylostella, Spodoptera sp., Tortricidae leafrollers, and Trichoplusia ni	Pome and stone fruit trees and cabbage vegetables	Leprotec	[43,44]
Bacillus thuringiensis spp. kurtsaki strain EG7841	Lepidopteran larvae: Agrotis sp. Grafolita molesta, Grapholita packardi, Lobesia botrana, Spodoptera sp., Tortricidae leafrollers, and Trichoplusia ni	Vegetables, pome and stone fruit trees, and grapes	Crymax OG	[43,44]
Bacillus thuringiensis spp. kurtsaki strains EG7826, M-200, VPTS-2546, EG2348, PMP 123EG7826, EG7841, M 200	Lepidopteran larvae: unknown names	Vegetables and pome and stone fruit trees	Registered in US (unknown names)	[44]
Bacillus thuringiensis spp. tenebrionis ATCC-1252 strain NB 176	Coleopteran larvae: Leptinotarsa decemlineata	Potatoes	Novodor	[42,43,47]
Bacillus thuringiensis spp. tenebrionis strain SA-10	Coleopteran larvae: Leptinotarsa decemlineata	Potatoes	Trident	[44]
Streptomyces avermitilis	Dipteran larvae: Liriomyza sp. Thrips: Frankliniella occidentalis Mites: Tetranynchus urticae	Tomatoes, pepper, eggplant, and cucumber	Abamax, Acaramik, Agri-Mek S.Ci, Grot, Vertigo, and Vertimec (only under-cover crops in EU)	[42,44]
Saccharopolyspora spinosa	Coleopteran larvae: Leptinotarsa decemlineata Lepidopteran larvae: Cydia pomonella, Mamestra brassicae, Pieris brassicae, Pieris rapae, and Tortricidae leafrollers Dipteran larvae: Drosophila suzukii Thrips: Thrips tabaci	Cabbage vegetables, onion, potatoes, pome and stone fruits, and berries	Biospin, Blackhawk, Conserve, Entrust, GF-120, Naturalyte, Spinosad, SpinTor, and Seduce Insect Bait Teracer	[42]
Fungi
Beauveria bassiana strain GHA	Coleopteran: Otiorhynchus ovatus, Otiorhynchus sulcatus, and Leptinotarsa decemlineata Lepidopteran larvae: Autographa gamma, Mamestra brassicae, Pieris brassicae, Pieris rapae, Plutella xylostella, and Trichoplusia ni Hemipteran: Erythroneura elegantula	Cabbage vegetables, potatoes, strawberries, and grapes	Botanigard and Mycotrol	[42,44]
Beauveria bassiana strain ATCC 74040	Hymenopteran: Aphididae Coleopteran larvae: Elateridae Thrips: Thrips tabaci Mites: Tetranynchus urticae	Vegetables and strawberries	Naturalis and Naturalis Biogard	[42,44]
Beauveria bassiana strain IM 138521	Lepidopteran larvae: Heliothis armigera and Spodoptera litura Coleopteran: Anthonomus grandis and Listroderes costirostris Hemipteran: Empoasca fabae	Vegetables and fruit crops	Beauveria bassiana	[42]
Beauveria bassiana strain PPRI 5339	Lepidopteran larvae: Plutella xylostella and Thaumatotibia leucotreta Thrips: Thrips tabaci and other spp. Mites: Tetranynchus urticae	Cabbage vegetables, pepper, tomatoes, garlic, leeks, onions, peas, apricots, nectarines, peaches, plums, berries, and strawberries	Broadband OD	[44]
Beauveria bassiana strain 147	Coleopteran: Cosmopolites sordidus and Rhynchophorus ferrugineus	Bananas and palms	Ostrinil and Serenisim	[42,44]
Beauveria bassiana strain 203	Coleopteran: Rhynchophorus ferrugineus	Palms	Phoemyc+	[44]
Beauveria bassiana strain BB1	Hemipteran: Aphididae, Aleyrodidae, and Cicadellidae Lepidopteran larvae: Agrotis sp. and Spodoptera sp. Coleopteran: Scarabaeidae Thrips: Thrips tabaci and other spp.	Vegetables	Biopower	[45]
Beauveria bassiana strain ANT 003	Coleopteran: Leptinotarsa decemlineata and Holotrichia mindanaona	Potatoes, tomatoes, peppers, strawberries, and blackberries	Biotita and Bioceres	[45]
Isaria fumosorosea Apopka strain 97 (formerly Paecilomyces fumosoroseus)	Hemipteran: Aphididae and Aleyrodidae Thrips: Thrips tabaci and other spp.	Vegetables	Preferal	[42]
* Metarhizium brunneum strain F52	Coleopteran: Otiorhynchus sulcatus	Berry bushes and strawberry	Met 52	[45]
* Metarhizium brunneum Ma43 *	Coleopteran: Otiorhynchus sulcatus	Berry bushes and strawberry	Lalguard M 52	[44]
* Metarhizium brunneum strain FI-1045	Coleopteran: Scarabaeidae	Fruits and vegetables	Biocane	[44]
Heterorhabditis bacteriophora	Coleopteran: Chrysomelidae, Melolontha melolontha, Phyllopertha horticola, and Otiorhynchus sulcatus	Strawberries, grapes, and vegetables	Larvanem, NemaTrident–H, and NemaTrident−B	[42]
Steinernema feltiae	Lepidopteran larvae: Agrotis sp., Cydia pomonella, Tuta absoluta, and Spodoptera sp. Hymenopteran larvae: Hoplocampa minuta and Hoplocampa flavum Coleopteran: Elateridae, Otiorhynchus sulcatus, Otiorhynchus ovatus, and Scarabidea Dipteran larvae: Delia antiqua, Delia platura, Liriomyza sp., and Psila rosae	Pome and stone fruit trees, grapes, strawberries, berries, cabbage, and other vegetables	Entonem, Capriel, Sciarid, Biosafe -N, Scanmask, and NemaShield	[42,44]
Steinernema kraussei	Coleopteran: Otiorhynchus sulcatus	Strawberries	Nemasys L	[42,44]

* Metarhizium brunneum, formerly Metarhizium anisopliae var. anisopliae.

.

Bacterial biopesticides are available in powder or granulated form. Aqueous suspension preparations are easy to apply using sprayers, and they can be applied by professionals and allotment gardeners [47].

Due to the hidden nature of pests, the effectiveness of the available Bt and viral biopesticides may be limited. Therefore, all surfaces of the plants should be thoroughly covered with these products.

