Integrated Pest Management Strategies for Controlling Phthorimaea (Tuta) absoluta: Advances in Biological, Pheromone, and Cultural Control Methods

Simple Summary

The tomato leaf miner, Phthorimaea (Tuta) absoluta Meyrick 1917, is a significant pest that affects tomato crops globally. Effective control of this pest typically involves a combination of integrated pest management (IPM) strategies, including the use of natural predators, sex pheromone traps, and crop rotation practices, and their combined application tends to yield significant results. Recent research highlights the potential for enhancing these traditional approaches through the incorporation of novel technologies, such as genetic control techniques, to achieve more sustainable and environmentally friendly pest management solutions.

Abstract

The tomato leaf miner, Phthorimaea (Tuta) absoluta, Meyrick 1917 is recognized as a highly destructive pest, causing significant economic losses to crops in both greenhouse and open field environments across four continents: Asia, Africa, Europe, and South America. High genetic homogeneity among populations from various regions and countries indicates significant gene flow between P. absoluta populations, suggesting a lack of geographical barriers to dispersion. Furthermore, P. absoluta has developed resistance to insecticides due to target-site mutations or metabolic resistance, which enable the insect to withstand lethal doses of insecticides. To control this insect pest, the plant-mediated RNA interference (RNAi) is most promising host-induced gene silencing technique, utilized the plant’s machinery to express double-stranded (dsRNA), which triggers the RNAi pathway in P. absoluta. Due to thermal tolerance, the P. absoluta has increased its area of invasion by 600 km per year over 9 years. Female P. absoluta releases pheromones that are recognized by males with a sophisticated olfactory circuit on their antenna. Pheromone binding proteins (PBPs) play a crucial role in mate recognition and attraction, and their expression peaks during courtship, specifically around 6:00 a.m. Given its potential to significantly alter the insect genome, clustered regularly interspaced short palindromic repeats (CRISPR) and CRISPR-associated protein 9 (Cas9) offer a revolutionary strategy to control P. absoluta. Furthermore, this pest has developed remarkable adaptations to survive on unfavorable hosts by secreting specific proteins from its salivary glands that detoxify plant defenses. Insecticide resistance is likely the cause of field control failures of P. absoluta. Biological control, sex pheromone traps, and cultural control are the most promising approaches to address insecticide resistance resulting from these failures. Therefore, the implementation of integrated control programs and appropriate resistance management strategies is necessary to keep P. absoluta infestations under economic damage thresholds.

1. Introduction

The tomato leaf miner, Phthorimaea (Tuta) absoluta (Meyrick, 1917), is a major pest affecting solanaceous crops, particularly tomatoes, and has become a global threat due to its rapid spread and high reproductive potential [1]. Native to South America, P. absoluta has expanded its range to regions including Europe, Africa, and Asia, causing severe economic losses in tomato production [2]. Its high reproductive potential, wide host range, and strong adaptability enable severe infestations, often causing yield losses in both greenhouse and open-field systems, making it a major concern for global food security and agricultural sustainability [3,4,5,6,7]. Implanting effective and efficient management strategies to control insect pest outbreaks is a significant challenge, as it requires a comprehensive understanding of the pest’s biology and ecology [8]. For over a decade, population genetics has traced insect pest histories and the role of genetic variation in their success [9,10]. A key strategy in managing pest outbreaks is reconstructing their spread to prevent further migration. For example, Drosophila suzukii, discovered in 2008, rapidly spread across the USA, emphasizing the need for early detection and management [11]. Moreover, genetic variation within insect pest populations is critical driver of their success, rapid spread, and adaptation to environmental stressors [12].

The ecological success of P. absoluta is supported by multiple interacting biological and environmental factors [7,13,14,15]. Its reproduction relies on sophisticated pheromone-mediated communication [16], while its broad host range enhances survival and spread.

For the development of a sustainable pest management tool, it is essential to identify the movement pathways of specific insect pest species to reduce the likelihood of their introduction into new environments [17]. One promising strategy for controlling P. absoluta is plant-mediated RNA interference (RNAi), a biotechnological approach designed to target specific genes in pests, disrupting their development and reducing damage [18]. Despite its potential, RNAi faces significant challenges which are discussed in this review article. Compounding these challenges is the widespread insecticide resistance seen in P. absoluta populations, particularly mechanisms involving target-site mutations and metabolic detoxification processes [19,20]. The spread of resistance across countries has led to a variety of country-specific resistance mechanisms, making the management of this pest even more difficult. To address these challenges, integrated pest management (IPM) strategies combining biological, pheromone, and cultural control methods are essential.

This review examines the ecological and genetic factors contributing to the spread and resistance patterns of P. absoluta. It highlights the importance of understanding the pest’s genetic diversity, its rapid expansion, and the evolving resistance to insecticides. The review also discusses the role of plant-mediated RNAi as a potential biotechnological solution, outlining its current status, and limitations, in the sustainable management of P. absoluta.

2. Review Methodology

A comprehensive literature search was performed running a query comprising keywords and Booleans: (“Tuta absoluta” OR “Phthorimaea absoluta”) AND (“insecticide resistance” OR “integrated pest management” OR “CRISPR/Cas system” OR “genetic variation”) across multiple databases, e.g., Google Scholar, PubMed, and Science Direct. The pee-reviewed article published between 2000 and 20 March 2026 were retrieved. A wide range of retrieved articles underwent a systematic selection process in line with PRISMA guidelines [21]. A total of 2131 records were retrieved from all databases, and those remained in 1791 after the exclusion of duplicates. The initial screening, based on titles and abstracts, resulted in the remaining 840 articles. Moreover, 592 records, including conference proceedings and studies with irrelevant titles and abstracts, were found short of the eligibility criteria, and 248 records were used to extract information for this review (Figure 1). Clustering and co-occurrence of keywords in the selected articles were analyzed using VOSviewer (version 1.6.19), as depicted in Figure 2. A total of 93 numbers with five distinct clusters of keywords showing most frequently, integrated pest management, biological control, Tuta absoluta, insecticide resistance, and CRISPR/Cas9 among all. Further bibliometric parameters included the number of publications in respective years. About 54% of the selected retrieved articles were published between 2020 and 2026, indicative of the research advancement in the prospect of the topic (Figure 3). The information gathered from the selected literature focused on the ecological, genetic, and resistance patterns of P. absoluta, as well as the mechanisms contributing to its rapid spread and resistance to insecticides. Additionally, the review examined the potential of plant-mediated RNA interference (RNAi) as a biotechnological solution, highlighting its current applications, limitations and future prospects in pest management. The illustrations used in this review article were created with BioRender (https://app.biorender.com).