3.1.2. Viral Biopesticides

Insect pathogenic viruses are also a good source of microbial control agents. The most used are the genera Alphabaculovirus and Betabaculovirus from the family Baculoviridae. They produce inclusion bodies, i.e., nucleopolyhedroviruses (NPVs) with polyhedral shells, and granuloviruses (GVs) with granulin shells of the capsid ensure better virus survival in the environment [23]. Reid et al. [48] reported that, worldwide, approximately 60 bioinsecticides containing baculoviruses are used to control insect pests. Among the known baculoviruses, the NPV isolated from the caterpillar of the alfalfa looper, Autographa californica, has the highest host range, infecting 43 species from 11 families of Lepidoptera [49,50]. Most baculoviruses infect only the susceptible larval stage of insects. The exception is some NPVs that infect Hymenoptera larvae and adults. Insects are infected by the intestinal route, i.e., after the larvae consume food with polyhedral inclusion bodies (PIBs) or granules. In the alkaline environment of the intestine, the protein of the PIBs is dissolved, and occlusion-derived viruses cross the peritrophic membrane barrier and infect midgut epithelial cells. The larva stops feeding and dies of starvation and damage to the intestinal epithelium, which causes heavy diarrhetic disorder and death within 4 to 7 days [23]. The most effective virus in IPM in fruit orchards is Cydia pomonella granulovirus (CpGV). The biological efficacy of CpGV in reducing the coddling moth population density ranged from 75.5% to 96.0% and decreased to 50.0% from 10 to 20 days after treatment [51]. Four years of CpGV treatment by the direct spraying of apple trees lowered fruit injury at harvest to 3.0–7.0%, with a trend of further decline and stagnation at a level of 2.0–4.0% [50]. Recent studies indicate that some CpGV strains have a biological efficacy of 93.0% to 100.0% [52]. Contrary to expectations, the resistance of coddling moths to CpGV has been described in Europe [53]. That is why it is necessary to constantly search for new strains of entomopathogenic viruses with insecticidal properties. Commercial biopesticides with the CpGV approved in most OECD countries are available from several companies under different trade names (Table 1). In turn, Adoxoyphyes orana granuloviruses (AoGVs) can be used to control summer fruit tortrix (Table 1). In organic farming, two-time spring spraying with bioinsecticide Capex with AoGV at a dose of 100 mL/ha in the orchard had an effectiveness of 50.0–60.0%, which was increased to 81.0–94.0% by adding NeemAzal-T/S with azadirachtin [54]. Stará et al. [55] indicated that the use of Capex^® 2 with AoGV has a long-term effect on the pest population. The population density was reduced by AoGV below the economic threshold within two years after treatment with the virus. For CpGV and AoGV to be effective, they must be eaten by the youngest moth larvae before they burrow into the fruit, so they must be applied just before the caterpillars hatch from the eggs. In vegetable IPM, Plutella xylostella granulovirus (PxGV) infects caterpillars of the diamondback moth [56], and Helicoverpa armigera single nuclear polyhedrosis virus (Hear SNPV) infects the cabbage moth and other armyworms [57]. Also, other viral biopesticides are dedicated to controlling armyworms [58].

3.1.3. Mycobiopesticides

Entomopathogenic fungi are significant biological control agents due to their broad host range and effectiveness against sap-sucking pests and those with biting mouthparts. The infection typically begins when conidia or spores germinate upon contacting the host’s cuticle. Due to the action of enzymes, the fungus penetrates the host body, and the mycelium develops internally and colonizes the host. During this period, the fungus produces a variety of metabolites that promote its growth and toxins. The death of an insect is most often the result of mechanical damage to internal organs caused by the mycelium growing inside the insect’s body (mummification) and as a result of the production and release of toxins by the pathogen [59]. The main factor limiting the effectiveness of entomopathogenic fungi is their requirement for high humidity and moderate temperature for spore and conidia germination and development [60]. Their use as mycoinsecticides in the IPM of fruit crops and grapes is limited to the application of Bauveria bassiana and Metarhizium brunneum, formerly M. anisopliae [6], to control the larvae of the codling moth and apple clearwing moth Synanthedon myopaeformis, fruit fly Drosophila melanogaster, and black vine weevil Otiorhynchus sulcatus [61,62,63]. The results obtained by Godonou et al. [64] indicate that B. bassiana and M. brunneum hold great promise as biological agents in IPM measures against the diamondback moth on cabbage crops; the yield from crops treated with them was approximately three times higher than the yield in untreated plots. Moreover, Aynalem et al. [65] indicated that combined treatments with both fungal species and bacterium Bt improved the effectiveness of leaf protection to 95.3% in field tomato cultivation. M. brunneum effectively controls wireworms (Agriotes spp.) in potatoes and asparagus crops [66]. Furthermore, B. bassiana and M. brunneum are recommended to control aphids: cabbage aphid Brevicoryne brassicae, green peach aphid Myzus persicae, and pea aphid Acyrthosiphon pisum [67,68,69]. Biopesticides with M. brunneum and B. bassiana are available under many trade names, some of which are listed in Table 1. Fungal biopesticides can be applied as foliar treatments, through soil drainage, or by directly introducing them into the soil. Encapsulation techniques such as thermal gelation, ionic gelation, spray drying, and coacervation can be used to protect the fungi [60].

3.1.4. Entomophagous Nematodes as Biopesticides

Biopesticides containing entomophagous nematodes (EPNs) are becoming increasingly popular in IPM programs. Species of the two genera Steinernema and Heterorhabditis have been commercialized. Representatives of both genera inhabit soil environments worldwide [70,71]. When an infective juvenile enters the body cavity of a susceptible host, it enters the hemolymph, and symbiotic bacteria present in the nematode gut are released: Steinernema sp. releases Xenorhabdus sp., and Heterorhabditis sp. releases Photorhabdus sp. [72]. In the hemolymph, these bacteria multiply rapidly producing a wide range of toxins and exoenzymes that kill the host. The duration of the biological cycle is influenced by the environmental temperature, soil composition, moisture retention, oxygen supply, texture, and the species/strain of the nematode [73]. Usually, the host’s death occurs quickly, as 48 h is sufficient time for the bacteria to take effect [72].

In fruit IPM, Steinernema carpocapsae and S. feltiae are used to control the overwintering larvae of the codling moth [74], plum fruit sawfly Hoplocampa minuta, and plum sawfly Hoplocampa flavam [75], while S. carpocapsae and Heterorhabditis bacteriophora are used to control the apple sawfly Hoplocampa testudinea [76,77]. To control the larvae of the black vine weevil and strawberry root weevil Otiorhynchus ovatus in strawberries and berry crops, S. carpocapsa is also recommended for use [78,79]. S. carpocapsae expresses limited host search behavior (ambusher species), while S. feltiae and H. bacteriophora are more mobile and actively search for prey (the cruiser strategy) [73]. In field tomato crops, the foliar application of S. feltiae is recommended for controlling the caterpillars of tomato leafminers and the cotton bollworm [80,81]. To control armyworms and the larvae of leafminers (Liriomyza spp.) in vegetable crops, mainly S. feltiae and S. carpocapsa are recommended [62]. The trade names of some EPN biopesticides are listed in Table 1. EPN biopesticides are available in alginate gel, clay, and water-dispersible granules [78].

3.1.5. Microbe Metabolites as Biopesticides

Actinomycetes belonging to the Actinobacteria phylum are also recommended in IPM programs because they synthesize metabolites with insecticidal properties, such as avermectins and spinosyns. These compounds occur in the fermentation products of two species of actinomycetes, Streptomyces avermitilis (abamectin) and Saccharopolyspora spinosa (spinosad and spinosyn D), causing the paralysis and death of insects [25]. Spinosad disrupts the binding of acetylcholine in nicotinic acetylcholine receptors at the postsynaptic cell of the insect, leading to tremors and paralysis [82]. Abamectin is active against several species of mites, leafminers, and leafhoppers, while spinosad and spinosyn D are active against caterpillars, foliage-feeding beetles (Coleoptera), and thrips (Thysanoptera) [83]. Spinosad is a mixture (85.0%:15.0%) of spinosyn A and spinosyn D and is used in orchards to control codling moths. Lukehart [84] reported that the average fruit damage in the case of spinosad was 14.0% compared to the control, where as much as 51.0% of the fruit was damaged. Spinetoram is an analogue of spinosad, a mixture of two synthetically modified spinosyns (spinosyn J and spinosyn L) [85]. Depalo et al. [86] reported that spinetoram can also be considered a valuable tool in IPM strategies for the control of codling moths and oriental fruit moths. Since 2015, the use of spinetoram has been authorized in Spain to control spotted wing drosophila, Drosophila suzukii, on cherries and against psyllids (Psyllidae) in pear orchards. The best results for spinosad biopesticides are obtained by spraying young larvae; in the case of larger insects, higher doses of the insecticide are necessary. Spinosad and abamectin are available in the following forms: suspension, gel, paste, aerosol, solution, liquid, aqueous concentrate, jelly, and flakes [25,87]; these forms have been registered under various names (Table 1).

3.2. Macroorganisms as Biocontrol Agents (Insects and Mites)

In the available literature, the role of insects and mites as natural enemies in IPM has been widely discussed in the context of conservation methods and the release of some species of beneficial insects and mites [88].

3.2.1. Conservation Biocontrol

The main goal of conservation methods is to improve the quality of the living environment of beneficial arthropods by diversifying the landscape, creating shade, hiding places, and appropriate wintering places, and securing the necessary, diverse food base. The beneficial macro-agents most often inhabiting crops include predatory ladybird beetles (Coleoptera, Coccinellidae), ground beetles (Coleoptera: Carbidae), rove beetles (Coleoptera: Staphylinidae), lacewings (Neuroptera: Chrysopidae), hoverflies (Diptera: Syrphidae), aphis midges (Diptera: Cecidomyiidae), hemipterans like minute pirate bugs (Hemiptera: Anthocoridae, Anthocoris sp., Orius sp.), sting bugs (Hemiptera: Pentatomidae, Podisus sp.), earwigs (Dermaptera: Forficulidae), parasitoid wasps (Hymenoptera), such as braconid (Braconidae), chalicid (Chalcididae), ichneumon (Ichneumonoidae), pteromalid (Pteromelidae), and trichogrammatids (Trichogramatidae), and tachinid flies (Diptera: Tachinidae) [89,90,91,92,93]. A reduced share of intensive monocultures and greater landscape diversity are crucial for increasing biological control [94]. For example, in landscapes dominated by arable land, the biological control of aphids can be reduced by 46.0% compared to more diverse landscapes [95]. Planting strips of flowering plants, including wildflowers, a source of pollen and nectar, attracts beneficial insects and mites [96,97]. Intercropping apple orchards with aromatic plants increased predator abundance and species richness by 18.8 and 15.6%, respectively, compared with natural herb vegetation [98]. The presence of aromatic plants also reduced the population of leafrollers, summer fruit tortrix, apple fruit licker Spilonota lechriaspis, and yellow tortrix moth Acleris fimbriana due to the increased densities of parasitic wasps belonging to the braconid, ichneumon, and trichogrammatid wasps [99]. Cover crops and living mulches affect the density of coleopteran predator activity. Ground beetles are the best-known beetle predators of the codling moth; they dominate the epigeal zone around the tree base when caterpillars seek a cocooning site and moth cocoons are likely to be found [100]. Traditional hedgerows which also act as windbreaks around orchards support anthocorids (Anthocoris sp.) and also benefit other beneficial insects including European earwigs Forficula auricularia [101]. Flower strips and margins can also positively influence pest-beneficial insect relationships in vegetable crops. McGrath [102] found that annual wildflower strips (WFSs) in carrot crops attracted natural enemies of the willow-carrot aphid, Cavariella aegopodii, and contributed to yield. Hatt et al. [103] demonstrated that WFSs of 17 perennial field species increased hoverfly populations in pea crops, while adjacent forests may offer overwintering sites for parasitic wasps and allow for early parasitism. Also, an important element of conservation strategies is the rational use of selective chemicals, allowing for a reduction in their negative impact on beneficial organisms. Low pesticide doses and alternating spraying techniques in the middle of the row left shelter for the spider mite predator Stethorus punctillum (Coleoptera: Coccinellidae), which was a key factor in the effective biological control of tetranychid mites in orchards [104]. In apple trees, pyrethroids are especially harmful to the predatory phytoseiid mites (Acari: Phytoseiidae) [105]. Typlodromus pyri, Amblyseius andersoni, and Euseius finlandicus are the main predatory mites of the European red mite Panonichus ulmi and other tetranychid pests in apple orchards and vineyards in Europe [106,107]. The species richness of predatory mites in orchards is influenced by different protection systems (organic, IPM, and conventional) and—as new studies show—by the presence or absence of domatia on the leaves of different apple varieties [108]. It has been demonstrated that leaves with domatia are rich in predatory mites [109]. Mites use leaf domatia as a safe place to lay eggs and for molting. In the case of orchards with few or no beneficial mites, other strategies need to be developed to conserve generalist predators or to release pyrethroid-resistant mite strains.

3.2.2. Classical Biocontrol (Introducing Macro-Agents)

In fruit trees, vineyards, and strawberry, raspberry, and currant fields in Europe, North America, and New Zealand, the release of resistant strains of phytoseiid mites has been confirmed to be effective in controlling herbivorous mites [110,111,112]. In Europe, the most common method of dispersing T. pyri in orchards is the transfer of pruned branches and tree seedlings during periods of female hibernation or by establishing material strips with hibernating predators [113,114]. In turn, A. andersoni overwinters on the trees and in ground litter and can be transferred via ground litter from old to young apple orchards [115]. In the US and Canada, the commercial supplier of the spider mite destroyer Bio-nomics recommends its release against two-spotted spider mites and European red mites [104,116]. In turn, in Switzerland, it has been shown that the release of larvae of the two-spot ladybird, Adalia bipunctata, in an apple orchard significantly prevented the colony formation of the rosy apple aphid Dysaphis plantaginea [117]. Because these beetles are expensive to purchase, they are sold in only modest numbers compared to phytoseiid mites and are used mainly for occasional field application in small orchards and vegetable plots. The seven-spotted ladybird Coccinella septempunctata is also a very effective predator of aphids, but unfortunately, attempts to release these ladybirds in open fields have generally not been very successful, as released adults tend to disperse into adjacent fields and wastelands [118]. Also, the true bug Anthocoris nemoralis and the minute pirate Anthocoris nemorum are on the list of species permitted to be released in orchards in many European countries to control psyllids [119,120,121,122]. In 2004, in Denmark, true bug nymphs were released in three pear orchards naturally infested with pear psyllids, Cacopsylla pyri, and their populations were reduced by up to 40.0% [121]. As for the use of parasitic wasps in orchards, Aphelinus mali (Hymenoptera: Aphelinidae) has been released in apple orchards for many years to control the woolly apple aphid (WAA), Eriosoma lanigerum (Hemiptera: Eriosomatidae), in many countries [93,120,123]. However, according to some studies, the release of A. mali in apple orchards reduced the WAA population, although its effect was not high enough to prevent tree injury [124,125]. In an experiment by Alins et al. [126], researchers proved that releasing European earwigs in an apple orchard effectively reduced the aphid population, with visible effects noted starting in the second year after their release. These results emphasize the importance of considering the temporal scale within augmentative biological control strategies. Trichogrammatid wasps are the most widely exploited and used for pest management worldwide among all the egg parasitoids. Dodiya et al. [127] listed eleven species used worldwide, while in Europe, six sp. are listed in

Table 2. Commercially available natural enemies (parasitic and predatory insects and mites) used in orchards and vegetable crops in open fields in the EPPO region.