3. Genetic Diversity and Resistance Patterns Across Geographic Populations

3.1. Taxonomy

The tomato leaf miner, Phthorimaea (Tuta) absoluta, Meyrick 1917 belongs to the order Lepidoptera (Family: Gelechiidae) and is native to South America [22]. As a potential insect pest of tomato, P. absoluta was reported for the first time in Argentina, Bolivia, Brazil, Chile, Colombia, Peru, Paraguay, and Uruguay [23,24]. In Eastern Spain, it was identified in 2006 [25], and it was first discovered in Africa in 2008 [26,27]. Then it invaded Europe, the Middle East, South Asia (India), and north, east, and West Africa [28,29,30,31,32]. The presence of P. absoluta was first detected in North Africa in Tunisia and Morocco in 2008 [33,34]. In West Africa, it was identified in Niger and Nigeria in 2010 [35], and later in Senegal in 2012 [36]. In East Africa, the pest was reported in Sudan (2010) [37] and Ethiopia in 2012 [38], followed by Kenya (2014) [39], Tanzania (2014) [40], and Uganda in 2015 [26]. In Southern Africa, P. absoluta was confirmed in Zambia [41] and South Africa in 2016 [41]. After this, it was discovered in the Kathmandu Valley in 2016 and spread to the nearest districts, including Kavrepalanchowk, Dhading, and Nuwakot [42]. Pandey, Bhattarai [7] reported that in Nepal, P. absoluta is recognized as a highly destructive pest that can cause up to 100% loss in a commercial tomato (Solanum lycopersicum Linnaeus, 1753) farm in Kathmandu. In addition, tomato, P. absoluta infests many other Solanaceous plants, such as potato (Solanum tuberosum L.), eggplant (Solanum melongena Linnaeus, 1753), pepino (Solanum muricatum Aiton, 1789), and African nightshade (Solanum nigrum Linnaeus, 1753) [43,44,45].

P. absoluta is recognized as a highly destructive pest that imposes significant economic losses on tomato. In both greenhouse and open-field environments, unchecked infestations of P. absoluta can result in yield reductions of 80–100% [46]. Accurate classification enables the precise identification of insect pests, which is crucial for developing targeted, eco-friendly control measures and minimizing economic losses in agriculture [47]. The classification of T. absoluta has been problematic, with this pest originally placed in the genus Phthorimaea Meyrick, 1902, a “catch-all genus for similar species. The boundaries of the tribe Gnorimoscheminis, to which T. absoluta belongs, have been unstable, leading to confusion in its classification [48]. Corro and Metz [48] constructed a phylogenetic tree using 22 morphological characters from species within the genera Phthorimaea, Scrobipalpuloides, and Tuta, resulting in a single, most parsimonious tree that groups T. absoluta with Phthorimaea operculella Zeller, 1873, and confirms the validity of the genera Tuta and Scrobipalpuloides within the tribe. Furthermore, T. absoluta should be reinstated under the genus Phthorimaea, with a new combination proposed for Phthorimaea chiquitella Busck 1910. Therefore, Corro and Metz [48] resolved the long-standing taxonomic uncertainty around T. absoluta by using a rigorous cladistics approach ultimately enhances pest control efforts.

3.2. Detection of Genetic Variation

Genetic variability in insect plays a significant role in the success, spread, and adaptation of insect pests [49]. In Tunisia, P. absoluta specimens were collected from infested tomato leaves across the northern, central, and southern regions. The study revealed low genetic diversity within pest populations in the selected regions, attributed to the founder effect, subsequent population expansion, and significant gene flow between populations. These factors have contributed to the genetic homogenization of P. absoluta across the country. Although various haplotypes were observed in some markers, the overall genetic variation remains markedly low [50]. Li, Fu [51] explored the broader understanding of invasive P. absoluta adaptation to new environments and spread across different regions of China with varying levels of genetic diversity. The larvae were collected from tomato fields in Xinjiang and Yunnan, China, and results indicated that the complete mitogenome of P. absoluta is 15,298 bp for the individual from Xinjiang and 15,296 bp for the individual from Yunnan, both of which are longer than the reported mitogenome from Spanish population (15,290 bp). However, higher genetic diversity, as measured by mitochondrial markers, cytochrome c oxidase subunit 2 (cox2), ATP synthase subunit 6 (atp6), NADH dehydrogenase subunit 1 (nad1), and NADH dehydrogenase subunit 5 (nad5), was observed in the Yunnan population compared to the Xinjiang population. Furthermore, using the mitochondrial cytochrome oxidase I (mtCOI) marker, high genetic homogeneity among the endosymbionts of P. absoluta populations collected from Iran and Turkey was observed, revealing a 100% prevalence of Pantoea and Wolbachia in these populations [52]. Javal, Ndiaye [53] investigated the genetic structure of P. absoluta populations in Africa. Results indicate that the African population shows high genetic homogeneity. Furthermore, P. absoluta in Africa likely originated from a small number of introduction events or from multiple introductions from genetically similar source populations rather than from numerous diverse sources. Wang, Tian [54] revealed a new invasion of P. absoluta into Gansu and Inner Mongolia, indicating the ongoing expansion of this pest. Additionally, the authors used the biological markers mtCOI and mitochondrial cytochrome oxidase I (mtCOII) and found high genetic homogeneity in the P. absoluta population both in China and worldwide. However, some genetic variability was observed in southern China, especially in Yunnan.

3.3. Resistance Patterns Across Geographic Populations

Understanding resistance patterns across different geographic populations of P. absoluta is crucial for designing effective and sustainable pest management programs. In this context, Zibaee, Mahmood [55] investigated organophosphate and pyrethroid resistance in P. absoluta from Iran. In P. absoluta, resistance to organophosphates arises from the A201S mutation in the ace1 gene, which results in an alteration in the structure of the acetylcholinesterase enzyme. Furthermore, substitution of alanine with serine alters the enzyme’s active site, causing a reduction in the binding affinity of organophosphates to acetylcholinesterase. The pyrethroid resistance in P. absoluta involves mutations in the sodium channel (kdr) genes, including L1014F, M918T, and T9291, which alter the channel’s structure and ultimately prevent the insecticide from binding to its target site. Haddi, Berger [56] identified three kdr/super-kdr mutations (M918T, T929I, and L1014F) in the para gene, specifically in the IIS4-IIS6 region of the sodium channel in P. absoluta, that confer resistance to pyrethroid insecticides such as lambda-cyhalothrin and tau-fluvalinate. Haddi, Berger [57] also collected strains from Brazil and Europe and identified a mutation in the ace1 gene of P. absoluta associated with organophosphate resistance, in which alanine at position 201 is replaced by serine. Therefore, this results in reduced sensitivity of the acetylcholinesterase enzyme to chlorpyrifos. Metabolic enzymes, such as glutathione S-transferases (GSTs) and esterases (ESTs), play a crucial role in the resistance mechanisms of P. absoluta. GSTs bind insecticides and catalyze their conjugation with glutathione, thereby neutralizing them and reducing their toxicity to P. absoluta. Furthermore, EST activity in this insect is increased when exposed to insecticides containing ester bonds, facilitating their hydrolysis and subsequent detoxification, thereby reducing their toxicity [58,59].