Species	Target Pests	Crops	References
* Adalia bipunctata: Coleoptera, Coccinalidae	Aphids: Toxoptera aurantia, Dysaphis plantaginea, and many others	Citron and fruit trees	[117,128]
* Aeolothrips intermedius: Thysanoptera, Aeolothripidae	Thrips: Frankliniella occidentalis and Thrips tabaci	Vegetables (onion, leek, tomatoes)	[119]
Aleochara bilineata: Coleoptera, Staphylinidae	Root flies: Delia antiqua and Delia radicum	Vegetables	[128]
* Amblyseius andersoni: Acari, Phytoseiidae	Mites: Aculops lycopersicae, Panonychus ulmi, Polyphagotarsonemus latus, Phytonemus pallidus, Tetranynchus cinnabarinus, and Tetranychus urticae	Apple and other fruit trees and vegetables	[115,128]
Anastatus bifasciatus: Hymenoptera, Eupelinidae	Sting (true) bugs: Halyomorpha halsy	Olive trees	[128]
Anthocoris nemoralis: Hemiptera, Anthocoridae	Psylids: Cacopsylla melanoneura and Cacopsylla pyri	Fruit trees	[120]
Anthocoris nemorum: Hemiptera, Anthocoridae	Psylids: Cacopsylla pyri	Pear trees and others	[120]
* Aphidius ervi: Hymenoptera, Braconidae	Aphids: Aulacorthum solani and Macrosiphum euphorbiae	Vegetables	[128]
Aphelinus mali: Hymenoptera, Aphelinidae	Aphids: Eriosoma lanigerum	Fruit trees	[119,120]
* Aphidoletes aphidimyza: Diptera, Cecidomyiidae	Aphids: Aphis gossypii, Aulacorthum sp., Macrosiphum sp., and Myzus persicae	Vegetables	[128]
* Aphytis lingnanensis: Hymenoptera, Aphelinidae	Scale: Aonidiella aurantii	Citrus trees	[128]
* Aphytis melinus: Hymenoptera, Aphelinidae	Scale: Aonidiella aurantii	Citrus trees	[128]
Chilocorus bipustulatus: Coleoptera, Coccinalidae	Scale: Saissetia oleae	Olive trees	[128]
Coccinella septempunctata: Coleoptera, Coccinalidae	Aphids	Fruit trees and vegetables	[119,120,128]
* Comperiella bifasciata: Hymenoptera, Encyrtidae	Scale: Aonidiella aurantii and Chrysomphalus aonidum	Citrus trees	[128]
* Cryptolaemus montrouzieri: Coleoptera, Coccinalidae	Scale: Planococcus citri	Citrus trees	[128]
* Chrysoperla carnea: Neuroptera, Chrysopidae	Aphids: Aphis pomi and many others	Apple trees and others	[120,128,129]
* Dacnusa sibirica: Diptera, Braconidae	Flies, leafminers: Liriomyza sp.	Celery, lettuce, and tomatoes	[128]
* Diglyphus isaea: Diptera, Eulophidae	Flies, leafminers: Liriomyza sp.	Celery, lettuce, and tomatoes	[128]
* Episyrphus balteatus: Diptera, Syrphidae	Aphids	Fruit trees and vegetables	[128]
* Eupeodes corollae: Diptera, Syrphidae	Aphids	Fruit trees and vegetables	[128]
Kampimodromus aberrans: Acari, Phytoseiidae	Mites: Panonychus ulmi	Fruit trees and grapes	[130,131]
* Leptomastix dactylopii: Hymenoptera, Encyrtidae	Scale: Planococcus citri	Citrus trees	[128]
* Leptomastix dactylopii: Hymenoptera, Encyrtidae	Scale: Planococcus citri	Citrus trees	[128]
* Metaphycus helvolus: Hymenoptera, Encyrtidae	Scale: Coccus hesperidum and Saissetia oleae	Olive trees	[128]
Metaphycus lounsburyi: Hymenoptera, Encyrtidae	Scale: Saissetia oleae	Olive trees	[128]
* Microterys nietneri: Hymenoptera, Encyrtidae	Scale: Saissetia oleae	Olive trees	[128]
* Phytoseiulus persimilis: Acari, Phytoseidaee	Mites: Tetranychus urticae	Tomatoes, cucumbers, and peppers	[128]
Picromerus bidens: Hemiptera, Pentatomidae	Coleopteran: Leptinotarsa decemlineata	Potatoes	[128,132]
Podisus maculiventris: Hemiptera, Pentatomidae	Coleopteran: Leptinotarsa decemlineata	Potatoes	[128,132,133]
* Propylea quatuordecimpunctata: Coleoptera, Coccinalidae	Aphids	Vegetables	[120]
* Sphaerophoria rueppellii: Diptera, Syrphidae	Aphids, whiteflies, thrips, and mites	Fruit trees and vegetables	[128]
* Trichogramma brassicae: Hymenoptera, Trichogrammatidae	Lepidopteran eggs: mainly Ostrinia nubilalis	Sweet corn and cabbage vegetables	[119,128]
Trichogramma cacoeciae: Hymenoptera, Trichogrammatidae	Lepidopteran eggs: Cydia pomonella and Grapholita funebrana	Apple and plum trees and tomatoes	[119,128]
Trichogramma cordubensis: Hymenoptera, Trichogrammatidae	Lepidopteran eggs: Lobesia botrana and Eupoecilia ambiguella	Grapes	[128]
Trichogramma dendrolimi: Hymenoptera, Trichogrammatidae	Lepidopteran eggs: Cydia pomonella	Apple and pear trees	[119,128]
* Trichogramma evanescens: Hymenoptera, Trichogrammatidae	Lepidopteran eggs: Cydia pomonella and other species	Sweet corn and cabbage vegetables	[119,128]
* Trichogramma pintoi: Hymenoptera, Trichogrammatidae	Lepidopteran eggs: Cydia nigricana, Cydia pomonella, Grapholita funebrana, Helicoverpa armigera, Lacanobia oleracea, Mamestra brassicae, Plutella xylostella, and Ostrinia nubilalis	Sweet corn, peas, vegetables, and apple and pear trees	[128]
* Trichopria drosophilae: Hymenoptera, Diapriidae	Flies: Drosophila suzukii	Grapes and soft fruits	[128]
Typhlodromus pyri: Acari, Phytoseiidae	Mites: Epitrimerus vitis, Panonychus ulmi, and Tetranychus urticae	Apples and pear trees and grapes	[119,120,128]

* Also intended for indoor release.

.

For example, Trichogramma cacoaciae, Trichogramm dendrolimi, Trichogramm pintoi, and Trichogramma evanescens are commercially available for use against the codling moth, as is T. cacoaciae to control the plum fruit moth and Grapholita funebrana [128,134]. They are released in two ways: one is Trichocard, and the other is release as pupae or adults by an unmanned aerial system [135]. The synergistic effect of combining the sterile insect technique, mating disruption techniques, and the mass release of eggs of different trichogrammatid wasps to control codling moths in commercial apple orchards apple trees has been proven in Canada, Argentina, and Denmark [135,136,137,138]. In Denmark, mating disruption techniques and the mass release of T. evanescens and T. cacoaciae to control coddling moths in apple orchards is a promising biocontrol method [138]. Trichogrammatid wasps are also used to control European grapevine moths and vine moths on grapes [128,139]. In California, Mills [140] suggested that the release of Trichogramma spp. can reduce codling moth damage by 50.0% in walnuts and pears. The suitability of Trichogramma brassicae to control the silver Y moth in spinach was investigated under field conditions in Germany. Parasitism rates were as high as 20.0% and 16.0–19.0% on the fourth and ninth day after the mass release of parasitic wasps, respectively [141]. In turn, the parasitism rate of cabbage moth eggs after the release of T. brassicae was 62.0–100.0% [138], and against the pea moth and the leek moth, the figure for Acrolepiopsis assectella was about 56.0% [142]. In Florida, Hu et al. [143] indicated that Cotesia plutellae released in fields did not survive for longer than a year because the species does not survive winters there. Therefore, this wasp, as a biocontrol agent for the diamondback moth, could be limited to annual inoculative release [144]. Ichneumonid wasps Diadegma fenestralis, Diadegma semiclausum, and Diadegma insulare also have great potential in controlling the diamondback moth in field vegetable crops [93,120,145,146]. A list of some macro-agents dedicated to release in orchard and field vegetables is presented in Table 2.

The major factors limiting the efficacy of the release of macro-agents include their dispersal or quality, intraguild predation, compensatory mortality, and environmental conditions (ecological limits) [147]. The tendency of introduced arthropods to escape and disperse to nearby areas can be partially addressed by implementing a conservation method for biocontrol, which involves managing habitats to promote the development and overwintering of beneficial organisms [95,96,97,102]. Also, the cost of beneficial arthropods is a constraint for release [147]. Future research should focus on finding solutions to counteract ecological constraints by skillfully combining different species of natural enemies and/or combining the release of natural enemies with low-risk pesticides.