The resistance in P. absoluta is also associated with intensive pesticide use. In this context, Lewald, Tabuloc [60] conducted whole-genome sequencing on individuals from three distinct geographic regions of Latin America (Andes, Central, and North clusters). Results indicated that the Andes population showed resistance to pyrethroid, which are commonly used in this region. The P. absoluta population showed increased allele frequencies at resistance loci, particularly at the sodium channel gene. Furthermore, the overexpression of GST, EST, and cytochrome P450 (CYP450) enzymes in the Andes population has become a significant factor in pyrethroid resistance. Whereas the central and north P. absoluta populations exhibited lower levels of resistance than the Andes cluster due to less intensive pesticide use in those areas. Moreover, the identification of resistance-related loci in these insects that show signatures of positive selection indicates that insecticide use continues to exert selection pressure on these populations. Authors also found less pronounced changes in detoxifying enzyme activity in the insect populations of the central and north clusters.

4. Dynamics of Phthorimaea (Tuta) absoluta Spread in Invaded Areas

For the development of a sustainable pest management tool, it is essential to identify the movement pathways of specific pest species to reduce the likelihood of their introduction into new environments [61,62]. Central Chile is the sole source of P. absoluta introduction into Europe, as revealed by genetic markers [63]. Between the 1960s and 1980s, this pest spread from its native range in the Peruvian central highlands to the Latin American regions, including Argentina, Bolivia, Brazil, Chile, Colombia, Ecuador, Panama, Paraguay, Peru, Uruguay, and Venezuela [25].

Table 1. Geographic distribution timeline of Phthorimaea (Tuta) absoluta worldwide.

Region/Continent	Country/Area	Year of First Report	Probable Route of Spread	Major Host Crops Affected	Current Status	References
Africa	Algeria	2008	Trading of tomato fruits	Tomato (S. olanum lycopersicum)	Present	[70]
	Morocco	2008	Trading of tomato fruits	Tomato (S. lycopersicum)	Present	[71]
Asia	Israel	2009	Trading of tomato fruits	Tomato (S. lycopersicum)	Present	[72,73]
	India	2009	Trade, agriculture imports	Tomato (S. lycopersicum)	Expanding	[74]
	Tajikistan	2018	Likely through trade, spread via tomato seedlings	Tomato (S. lycopersicum), Potato (Solanum tuberosum), Sweet pepper (Capsicum annuum)	Established, causing severe damage to tomatoes	[75]
Europe	Spain	2006	Trading of tomato fruits	Tomato (S. lycopersicum)	Rapid spread across Mediterranean	[76]
	France (Including Corsica)	2008	Trading of tomato fruits	Tomato (S. lycopersicum), Eggplant (Solanum melongena)	Established populations	[77]
	Italy (Including Sicily and Sardinia)	2008	Trading of tomato fruits	Tomato (S. lycopersicum), Potato (Solanum tuberosum), Eggplant (S. melongena)	Widely spread	[78]
	Albania	2008	Trading of tomato fruits	Tomato (S. lycopersicum)	Present	[77]
	Bulgaria	2009	Trading of tomato fruits	Tomato (S. lycopersicum)	Present	[72]
	Greece	2009	Trading of tomato fruits	Tomato (S. lycopersicum)	Present	[79]
	Russia	2010	Trading of tomato fruits	Tomato (S. lycopersicum)	Present	[80]
Middle East	Tunisia	2009	Spread via imports	Tomato (S. lycopersicum)	Endemic	[77]
	Saudi Arabia	2010	Trading of tomato fruits	Tomato (S. lycopersicum)	Present	[81]
	Iran	2016	Likely via trade from Mediterranean regions	Tomato (S. lycopersicum)	Established	[82]
South Asia	Pakistan (Punjab)	2018	Likely through trade, spread via tomato seedlings	Tomato (S. lycopersicum)	Established in Charsadda; spreading in Rawalpindi	[82]
	Pakistan (Khyber Pakhtunkhwa)	2019	Likely via trade, urban-to-urban movement	Tomato (S. lycopersicum), Potato (S. tuberosum)	Spread in Charsadda, spreading across Khyber Pakhtunkhwa	[82]
Sub-Saharan Africa	Ghana	2017	Likely through imports	Tomato (S. lycopersicum)	Present	[83]
West Africa	Côte d’Ivoire (nationwide: North, South, East, West, Center regions)	2016	Likely regional spread via trade and/or natural dispersal from neighboring countries (e.g., Senegal, Ghana, Burkina Faso, Mali)	Tomato (S. lycopersicum); eggplant (S. melongena), black nightshade (Solanum nigrum), pepper (Capsicum annuum)	Fully established and widely distributed across all surveyed regions with high infestation levels	[84]

summarized the geographic distribution timeline of P. absoluta across various regions. Roques, Auger-Rozenberg Roques, Auger-Rozenberg [62] reported that after invading Europe, P. absoluta increased its area of invasion by 600 km per year over 9 years. Currently, in China, many scientists have reported its invasion in Yunnan on Solanum indicum (Linnaeus, 1753) [64], in Xinjiang on S. melongena, S. tuberosum, and S. nigrum [65]. The female P. absoluta prefers to oviposit on leaves, and after hatching, neonates penetrate various plant parts, creating distinctive galls and galleries [66]. In tomato leaves, mining within the mesophyll reduces photosynthetic capacity, thereby decreasing productivity, which may cause necrosis due to disrupting overall plant development [67]. Additionally, galleries within fruits can facilitate the invasion of secondary pathogens, leading to fruit rot [68,69].

Factors Influence Phthorimaea (Tuta) absoluta Invasion

The P. absoluta invasion is strongly influenced by abiotic factors, which shape its population dynamics and spread [15]. Temperature is the primary abiotic factor that acts as an ecological filter, determining whether the pest can establish itself in a new environment [85]. In this context, Machekano, Mutamiswa [15] performed a thermal tolerance assay on adults and larvae of P. absoluta. Results indicated that larvae were more heat-tolerant, with a higher critical thermal maximum (CTmax) than adults (p < 0.01). In contrast, the adults were more tolerant of cold, with a significantly lower (p < 0.001) critical thermal minimum (CTmin) than larvae. Larvae and adults differ in their temperature tolerance, reflecting the different physiological needs and adaptations of each. The P. absoluta larvae maintain elevated expression levels of heat shock proteins (HSPs), which function as molecular chaperones to prevent protein denaturation and aggregation under heat stress, thereby protecting the cell from damage [86]. In addition to larvae, pupae of P. absoluta are also susceptible to fluctuations in environmental temperature. When the pupae were exposed to a constant temperature of 11 °C for thirty days, 47% of the pupae emerged. However, when the temperature was lowered to 10 °C for sixty days, the emergence rate decreased significantly to just 12%. Furthermore, no adult emergence was observed when the pupae were subjected to an even lower temperature of 5 °C [87]. Additionally, rainfall directly influences mortality rates in P. absoluta in such a way that excessive moisture can disrupt the pest’s life cycle by delaying mating and oviposition [88]. Regarding biotic factors, the spread of P. absoluta is facilitated by the availability of wild and cultivated Solanaceous plants, which serve as its hosts. In Botswana, wild hosts such as Solanum coccineum (Linnaeus, 1753), Solanum supinum (Jacquin, 1760), and Solanum aculeatissimum (Jacquin, 1760) have been identified as crucial dispersal drivers for this insect pest [15].

5. Ecology

5.1. Mate Attraction

Mate attraction in insects is a core part of their ecology, involving complex sensory communication to find, assess, and choose mates [89,90,91]. The odorant-binding proteins play a crucial role in the insect olfactory system, which is essential for odor discrimination [92]. The insect odorant-binding proteins (OBPs) are small, amphipathic, water-soluble, globular proteins containing about one hundred and fifty amino acids and made up of six alpha-helical domains that interact with each other by disulfide bridges [93,94]. The female P. absoluta releases a volatilized, hydrophobic pheromone molecule, (3E, 8Z, 11Z)-tetradecatrien-1-yl acetate (TDTA), which enters the male’s antenna through microscopic pores in its cuticle, reaching the sensillar lymph [92]. Within this lymph, the Tuta absoluta pheromone-binding protein 2 (TabsPBP2) and Tuta absoluta pheromone-binding protein 3 (TabsPBP3), specific subgroups of the larger OBP family, act as carriers. They solubilize and transport the TDTA to olfactory receptors (ORs) located on the membranes of receptor neurons [92,95]. The TabsPBP3 protein, in particular, has a hydrophobic cavity consisting of key residues, including Phe37, Tyr61, Ile77, Leu84, Ile86, Leu87, Phe101, Ala136, Ile139, and Ala140, which facilitate the binding of TDTA. The PBP-pheromone complex interacts with specific ORs and a co-receptor, Orco, triggering receptor activation. This activation sends an electrical signal through the axon to the antennal lobe in the brain and ultimately causes the male to orient toward the female [96] (Figure 4). Ou, Li [92] revealed that the TabsPBP3 expression peaks during courtship, specifically around 6:00 a.m., aligning with the timing of mating activity in the field. Furthermore, the TabsPBP3 is also highly expressed in the female pheromone gland ovipositor and may play a role in regulating adult mating behavior. The thirty-three OBP genes are also identified in the male antennae of P. absoluta, including Tuta absoluta general odorant-binding protein 1 (TabsGOBP1), Tuta absoluta general odorant-binding protein 2 (TabsGOBP2), Tuta absoluta pheromone-binding protein 1a (TabsPBP1a), Tuta absoluta pheromone-binding protein 1b (TabsPBP1b), and Tuta absoluta pheromone-binding protein 1c (TabsPBP1c) [92]. However, the clustered regularly interspaced short palindromic repeats (CRISPR) and CRISPR-associated protein 9 (Cas9) represent the most promising tools for knocking out the TabsPBP2, and TabsPBP2 genes in P. absoluta, thereby impairing the perception of sex pheromone TDTA. The female T. absoluta is also capable of auto-detecting its own pheromone, TDTA, which is weaker than that perceived by the males [97]. Moreover, the virgin females showed stronger responses than the mated females [97]. The mate choice is a fundamental behavior of insects in which individuals prefer mates that exhibit characteristics of higher reproductive quality [98]. The female P. absoluta prefer young, virgin, and heavy weight males for enhancing their longevity and reproductive performance [98]. Because young, virgin and heavier males produce larger and more nutrient-rich spermatophores during mating [99]. These nutrients contribute to the female’s health, increasing her longevity and reproductive performance [100,101,102].

Currently, the chemical industry is currently focused on producing synthetic pheromone lures that emit pheromones consistently and over extended periods [103]. Chermiti and Abbes [104] performed an experimental trial of installing thirty-two traps per hectare in a five-hectare field of open-field tomato crops in Kairouan city of Tunis. Results indicated that the “superdosed” TUA-Optima^® pheromone lures, containing 0.8 mg of synthetic pheromone, were more attractive to males of P. absoluta compared to the standard pheromone (0.5 mg), and are recommended for use in areas with high populations of P. absoluta. In Khyber Pakhtunkhwa province of Pakistan, Sadique, Sadique, Ishtiaq [105] conducted a study for two consecutive years (2020–2021) to compare the efficiency of pheromone-based traps and sticky pads in capturing male P. absoluta adults. The results indicated that delta traps with rubber septum pheromone lures, containing a mixture of (3E,8Z,11Z)-3,8,11-tetradecatrienyl acetate and (3E,8Z)-3,8-tetradecadienyl acetate in a 90:10 ratio, along with black sticky pads, together offer the most effective method for managing P. absoluta. In the United Arab Emirates, Sabbahi and Azzaoui [106] also revealed the higher efficiency of sticky traps with a mean number of P. absoluta adults (70.44 ± 4.57 captures/trap/week), compared to delta traps (55.94 ± 4.77 captures/trap/week) and water pan traps (18.63 ± 1.49 captures/trap/week).

CRISPR/Cas9 offers important practical advantages for next-generation pest management because this technology enables more targeted and species-focused control than conventional broad-spectrum pesticides [107]. CRISPR/Cas9 allows precise genome modification that can be used either to suppress pest traits or to improve beneficial insects used in biological control [108]. Furthermore, this tool may strengthen integrated pest management by improving efficacy, reducing reliance on chemical pesticides, and potentially lowering unintended impacts through better target specificity [109,110,111]. Their practical promise is therefore substantial, especially for the future development of sustainable and biologically informed pest-control systems [108].

Despite these advantages, CRISPR/Cas9 still faces major practical limitations that restrict their field deployment. CRISPR/Cas9 faces operational barriers, including transformation inefficiency, the need to optimize editing systems separately for each species, challenges in identifying suitable target genes, and the mass-rearing constraints associated with approaches such as the precision-guided sterile insect technique [112,113,114]. CRISPR/Cas9 requires careful biosafety assessment focused on off-target effects, environmental persistence, non-target exposure, migration risks, and possible ecological disruption [115,116,117,118,119,120]. Furthermore, this technique faces significant limitations such as repeated species-level optimization, specialized delivery systems, transformation efficiency challenges, mass-rearing needs, and regulatory testing that may increase implementation costs and delay large-scale adoption [108].