3.3. Semiochemicals: Pheromones and Kairomones

3.3.1. Pheromones

Semiochemicals, including pheromones, represent one of the components of integration-based orchard and vegetable pest management [148,149]. Pheromones are specific to a given species, enabling intraspecies communication by eliciting a response in the recipient. These substances or mixtures of substances released by the organism trigger a behavioral or physiological response in an individual of the same species. A characteristic feature of pheromones is their action at low concentrations. Pheromones play a crucial role in influencing social structure and reproductive behaviors in insects [150,151]. These compounds are completely safe for beneficial insects and other arthropods and at the same time enable significant manipulation of pest behavior [151]. In practice, the action of pheromones comes down to using the following strategies: mating disruption (MD) of individuals for reproduction; mass trapping (MT), attracting, and killing using another factor (pesticide, glue, liquid, mechanical, etc.), and the push–pull strategy [152,153,154]. This strategy involves manipulating insect pest behavior using a two-pronged strategy: pushing target pests away from the crop and attracting them toward the trapping system [155]. Repulsion and attraction are accomplished using push and pull signals, usually volatile substances, including alarming, aggregation or anti-aggregation, attracting sexual partners and host-marking pheromones, and/or allelochemicals [153,156,157,158,159]. The push–pull strategy is becoming increasingly popular because it can increase the effectiveness of capturing aphids or fruit flies [160,161]. An example where the push strategy has proven to be very effective is the use of the oviposition-deterring pheromone of the cherry fruit fly Rhagoletis cerasi in cherry orchards. This treatment reduced infestations of this pest by 90.0% [162]. Also, pheromones can determine appearance dates, economic thresholds, and treatment timings with chemicals [162,163,164]. The first commercially available pheromone dispenser with sex pheromones for control the coddling moth was Isomate-C^®, which became available in the USA in 1991 [165]. Since then, a wide range of pheromone delivery systems has been developed and made available, and they have become popular not only among professional farmers but also among gardeners and allotment owners [149,162]. Global estimates suggest that over 800,000 hectares of agricultural pests are managed with MD. On a large scale, the MD strategy is implemented in the IPM of apples, pears, peaches, grapes, and soft fruits [166]. Mating disruptions were implemented to control over 120,000 hectares of vineyards in France, accounting for 17% of the total [167]. About 90.0% of pome fruit growers in Washington State, USA, use MD in their insect control programs [168], with a comparable percentage of use in apple orchards in the Trentino region in northern Italy [169]. For the codling moth, there are many options for exploiting semiochemicals, such as mass trapping (MT) or mating disruption (MD) using female-produced sex pheromones or female repellents and attractants using allelochemicals. The effectiveness of these methods is influenced by many factors such as the shape and size, isolation, and environment of orchards, release rates of substances, weather, wind conditions, number, and inter-trap spacing, as well as the initial density of the codling moth population [170,171,172]. Strategies vary in effectiveness; for example, mass trapping alone is unreliable at economic thresholds [173]. The efficacy of mating disruption in apple orchards was 52.4 and 95.8% [174], 86.9% and 97.6% [175], and 67.6% and 73.5%, even when it was combined with the application of insecticide treatments [176]. To increase the effectiveness of MD, it can be combined with other methods such as crop sanitation, insect growth regulators (IGRs), mineral oils, Bt toxins, CpGV, entomopathogenic nematodes to kill overwintering larvae, sterile insect techniques, and chemical treatments, especially in orchards with high pest population pressure [177,178,179]. Also, it is recommended to control leafrollers like the summer fruit tortrix, appleseed moth Grapholita lobarzewskii, peach moth, apple brown tortrix, bud moth Spilonota ocellana, and leafrollers in vineyards, i.e., the vine moth and European grapevine moth, using MD [31,180,181,182,183,184]. Additionally, female attractants such as acetic acid, pear ester, and (E)-4,8-dimethyl-1,3,7-nonatriene can influence the behavior of female codling moths, causing a reduction in their population and oviposition [185,186,187]. Traps baited with lures containing pear ester, acetic acid, (E)-4,8-dimethyl-1,3,7-nonatriene, and pyranoid linalool oxide captured more than twice as many codling moth specimens as traps baited with sex pheromone, pear ester, and acetic acid. Notably, 55.0% of the caught individuals were females [188,189]. Currently, several products containing sex pheromones are available for controlling the codling moth. These include CheckMate Puffer CM, Ecodian-CP VP, SemiosNET-Codling Moth, Isomate CLS, and Isomate CTT. For the summer fruit tortrix, RAK 3 and 4 are available, while Isonet Z can be used for the currant clearwing, Synanthedon tipuliformis [190]. In cabbage vegetables, sex pheromones are used for the monitoring and mating disruption of many species of Agrotis spp. moths, e.g., the silver Y, cabbage moth, cabbage looper Trichoplusia ni, diamondback moth, and fly of swede midge Contarinia nasturtii [191,192,193,194,195]. In turn, MD is used in pea crops for the pea moth, in cucumber for the cucumber moth Diaphania indica, and in tomatoes and other crops for the tomato pinworm Keiferia lycopersicella, tomato leafminer, and cotton bollworm [149,196,197,198]. Mass trapping (MT) with aggregation-pheromone-baited traps offers promising prospects in controlling the striped flea beetle Phyllotreta striolata in vegetable brassicas [149,199]. The MT technique aims to catch the maximum number of pests and has been used in fruit orchards to control Mediterranean fruit flies [200]. In turn, the attract-and-kill strategy is designed to control the pea leaf weevil Sitona lineatus using aggregation pheromone combined with contact insecticide [201]. Pheromonal control involves using dispensers that continuously release pheromones into the environment throughout the flight period of the target insects. The emission of pheromones is crucial for optimizing their impact on pest control effectiveness. Controlled release systems (dispensers) are the basis for achieving release rates. The differences between them concern the method of application, dosing, and release of different types of compounds with various chemical and physical properties over time, the protection of substances against degradation caused by environmental factors, and exploitation costs [202,203,204]. Two primary types of devices have been recommended for semiochemical application: retrievable dispensers and passive non-retrievable dispensers [42]. Pheromone-impregnated lure is encased in a conventional trap such as a bottle, delta, water pan, or funnel trap [205]. Research also indicates that emitters should be monitored throughout the field season because pheromone release rates vary with environmental conditions and may be highly dependent on formulation additives [203,204]. Pheromone molecules must be protected from degradation by UV light and oxygen. Also, high wind speeds can dilute pheromone concentrations. Research conducted by El-Sayed et al. [206] provides the first evidence that climate change affects the pheromone molecules’ stability, thus reducing their biological efficacy. In turn, environmental conditions and the rate at which substances are released can affect the amount of pollutants released into the environment and the effects these substances have on human health (skin irritants and/or sensitizers) and the environment [207]. It is essential to identify any absence of side effects during the pheromone registration process. Currently, the regulation of semi-chemicals used in plant protection mirrors that of conventional pesticides. This results in lengthy approval processes for products based on these substances [6,7,42]. Pheromones can be combined with attractive plant-derived kairomones to increase the efficiency of monitoring traps.

3.3.2. Kairomones

Kairomones may act as attractants secreted by the host insect, luring parasitoids or predators to the area where they occur. They make finding prey easier and stimulate the process of laying eggs in or near the host’s body [208,209]. The effectiveness of kairomones in attracting natural enemies to enhance the biological control of insect pests was studied under field conditions. Methyl salicylate, which is a volatile component of grape herbivore-induced mixtures, attracts predatory insects such as the green lacewing Chrysopa nigricolis, Chrysopa oculate, the predatory plant bug Deraeocoris brevis, the minute pirate bug Orius tristicolor, and the seven-spot ladybird [210,211]. Jones et al. [212] identified pest-induced plant volatiles in an apple orchard (squalene, iridocycline, and benzaldehyde) as attractants for ground beetles, Chlaenius nigricornis and Chlaenius oculata, and lacewing Chrysoperla plorabunda. In turn, dimethyl disulfide, which is released by cruciferous vegetables during the feeding of the cabbage fly Delia radicum, has an attractive effect on Aelochara bilineata (Coleoptera, Staphylinidae) [213]. Such studies have also been conducted to evaluate volatile substances as attractants in pears [214], cherries [215], and strawberries [216]. The kairomone phenylacetaldehyde, present in honeydew secreted by the cotton aphid Aphis gossypii, attracts the predatory fly aphid midge Aphidoletes aphidimyza [217]. The honeydew excreted by the pea aphid was identified as an arrestant and a contact kairomone for young larvae and adults of a common predatory hoverfly, Episyrphus balteatus [218]. In recent years, the use of kairomones in field conditions has mainly focused on attracting natural enemies to crops and retaining them. The combined use of the attractant synthetic methyl salicylate and coriander plants as a reward led to increased numbers of predatory thrips Franklinotrips vespiformis and predatory true bugs Orius insidiosus on bean plants [219].

3.4. Plant-Origin Biopesticides

Essential oils (EOs) and plant extracts from azadirachtin and pyrethrum, followed by nicotine and rotenone, are the botanical products most frequently used as biopesticides [220].

3.4.1. Plant Extracts

Plant extracts are typically obtained from dried plant material, mainly by a solid/liquid extraction method using aqueous or organic solvents, e.g., acetone, ethanol, hexane, and methanol [221]. Water extracts provide several benefits, including being easily degradable, non-persistent in the soil, and non-toxic to animals and humans [222]. Organic solvents such as ethanol and methanol are frequently used to obtain plant extracts due to their low toxicity and acceptance by the food industry [223]. When using organic solvents, it is essential to prepare a suitable formulation for application to plants. These formulations usually consist of the extract, water, oil, and a surfactant [224]. Different extraction methods can produce varying concentrations of bioactive molecules in the extracts. For example, methanolic extracts may contain higher concentrations of bioactive compounds than aqueous extracts [225]. There are several methods for applying natural extracts, including seed priming, soil supplementation, and foliar spraying; however, foliar spraying is the most popular method [226]. As a result, the extracts obtained are typically filtered to remove plant residues that could clog the sprayer [227]. The most commonly used concentrations for extracts are up to 10% [225].

Azadirachtin is a natural active substance belonging to the limonoid class. It is isolated from several species of neem trees belonging to the Meliaceae family, and Azdirachta indica is the most important species of this group [228]. It acts as an antifeedant on some groups of insects, disturbing their feeding abilities. Its effects are mediated through contact chemoreception (primary antifeedant effect) and a direct inhibitory effect on protein biosynthesis in the midgut, and this could account for the observed secondary antifeedant effects [229,230]. The ability of azadirachtin to inhibit protein synthesis has been demonstrated in the case of Colorado potato beetles treated with neem and toxin Bt [231]. Azadirachtin also exerts repellent, insecticidal, and development-inhibiting effects against insects by disrupting their growth and molting processes by interfering with ecdysone production [232,233]. The complete inhibition of molting caused by the blockage of the synthesis and release of ecdysteroids was observed in the migratory locust, Locusta migratoria [230]. In turn, reduced fecundity has been recorded in the fruit fly Drosophila melanogaster, the American serpentine leafminer Liriomyza trifolii, the Mediterranean fruit fly, the green peach aphid, the cabbage moth, and the tomato leafminer [234,235,236,237,238,239,240]. Ikeura et al. [241] observed a repellent effect of neem seed kernel oil cake against cabbage moths. In a field test, the damage to komatsuna Brassica rapa var. peruviridis and spinach Spinacia oleracea plants treated with azadirachtin was 40.0% and 30.0%, while untreated control plants were damaged at a level of 70.0%. A total of around 400 species of insects are sensitive to azadirachtin [242]. Neem-derived extracts are promising for the control of many target insect pests, including those mentioned earlier and the diamondback moth, the large white, the citrus root weevil, Diaprepes abbreviates, the pear leaf blister moth Leucoptera xitella, the European grapevine moth, the apple ermine Yponomeuta malinellus, whiteflies, tetranychid and eriophyid mites, and various other pests that bite and suck plants or mine them, as summarized in

Table 3. Main plant extracts and essential oils used as biopesticides.

Plant Product Used as Biopesticide	Origin	Target Pests	Mechanism of Action
Azadirachtin	Neem tree Azadirachta indica, Meliaceae	Aphis pomi, Dysaphis plantaginea, and other aphids, psyllids Psylinae sp., and a variety of sucking and chewing insects in vegetable and fruit crops	Antifeedant and disruptor of insect growth by blocking the release of the morphogenic peptide hormone [242]
* Nicotine	Tobacco Nicotiana tabacum, Solanaceae	Aphids, whiteflies, leafhoppers, Hypothenemus hampei, thrips, and mites	Neurotoxic, acetylcholine mimic, and agonist of nicotinic acetylcholine receptor [243,244]
Pyrethrins	Dalmatian pyrethrum Tanacetum cinerariifolium, Asteraceae	Aphids, whiteflies, Trichoplusia ni, flea beetles, Ceratitis capitata, leafhoppers, and thrips	Neurotoxic and disruptor of the sodium and potassium ion exchange process in insect nerves [245]
* Rotenone	Derris sp. and Lonchocarpus sp., Fabaceae	Aphids, Crioceris asparagi, Cerotoma trifurcata, Leptinotarsa decemlineata, Diabrotica undecimpunctata, flea beetles, and Galerucella tenella	Mitochondrial complex I electron transport inhibitor [245]
Citronella oil	Cochin grass Cymbopogon nardus and Java citronella Cymbopogon winterianu, Poaceae	Aphids, Helicoverpa armigera, Spodoptera littoralis, Tetranychus turkestani, and thrips	Repellent, oviposition deterrent, and inhibitor of AChE and glutathione-S-transferase [246,247]
*Cynamon oil	Cinnamon Cinnamomum sp., Lauraceae	Spodoptera littoralis, Plutella xylostella, and storage pests: weevils	Repellent, reducing the fecundity, fertility, and vitality of insects [245]
Clove oil	Clove Syzygium aromaticum, Myrtaceae	Phyllotetranychus egypticus, psyllids, and pests of stored peas and beans	Repellent, neurotoxic, and inhibitor of acetylcholinesterase [247,248]
* Eucalyptus oil	Eucalyptus globulus, Myrtaceae	Ascia monuste, Ceratitis capitata, and pests of stored products	Repellent, toxic, and activator of enzymes of intermediary metabolism [245,249]
* Lemongrass oil	Cochin grass Cymbopogon flexuosus, Poaceae	Agrotis ipsilon, Spodoptera frugiperda, Trichoplusia ni, and Tuta absoluta	Repellent, neurotoxic, and inhibitor of acetylcholinesterase (AChE) [250,251,252]
Mint oil	Spearmint Mentha spicata, Lamiaceae	Bactrocera oleae, Drosophila suzuki, and Tuta absoluta	Repellent, neurotoxic, and inhibitor of acetylcholinesterase (AChE) [245,253]
* Oregano oil	Oregano Origanum vulgare, Lamiaceae	Spodoptera littoralis and storage pests: weevils	Repellent, toxic, and reduces the fecundity, fertility, and vitality of insects [254]
Orange oil	Seville oranges (bitter oranges) Citrus × aurantium f. aurantium, Rutaceae	Trichoplusia ni, Aphis gossypii, Spodoptera frugiperda, Spodoptera littoralis, psyllids, leafhoppers, whiteflies, thrips, and mites	Physical mode of action, toxic, repellent, and neurotoxic [245,255]
* Rosemary oil	Rosemary Salvia Rosmarinus, Lamiaceae	Callosobruchus maculatus and Tetranychus urticae	Repellent, neurotoxic, and inhibitor of cetylcholinesterase (AChE) [245,256]
* Tea tree oil	Tea tree Melaleuca alternifolia (Myrtaceae)	Cotton leafworm Spodoptera littoralis and Ceratitis capitata	Repellent and toxic [245]
* Thyme oil	Thyme Thymus vulgaris and Thymus pulegioides, Lamiaceae	Tetranychus cinnabarinus, Glyphodes pyloalis, and storage pests	Repellent, toxic, and oviposition deterrent [245,257,258]

* Not approved in the EU according to [5].