5.2. Host Range

Studying the host range of P. absoluta infestation is critical for developing effective agricultural pest management strategies and preventing significant economic losses [43]. In fifteen randomly selected villages in four leading tomato-producing districts, such as Arumeru, Kilolo, Lushoto, and Mvomero, the solanaceous crops and wild plants of Tanzania were observed for P. absoluta infestation. Results indicated that in the tomato field, mine density ranged from 0.1 to 4.4 mines per leaf, and the percentage of fruits damaged by P. absoluta ranged from 0 to 41%. Whereas, in eggplant fields, the mine density was 0 to 2.7 mines per leaf, but fruits were not affected by P. absoluta. In potato and African nightshade, the mine density ranges from 0 to 0.3 and 0 to 0.08 mines per leaf, respectively [43]. Archives and Blog [121] also revealed that the tomato and African nightshade are identified as the most suitable plants for P. absoluta invasion. Host plant selection affects the biological parameters in insect pests [122]. In this context, Negi, Sharma [123] observed that, under controlled laboratory conditions (25  ±  0.5 °C temperature, 70  ±  5% relative humidity and 12 h light: 12 h dark photoperiod), P. absoluta exhibited the most rapid growth on tomato leaves, with the slowest growth occurring on potato leaves. Population growth parameters, doubling time, weekly multiplication rate, intrinsic rate of increase, and net reproductive rate were highest in tomato leaves. These findings suggest that tomato is the primary and most suitable host of P. absoluta. A recent study by Li, Cai [124] indicated the poor adaptability of P. absoluta to tobacco (Nicotiana tabacum, Linnaeus, 1753) in terms of its growth and reproduction, compared to tomato. Furthermore, when fed on tobacco leaves, the salivary glands of P. absoluta larvae secrete certain proteins, such as trypsin, B5 V51-1498, and Ta74, that could facilitate the insect to adapt to the less favorable host by enhancing its ability to process or neutralize the plant defense, thus enabling it to survive and feed.

5.3. Multivoltinism

P. absoluta is currently considered a key limiting phytosanitary factor affecting the global Solanaceous crop value chain due to multivoltinism [3,125]. Multivoltinism in P. absoluta is regulated by thermal accumulation, and this pest requires 799.1 accumulated degree-days above a developmental threshold of 5.268 °C to complete one full generation [126]. These thermal requirements were subsequently applied to climatic data from different regions of Egypt to predict the annual number of generations. In warmer regions of Egypt, such as Qena, the highest predicted voltinism was exhibited, with approximately 9.52 generations per year. In contrast, Giza showed an intermediate value of approximately 8.05 generations per year, while the cooler region of Mersa-Matrouh recorded the lowest values, with nearly 7 generations per year [126]. This temperature-driven generational turnover of P. absoluta can be used to improve timely pest management.

5.4. Life Cycle

The insect life cycle is a key ecological factor that is significantly influenced by metamorphosis [127]. Metamorphosis is a primary driver of insect success and ecological diversity, allowing species to adapt to different environments and reduce resource competition throughout their lives [127]. P. absoluta undergoes complete metamorphosis and exhibits distinct life stages with unique morphological and behavioral characteristics [46,69]. The larvae is the most dangerous stage that usually affects plants leaves and also found in fruits and stems where they feed and develop, creating conspicuous mines and galleries [128]. To reduce the P. absoluta infestation, modeling plays a crucial role in predicting the population dynamics of this pest based on environmental parameters, thereby facilitating the development of effective management strategies [129,130]. Furthermore, the Von Foerster-based age-structured population model successfully reproduced stage-specific dynamics of P. absoluta, showing that eggs hatch within 4–5 days, the larval stage (comprising four instars) is the longest (approximately 20 days; about 0–70% of the life cycle), followed by a pupal stage of 4–7 days, leading to a complete life cycle of approximately 30 days [131]. Stimulation results further demonstrated that temperature strongly regulates the duration and transitions between life stages, enabling accurate prediction of peak larval abundance and allowing farmers to plan timely and efficient environmentally friendly control strategies [131].

5.5. Seasonal Population Dynamics

Seasonal population dynamics are a core component of population ecology because they reveal the timing and progression of pest generations during the crop season, enabling timely, efficient, and environmentally sound pest management [132]. The seasonal dynamics of P. absoluta are governed by the combined influence of tomato crop phenology, climatic conditions and insecticide application [133]. Infestation was highest during the fruiting stage and under warm, low-rainfall conditions, while insecticides reduced but did not fully suppress pest populations [133]. Salama, Ammar [134] also observed the seasonal fluctuations in the population of P. absoluta in the fields of Giza, Egypt. They found that weather variables, particularly temperature and relative humidity, are the most important drivers of pest abundance. In Beni Suef Governorate, Egypt, the seasonal peaks in P. absoluta populations were closely aligned with the activity of parasitoids such as Bracon sp., Pteromalus sp., and Eulophus sp., suggesting that these parasitoids respond to increasing pest densities and may play a crucial role in naturally suppressing P. absoluta populations.

5.6. Endosymbiont Interactions

Endosymbionts play a crucial role in the survival of insect pests, making them one of the most challenging factors in integrated pest management [135,136]. These microorganisms, which live within the insects, contribute to their fitness, nutritional needs, and resistance to environmental stressors, including insecticides [137,138,139,140]. Resultantly, the presence of endosymbionts in pest species complicates efforts to control their populations effectively within integrated pest management strategies [141]. It is difficult to define a core microbiota for a diverse group of Lepidoptera as an order [142]. Paniagua Voirol, Frago [143] compared the gut microbiomes of thirty lepidopteran species and found that Bacillaceae, Enterococcaceae, Enterobacteriaceae, Pseudomonadaceae, Staphylococcaceae were the most prevalent families, while Bacillus, Enterobacter, Enterococcus, Pseudomonas, Staphylococcus were the most common genera. In P. absoluta, symbionts such as Acinetobacter, Enterobacter, Pseudomonas, Staphylococcus, and Wolbachia were found in the eggs, guts, salivary glands, ovary, fat body and Malpighian tubules of this insect pest, along with some unique species like Bacillus subtilis and Serratia marcescens [144]. The specific gut bacteria Enterobacter cloacae, Enterococcus gallinarum and Staphylococcus gallinarum found in P. absoluta are essential for enhancing the adaptability of this pest to different hosts [145]. These bacteria facilitate the breakdown of plant toxins and secondary metabolites by producing enzymes like hydrolases and oxidases. These enzymes detoxify harmful compounds, enabling the insect to efficiently utilize nutrients and enhance its growth and reproduction [146]. The presence of E. cloacae enhances the pest’s preference and adaptation to tomatoes, while S. gallinarum and E. gallinarum assist in adapting to potato plants [145]. Moreover, these insect endosymbionts also produce enzymes such as CYP450s and GSTs that detoxify insecticides and reduce absorption. They also enhance the insect’s own detoxification pathways, promoting efficient toxin metabolism and excretion [147,148], ultimately enhancing insect pest fitness. Insects with disrupted or altered symbiotic relationships often experience reduced survival rates, making them more vulnerable to both natural enemies and environmental stressors [135]. Modern techniques like CRISPR/Cas9 and RNA interference (RNAi) allow for the targeted manipulation of these symbiotic microbes, leading to an increase in pest mortality [135]. Elston, Leonard [149] also declared that engineered symbionts can be used to manipulate insect biology and population dynamics, offering a promising, sustainable pest-control approach. Therefore, CRISPR/Cas9 and RNA interference (RNAi) can be used to edit the microbiome by targeting specific genes in gut microbes of P. absoluta, either silencing gene expression or eliminating bacteria, ultimately controlling this insect pest.