.

Azadirachtin is most effective as a growth regulator on eggs and young larvae, e.g., in the case of the diamondback moth, it acts on third-instar larvae, for the tomato leafminer, it acts on second-instar larvae, and for the European grapevine moth, it acts on first-instar larvae—thus, application timing is paramount for successful control [259,260]. Many authors emphasize that azadirachtin is selective, easily degradable, and safer for non-target and beneficial organisms [261,262]. Akol et al. [263] did not demonstrate a negative effect of azadirachtin on the survival and feeding of parasitic Diadegma sp. when it was used to control the diamondback moth. Some researchers question the safety of azadirachtin, especially for pollinating insects [264]. Azadirachtin can work synergistically with other botanical compounds such as pyrethrin [265] and increase the efficacy of Bt toxins against the codling moth and SfNPV against the fall armyworm, Spodoptera frugiperda [266,267]. In turn, Hirose et al. [268] found that neem oil had a fungitoxic effect on two entomopathogenic fungi, M. anisopliae and B. bassiana. Many products derived from neem are produced by crushing the seeds and other parts of the plant, using various solvents to extract the active ingredients that have pesticidal activity. This can result in different active compound concentrations and, therefore, different efficacies. Singh et al. [269] found that among the three neem products used, neem oil (58.3% and 57.9%) was the most effective in reducing the cotton leafworm Spodoptera litura in field cauliflower, followed by neem seed kernel extract (54.8% and 55.2%) and neem leaf extract (50.70% and 51.42%). The results of Kumari et al. [270] revealed that azadirachtin 0.03 EC at a dose of 5 mL/ha reduced the number of coriander aphids Hyadaphis coriandri on fennel by 51.7%, and neem seed kernel extract 5.0% reduced the number of aphids by 50.8%, while neem oil 1.0% reduced the number of aphids by 48.1%. For controlling apple aphids Aphis pomi, two concentrations of neem oil (2.0% and 3.0%), neem seed kernel extract (NSKE) (4.0% and 5.0%), and azadirachtin (0.2% and 0.3%) were compared. The highest mean aphid mortality of 68.9% was recorded with azadirachtin (0.3%), followed by 65.1% with the same pesticide at a 0.2% concentration, while the lowest was with NSKE, 44.4% and 48.8% at concentrations of 4.0% and 5.0%, respectively [271]. In addition to foliar application, azadirachtin can also be applied to the soil. Soil treatment with azadirachtin in bean plants led to a significantly higher mortality of western flower thrips [272]. Many biopesticides with azadirachtin are commercially available and are listed in Table 3. Preferably, azadirachtin in pesticide formulations should range from about 0.1% to about 5.0% by weight of azadirachtin A and/or B. Currently, research is still being conducted to increase the stability of azadirachtin. Neem solutions lose effectiveness within about 8 h of being prepared and when exposed to direct sunlight. Neem is most effective in the evening, immediately after preparation, under humid conditions, and when plants and insects are moist [273]. Azadirachtin seems to act as a plant stimulant, which can lead to higher crop yields, but excessive concentrations of neem can cause plant leaf burn [274].

Apart from azadirachtin, another well-known botanical pesticide is pyrethrin. It is extracted from the dried flowers of the Dalmatian pyrethrum Tanacetum cinerariifolium (Asteraceae). Pyrethrins act as a modulator of voltage-gated sodium channels, which are required for proper electrical signals in the insect’s nervous system, causing a delay in the closing of sodium channels. As a result, excessive nervous stimulation, convulsions, paralysis, and the death of insects occur [275,276]. Pyrethrins may be used against many insects and mites, including aphids, thrips, whiteflies, leafhoppers, beetles, flies, the cabbage looper, and other moths [277]. Most studies also show consistently high levels of flea beetle suppression when using a pyrethrin-containing product [278,279]. The combination of azadirachtin and pyrethrin in Azera biopesticide at a rate of 2.34 L/h provides >75.0% control of green peach aphids, flea beetles, Mexican bean beetles Epilachna varivestis, the potato leafhopper Empoasca fabae, and cabbage worms [280]. Pyrethrins are quickly decomposed by sunlight, air, and moisture; therefore, they may require frequent use [281]. Some biopesticides with pyrethrin are listed in Table 3.

Rotenone is the most common natural product among rotenoids and is usually found in Derris sp. and Lonchocarpus sp. (Fabaceae) plants. It blocks nicotinamide adenine dinucleotide dehydrogenase (NADH), stopping the flow of electrons from NADH to coenzyme Q, thereby preventing the formation of ATP from NADH [282]. Rotenone can control mite pests, leaf-feeding beetles, caterpillars, and aphids on vegetables, fruit trees, and berries. The botanical pesticide rotenone can effectively control diamondback moths [283] and Colorado potato beetles [284]. According to Castagnoli et al. [285], rotenone was more toxic to the eggs than the females of two-spotted spider mites and was highly toxic to the predatory mite Neoseiulus californicus. Also, rotenone caused 59.5% mortality of T. papilionis, followed by cypermethrin (56.4% mortality) [286]. Rotenone is commercially available under different trade names but is not approved in the EU because it is toxic to humans, honeybees, animals, and aquatic life. It is also very toxic to fish and should not be used near water [287,288]. It persists for 3 to 5 days on the foliage after its application and is easily biodegradable, but scientists emphasize that for rotenone to be employed as a widely used biopesticide and substitute for synthetic pesticides, further studies should be conducted, in particular to determine the side effects of rotenone residues in vegetables and fruits on human neural cells, especially in connection with reports that they may affect the development of Parkinson’s disease [289].

Nicotine (along with pyrethrins and rotenone alkaloids) is a prominent example of first-generation botanical pesticides. Nicotine was originally isolated from Nicotiana tabacum (Solanaceae). It acts as an agonist of the acetylcholine receptor, leading to the influx of sodium ions and generating an action potential in the insect’s nerve cells [290]. Nicotine causes the overstimulation of cholinergic transmission and causes convulsions, paralysis, and the death of the insect [245]. Nicotine is a rapid nerve toxin and very effective in soft-bodied insects including aphids, thrips, whiteflies, leafhoppers, caterpillars, beetles, and mites [19]. In the case of the peach moth and peach twig borer Anarsia lineatella, the efficacy of tobacco extract reached as high as 98.3% and 99.0% [291]. In field trials on the effectiveness of tobacco extract in controlling the beet armyworm in shallot crops Allium ascalonicum, 22.5% and 30.0% larval mortality was found at concentrations of 30.0% and 60.0%, respectively [292]. Biopesticides containing nicotine are banned in the EU. Nicotine, like synthetic neonicotinoids, can harm pollinators by reducing survival and altering learning [245]. Also, garlic, Allium sativum (Amaryllidaceae), is a plant whose extract can be effective in the fight against pests. It can stimulate plant growth and has a repelling mode of action against pest insects [293]. The commercial preparation of garlic extract Bioczos BR effectively protected pea plants against pea leaf weevil. The damage to peas was about 18.0%, while in the unprotected control, it was 46.0% [294]. Garlic effectively reduced the severity and incidence of the diamondback moth on Chinese cabbage [295].