6. Factors Influencing the Spread of Phthorimaea (Tuta) absoluta: Climatic and Human-Mediated Factors

Climate change is projected to significantly expand the global suitability for P. absoluta [150]. Gao, Feng [151] indicated that the global potential climatic suitability area for P. absoluta is approximately 4.80 × 10⁷ km², which accounts for 35.29% of the earth’s land area, excluding Antarctica. Furthermore, over one-third of the world’s land area offers suitable conditions for the establishment and spread of P. absoluta. These areas are predominantly found in Africa, Asia, the Americas, and Europe, which have climates favorable to the pest’s growth, development, and reproduction. The extremely high temperatures negatively affect P. absoluta. Specifically, temperature around 33 °C significantly reduces the survival of the pest, as high heat stress decreases its reproduction and survival while increasing mortality [152]. Furthermore, areas around the equator, where annual average temperatures are close to 30 °C, may become unsuitable for P. absoluta by 2050 and 2100 due to projected temperature increases of approximately 2.11 °C [151]. This increase in temperature is expected to exacerbate hot-wet stress, further limiting the pest’s development in these regions. Guimapi, Srinivasan [153] revealed that this pest spread much faster in Asia than predicted by the stimulation model, which estimated a 20-year invasion period, but the pest reached Southeast Asia in just 10 years. The rapid spread was largely driven by international crop trade and human movement, rather than just natural flight ability. Additionally, the favorable climatic conditions support the pest’s establishment in many regions. P. absoluta has rapidly expanded across China, primarily through two dispersal corridors originating in Xinjiang and Yunnan, with human-mediated transport, such as the movement of infested tomato plants, significantly accelerating its spread [154]. This expansion is coupled with a substantial shift in the pest’s climatic niche, allowing it to adapt to a broader range of temperature and precipitation conditions. The pest’s physiological adaptations, such as enhanced cold tolerance and increased supercooling capacity, enable it to thrive in colder regions of China that were previously climatically unsuitable [154]. Furthermore, the widespread use of irrigation creates artificial microclimates, which buffer against environmental extremes [155], supporting its survival in arid and temperate regions [3,15]. This combination of biological adaptability and anthropogenic modifications has allowed P. absoluta to colonize a wider range of agroecosystems compared to other regions. These findings underscore the need for enhanced biosecurity measures to manage its spread.

7. Insecticide Resistance in Phthorimaea (Tuta) absoluta

Insecticide resistance is likely the cause of field control failures of P. absoluta [156]. In Kenya, the P. absoluta populations exhibited high frequencies of resistance genes such as kdr and ace-1 mutations [157]. The kdr mutation is caused by point mutations in the voltage-gated sodium channel (VGSC) gene, specifically in the S6 transmembrane region of domain II of the VGSC protein. The most common mutation is a leucine to phenylalanine substitution (L1014F), which alters the sodium channel’s structure and reduces its sensitivity to pyrethroid. This region is crucial for controlling the opening and closing of the sodium channel, and the mutation prevents pyrethroid from binding effectively, thereby leading to resistance in P. absoluta [157]. Furthermore, the ace-1 gene encodes acetylcholinesterase (AChE), an enzyme crucial for breaking down acetylcholine in the insect nervous system [158,159]. A mutation in this gene in P. absoluta, particularly point mutations that lead to a single-nucleotide polymorphism (SNP), alters the enzyme’s structure, especially at the active site [160]. This reduces AChE’s affinity for insecticides like organophosphates and carbamates, allowing the enzyme to continue breaking down acetylcholine even in the presence of these chemicals [157]. As a result, the insect pest survives, and the resistant trait spreads, making insecticide treatments less effective over time [157]. Furthermore, Ong’onge, Ajene [157] also stated that after about five years of insecticide application, the pest population started developing resistance, and this trend is predicted to continue, leading to failure of the chemical control method if not managed properly.

Resistance to key insecticides has evolved dramatically in field populations of P. absoluta, with varying degrees of resistance across different chemical classes [156]. Pyrethroids, including bifenthrin and permethrin, exhibited only low resistance (>12.5-fold), while Bacillus thuringiensis and the mixture deltamethrin + triazophos similarly showed limited resistance. In contrast, chitin synthesis inhibitors (diflubenzuron, triflumuron, and diflubenzuron) exhibited high resistance levels (up to 222.3-fold), suggesting a critical failure in their long-term efficacy. Indoxacarb also showed moderate resistance, with a 27.5-fold increase compared to susceptible populations. Notably, the emergence of resistance was strongly linked to insecticide use patterns, with a disproportionate reliance on chitin synthesis inhibitors exacerbating resistance development [156]. Furthermore, the insecticide resistance against P. absoluta has been reported from various countries such as China [161,162], Kenya [157], Latin America [60]. Zhang, Li [162] utilized insecticide efficacy monitoring as a basic tool for proactive evidence-based resistance management. They investigated the susceptibilities of seven populations (Gansu, Guizhou, Inner Mongolia, Shanxi, Sichuan, Xinjiang, Yunnan) of P. absoluta across China against six insecticides (Bacillus thuringiensis, chlorpyrifos, chlorantraniliprole, emamection benzoate, indoxacarb, and spinosad. The results indicated that P. absoluta exhibited the highest resistance to chlorpyrifos and chlorantraniliprole in Shanxi and Yunnan, while most populations showed low resistance to B. thuringiensis emamection benzoate, indoxacarb, and spinosad, highlighting the need for rational insecticide use to manage emerging resistance. Guedes, Roditakis [163] revealed that the development of insecticide resistance is relatively fast in this species in South America and Europe due to altered target-site sensitivity and/or enhanced detoxification. Therefore, the implementation of integrated control programs and appropriate resistance management strategies is necessary to keep P. absoluta infestations under economic damage thresholds.

Table 2. Country-wise insecticide resistance mechanisms and resistance ratios in Phthorimaea (Tuta) absoluta.