3.4.2. Essential Oils

Essential oils (EOs) are an alternative measure against plant pests. These are chemically complex mixtures of natural substances that the plant produces for its needs. They contain up to 150 different compounds. Among them, several of the most important groups are terpenes, alcohols, esters, phenols, and ethers [296]. The essential oils used most widely as biopesticides that have insecticidal/miticidal activity are thyme, mint, cinnamon, rosemary, orange, eucalypt, oregano, and clove oils [247]. The mode of action of some EOs is presented in Table 3 and depends on the main constituents present in the respective oil. Their toxic effects on caterpillars were demonstrated by Bathal et al. [297] and Larocque et al. [298], and their repellent properties on pests and their influence on reducing insect fertility were demonstrated by Pemoronge [299] and Marimuth et al. [300]. The tomato leafminer demonstrates increased sensitivity to lemongrass and mint oil, particularly in the larval stage [250,253]. In turn, citronella oil caused 100.0% mortality of cotton bollworm larvae after 120 h [252]. Good results were achieved using mixtures of extracts of chili pepper Capsicum annum with neem Azadirachta indica, orange Citrus sinensis peel with African curry Ocimum gratissimum leaf, or orange peel with beechwood Gmelina arborea to combat bean flower thrips Megalurothrips sjostedti in cowpea fields [301]. Orange oil (nanoemulsion) exhibited an aphicide effect on cotton aphids. At concentrations of 4.0% and 6.0%, the oil extracted from citrus fruits from the same orchard induced a mortality of over 90.0% in the aphid population [302]. Orange oil operates through a mechanical mode of action, desiccating the cuticles of mites and soft-bodied insects, leading to their sudden death by exposing them to a loss of body fluids. Significant results were obtained for the Mediterranean fruit fly with eucalyptus oil [255]. Thyme oil was effective against the carmine spider mite Tetranychus cinnabarinus [258]. Many studies involving essential oils have been conducted with aphids. Hemp oil extracted from Cannabis sativa effectively controlled rosy apple aphids on apple trees to such an extent that even at concentrations of 0.05% and 0.1%, its effectiveness was comparable to a pesticide containing acetamiprid. The strong repellent effect of rosemary Salvia rosmarinus oils on green peach aphids in field conditions has been proven by Hori [303]. However, the repellent effect of EOs on pests may also repel pollinators and be toxic to parasitic wasps [304]. The main problems associated with the effective use of EOs result from the fact that they are volatile, easily oxidizable, insoluble in water, and chemically unstable in the environment. Therefore, preparations containing essential oils as nanoparticles can be important in minimizing problems associated with their use [305]. Micro- and nanoencapsulation is currently used for EOs that are formed by different encapsulation techniques (emulsification, ionic gelation, and complex coacervation) [306]. Ibrahim et al. [252] compared two citronella essential oil (CEO) nanoencapsulation systems with a control without encapsulation to control the release of CEO for use against cotton leafworms. After two weeks, the CEO release from the nanosystems was 100.0% and 74.0%, resulting in the higher mortality of pest larvae, while 100.0% of the control sample was released after only 6 h. Also, horticultural oils are petroleum- or plant-based oils like cottonseed, palm, rapeseed, and natural soaps (saponins) that are often used in pest control [307]. Their mode of action is to disrupt the protective waxy covering of insects and mites, which leads to rapid water loss from the cuticle, and they block the air holes (spiracles) through which insects breathe, which leads to death by desiccation. In the EU, paraffin oil is used when fruit trees are in bud break (BBCH 54-56) but leaves have not yet appeared. This is a key time because the oil works on the wintering stages of pests such as spider mites, aphids, scale insects, and psyllids. The main limitation of spray oils is their potential to cause plant injury (phytotoxicity) in some situations [308].

3.5. Nanobiopesticides

In developing biological pesticides, it is essential to address issues such as improper formulation, low shelf life, slow pest control, high market costs, and other challenges related to marketing registration. Developments in nanotechnology have opened new perspectives for the production of controlled-release formulations (CRFs). These formulations bind the active ingredient to inert materials, which helps to protect the active compound and manage its release rate to the target site over a specified time and increase biopesticide activity [309,310]. Due to their small size and larger surface area, nanopesticides possess chemical properties that are significantly different from those of conventional pesticides. These unique properties can be utilized to develop efficient structural assemblies that offer several advantages, including improved interactions and modes of action. Nanosized products demonstrate higher selectivity while maintaining the bioactivity of the compound [311]. Additionally, their increased toxicity can enhance pest penetration [312]. The application of nanoparticles reduces drift and leaching issues, enabling the use of smaller amounts of active compounds per area, as long as the formulation maintains optimal concentrations for effective insecticide targeting over prolonged periods. Various methods exist for creating nanopesticide products, including nanocapsules, nanoemulsions, and inorganic engineered nanoparticles, such as metals, metal oxides, and clays. These methods can be further refined to enhance their effectiveness and reduce environmental toxicity [312].

Recent discoveries related to Bt and the processes of the encapsulation of Bt derivatives, such as pesticidal proteins (Cry), concern techniques such as extrusion, emulsion, spray drying, spray cooling, fluidized bed, lyophilization, coacervation, and electro-spraying to obtain micro- and nanoparticulate systems [311]. Tamez-Guerra et al. [313] tested the encapsulation of the spore-toxin of Bt, evaluating over 80 formulations of spray-dried microcapsules. In a field test, the microcapsules demonstrated enhanced residual insecticide activity in cabbage after 7 days against the young caterpillars of cabbage looper compared to commercial formulations. Promising results were also achieved in encapsulating baculoviruses isolated from the codling moth and the fall armyworm [314,315]. Also, several studies have reported using nanoformulations to encapsulate essential oils and plant-origin biopesticides [316,317]. Systematic risk assessment studies of the new nanobiopesticides are essential. Inhalation, ingestion, and dermal contact are the primary sources of nanoparticle exposure for humans and animals. This includes examining interactions with other organisms, the formation of toxic secondary metabolites, and the interspecific transfer of genetic material.

4. Conclusions

In summary, the current biological control techniques present promising solutions for integrated crop protection in fruits and vegetables. Biological control utilizes natural predators, parasitoids, pathogens, plant biopesticides, and semi-chemicals, offering environmentally friendly alternatives to chemical pesticides. This approach helps reduce pesticide residues in fruits and vegetables while preserving biodiversity and enhancing the stability of orchards and vegetable crops. By combining biological control with IPM practices and the judicious use of chemical insecticides, we can improve the overall effectiveness of pest control while minimizing risks. The regulatory framework should promote the safe and responsible use of biopesticides, ensuring that they meet safety and efficacy standards, thus also making it easier for farmers to use them. Biopesticides have emerged as a promising alternative to chemical pesticides, making it essential to maximize their use in agriculture. However, their shelf life is limited due to the specific temperatures and conditions required for transportation and storage. Therefore, additional research is needed to uncover the mechanisms that enhance the stability of biopesticides and extend their shelf life, which will significantly improve their effectiveness. It is also crucial to explore new biocarriers that can help increase the persistence of biopesticides in the environment. Furthermore, conducting studies on the compatibility of different biopesticides intended for use on the same crop is vital. Lastly, more emphasis should be placed on assessing the nutritional quality of plants treated with biopesticides. Looking to the future, the continued development and adoption of biological control methods hold great potential for advancing sustainable agriculture and ensuring food security. The strategy to increase the use of biopesticides in IPM also requires increased resources for education and the dissemination of proven, ready-to-use biological control options for specific crops.