Country	Insecticide/Active Ingredient	Class	Population/Strain	Resistance Ratio (RR)	Mechanism Identified	Method/Evidence	Remarks/Management Implication	References
Brazil	Chlorantraniliprole, Flubendiamide	Diamide insecticides	BR-GML1, BR-PSQ	>3000-fold	G4903E, I4746M mutations	Genotyping, pyrosequencing	High resistance in Brazilian strains, highlighting the importance of early resistance detection and management	[164]
	Deltamethrin	Pyrethroid	Various Brazilian populations	1.18 to 5.12	Target site mutation: L1014F, M918T, T929I	Bioassays, TaqMan diagnostic assay	High frequency of L1014F mutation, suggesting widespread resistance. Control failure in all populations.	[165]
	Alpha-Cypermethrin	Pyrethroid	Various Brazilian populations	1.27 to 11.10	Target site mutation: L1014F, T929I	Bioassays, TaqMan diagnostic assays	The T929I mutation appears to provide selective advantage in some populations. Widespread resistance.	[165]
	Permethrin	Pyrethroid	Various Brazilian populations	1.26 to 5.27	Target site mutation: L1014F, M918T, T929I	Bioassays, TaqMan diagnostic assays	Resistance to permethrin similar to other pyrethroids. Confirmed role of metabolic detoxification enzymes.	[165]
	Abamectin	Avermectin	8 populations from Northeast, Midwest, Southeast, and South Brazil	1.5 to 6.2 times	Detoxification enzymes (cytochrome CYP450s, GSTs)	Bioassays, enzyme activity assays	Resistance levels low, no major control failures observed, monitor long-term effectiveness	[166]
	Cartap	Nereistoxin derivative	8 populations from various Brazilian regions	1.5 to 6.4 times	Cytochrome CYP450s, GSTs involvement	Bioassays, enzyme activity assays	Populations from certain regions show resistance ratios that may lead to control failures	[166]
	Chlorfenapyr	Pyrrole	8 populations from different regions	1.4 to 4.6 times	CYP450 monooxygenase and GST activity	Bioassays, enzyme activity assays	Populations show low resistance, no cross-resistance to other insecticides like indoxacarb	[166]
	Indoxacarb	Oxadiazine	8 populations from various Brazilian region	1.1 to 3.3 times	No cross-resistance with metaflumizone	Bioassays, enzyme activity assays	No significant resistance was found; populations remain susceptible at recommended doses	[166]
	Metaflumizone	Semicarbazone	8 populations from different regions	2.5 to 21.2 times	Cross-resistance not observed	Bioassays, enzyme activity assays	Low to moderate resistance, some populations resistant at higher doses	[166]
	Spinosad	Spinosyn	IRA -Sel, IRA-Unsel, PLT-Sus	IRA-Sel: 48,900-fold, IRA-UnSel: 284-fold, PLT-Sus: 1-fold	Mutation G275E in nAChR α6 subunit	Bioassays, gene sequencing, TaqMan diagnostic assays	Resistance is linked to the G275E mutation in the nAChR α6 subunit. Resistance is autosomal, recessive, and monofactorial in the IRA-Sel strain.	[167]
	Cartap Hydrochloride	Nereistoxin derivative	GML2-Res, JDR1-Sus	GML2-Res: 537.1-fold, JDR1-Sus: 2.3-fold	Detoxification (hydrolases, GSTs, CYP450 monooxygenases)	Concentration-mortality bioassays, genetic studies	Cross-resistance with other insecticides (e.g., deltamethrin, methoxyfenozide). Synergism observed with inhibitors.	[168]
	Isocycloseram	Isoxazoline	JUA-2024, LGD-Clora, GVT-Aba,	GVT-Aba: 30.19-fold, JUA-2024: 1.06-fold, LGD-Clora: 1.06	Detoxification (cytochrome CYP450s)	Leaf-dip bioassay, LC50 and LC99 estimates	Early tolerance shifts, suggesting emerging resistance. Monitoring needed.	[169]
	Tolfenpyrad	Pyrazole	PTY-2024, PIE-2024, IRE-2023	PIE-2024: 2.15-fold, PTY-2024: 2.15-fold IRE-2023: 14.13-fold	Detoxification enzymes involved (esterases, GSTs)	Bioassay, diagnostic concentration estimation	Early signs of tolerance observed; need to manage emerging resistance	[169]
	Abamectin	Glutamate-gated chloride channel agonist	GVT-Aba, IRE-2024, SUM-2024	Up to 30-fold resistance	Esterase-based resistance	Synergism bioassays with S,S,S-tributyl phosphorotrithioate, and Piperonyl butoxide	Widespread resistance, linked to metabolic detoxification pathways	[169]
	Fipronil	Phenylpyrazole	Various populations	Resistance in multiple populations	GABA receptor antagonism	Diagnostic dose monitoring, synergism assays	Cross-resistance potential with other chloride channel modulators	[169]
Chile	Spinosad	Spinosyn	Azapa 1, Azapa 2, Lluta, Colín, Valdivia, S	Azapa 1: 1.83, Azapa 2: 2.04, Lluta: 2.32, Colín: 1.71, Valdivia: 1.41, S: 1	Increased MFO, EST, and GST activity	Bioassays with diagnostic concentration (1 mg/L), enzyme activity assays	Enhanced detoxification enzyme activity (MFO, EST) in resistant populations; possible cross-resistance with other insecticides	[170]
China	Tetraniliprole	Diamide insecticide	HL and 17 other populations	HL: 36.2-fold, other populations: 1.1–3.0-fold	CYP450 monooxygenase and GST activity	Leaf-dip bioassay, synergist tests (PBO, DEM, TPP), genetic analysis, enzyme activity assays	Tetraniliprole resistance in HL population is moderate; resistance inheritance is autosomal and polygenic	[171]
	Spinetoram	Spinosyn derivative	SPI-R (20th generation)	410.86-fold	Increased detoxification enzyme activities (CYP450s, GSTs, CarEs)	Bioassay (leaf dipping), synergist assays (PBO, DEM, TPP)	Resistance inheritance was polygenic, autosomal, incompletely recessive with fitness costs observed (extended larval stages, reduced adult longevity)	[172]
Greece	Chlorantraniliprole	Diamide insecticide	GR-IER-15-2	55-fold	G4903E, G4903V mutations	Genotyping, bioassays	G4903E and G4903V mutations linked to resistance; also carries I4746M mutation in low frequency	[164]
Spain	Chlorantraniliprole	Diamide insecticide	Ssus, Mur, Sres, Sus strains of P. absoluta	Ssus: 1, Mur: 18.2-fold, Sres: 44,614-fold, Sus: 1.7-fold	Overexpression of UGT34A23	RNA-seq, gene expression analysis, bioassays with transgenic Drosophila melanogaster	Resistance linked to metabolic detoxification (UGT overexpression), suggesting potential for synergists and molecular assays in management	[173]
	Chlorantraniliprole	Diamide insecticide	ES-MUR-14	8-fold	RyR mutations (low frequency of G4903E)	Bioassays, pyrosequencing	Moderate resistance, further research needed on potential other resistance mechanisms (e.g., detoxification)	[164]
Iran	Indoxacarb	Oxadiazine	Ar, Bu, Ya, Kr, Sh, Mo	Ar: 10.51-fold, Bu: 6.03-fold, Ya: 14.45-fold, Kr: 2.37-fold, Sh: 10.04-fold, Mo: 1.59-fold	Mutations in sodium channel (F1845Y and V1848I), detoxification (CYP450s, CarEs)	Bioassay, synergism assays with PBO, DEM, TPP, enzyme activity assays	Resistance primarily via target site mutations; no significant cross-resistance with other insecticides	[174]
Italy	Chlorantraniliprole, Flubendiamide	Diamide insecticides	IT-GELA-SD4, GR-Lab	>1000-fold in IT-GELA-SD4, less than 2-fold in GR-Lab	Ryanodine receptor mutations (G4903E, I4746M, G4903V)	Bioassays (leaf dip), pyrosequencing, radioligand binding studies	Resistance is linked to mutations in the RyR gene, autosomal and incompletely recessive inheritance; urgent resistance management strategies recommended	[164]

BR-GML1, Brazil–Gameleira (Bahia)–population 1–2014 (field strain); BR-PSQ, Brazil–Pesqueira (Pernambuco)–2014 (field strain); G4903E, Glycine at position 4903 replaced by Glutamic acid; I4746M, Isoleucine at position 4746 replaced by Methionine; L1014F, Leucine is replaced by Phenylalanine at position 1014; M918T, Methionine is replaced by Threonine at position 918; T929I, Threonine is replaced by Isoleucine at position 929; CYP450s, Cytochrome P450 monooxygenases; CarEs, Carboxylesterases; GST, glutathione S-transferase; IRA-Sel, Iraquara (BA, Brazil) spinosad-selected resistant strain; IRA-Unsel, Iraquara (BA, Brazil) population without insecticide selection; PLT-Sus, Pelotas (RS, Brazil) susceptible laboratory strain; G275E, Glycine at position 275 is replaced by Glutamic acid; nAChR α6 subunit, nicotinic acetylcholine receptor alpha-6 subunit; TaqMan diagnostic assay, Fluorescent probe-based real-time PCR tests using Taq DNA polymerase to detect specific genes or mutations; GML2-Res, João Dourado (BA, Brazil)–population 2–resistant strain; JDR1-Sus, João Dourado (BA, Brazil)–population 1–susceptible strain; JUA-2024, Juazeiro (BA, Brazil)–collected in 2024 (field population); LGD-Clora, Lagoa Grande (BA, Brazil)–chlorantraniliprole-selected/resistant strain; GVT-Aba, Gravatá (PE, Brazil)–abamectin-selected/resistant strain; LC₅₀, Lethal concentration that kills 50% of the population; LC₉₉, Lethal concentration that kills 99% of the population; PTY-2024, Paty do Alferes (RJ, Brazil)–collected in 2024 (field population); PIE-2024, Piedade (SP, Brazil)–collected in 2024 (field population); IRE-2023, Irecê (BA, Brazil)–collected in 2023 (field population); IRE-2024, Irecê (BA, Brazil)–collected in 2024 (field population); SUM-2024, Sumaré (SP, Brazil)–collected in 2024 (field population); GABA receptor, Gamma-aminobutyric acid receptor; Azapa 1, Azapa Valley–population 1 (field population); Azapa 2, Azapa Valley–population 2 (field population); Lluta, Lluta Valley field population; Colín, Colín location field population; Valdivia, Valdivia field population; S, Susceptible lab strain; MFO, Mixed-Function Oxidases; EST, Esterases; HL, Huailai; PBO, Piperonyl butoxide DEM, Diethyl maleate, TPP, Triphenyl phosphate; SPI-R, Spinetoram Resistant Strain; GR-IER-15-2 = Greece–Ierapetra (Kalogeri)–collected in 2015–population 2 (field strain); G4903V, Glycine at position 4903 replaced by Valine; RyR gene, Ryanodine Receptor gene; Ssus, Super susceptible strain; Mur, Moderately resistant strain; Sres, Strongly resistant strain; Sus, Susceptible strain; UGT34A23, uridine diphosphate-glycosyltransferase 34A23; RNA-seq, RNA sequencing; UGT, uridine di-phosphate-glycosyltransferase; ES-MUR-14, Spain–Murcia (Lorca)–collected in 2014 (field strain); Ar, Ardabil; Bu, Bushehr; Ya, Yazd; Kr, Kerman; Sh, ShahreKord; Mo, control; F1845Y, Phenylalanine at position 1845 is replaced by Tyrosine; V1848I, Valine at position 1848 is replaced by Isoleucine; IT-GELA-SD4, Italy–Gela population–selected for 4 cycles (chlorantraniliprole-selected strain); GR-Lab, Greece–laboratory-maintained susceptible strain.

provides an overview of the country-wise insecticide resistance mechanisms in P. absoluta.

8. Other Management Strategies

8.1. Biological Control

Biological control is one of the components of an integrated management program through which a number of natural enemies are utilized against P. absoluta to keep its population below the economic threshold level [175,176]. The biological control agents include predators, parasitoids, pathogens, and nematodes are successfully utilized against insect pests [177]. Rubio, Montes [178] claimed that joint use of both predator Macrolophus basicornis (Stal, 1860) and Trichogramma pretiosum, (Riley, 1879) is a better option for decreasing the P. absoluta population as compared to the use of each biological control agent separately. Furthermore, the introduction of M. basicornis after T. pretiosum release significantly reduced the adult P. absoluta population by 28%, decreasing even more the damage caused in tomato crops compared to the use of T. pretiosum alone. It is necessary to determine the predators and parasitoid species to assess the effectiveness of these natural enemies for biological and integrated pest management in crops.

Akat and Bayhan [179] performed a survey to determine predators and parasitoid species of P. absoluta in tomato field in Diyarbakir province, Turkey and found the three parasitoids such as Bracon didemie (Beyarslan, 2002), Bracon viktorovi (Tobias, 1961), and Nracon hebetor (Say, 1836); and ten predators including, Campylomma diversicornis Reuter, 1890; Chrysoperla carnea (Stephens, 1836); Coccinella septempunctata (Linnaeus, 1758); Geocoris megacephalus (Rossi, 1790); Hippodamia variegate (Geoffroy, 1777); Macrolophus costalis (Fieber, 1858); Macrolophus pygmaeus (Rambur, 1839); Nysius graminicola (Lolenati, 1845); Orius spp. Orius niger (Wolff, 1804). Nearly sixty species of predators, belonging to approximately twenty-six families, have been employed as natural enemies against P. absoluta. Of these, fifty species have been recorded in South America, while only ten species have been documented within their invasive range, particularly in European countries [180].

The significance of integrated pest management using predators against P. absoluta became evident in areas that were invaded early. Current findings suggest that the commercial availability of biological control agents has played a significant role primarily in these early-invaded regions, such as southern Europe [181,182]. However, it is still too early to determine whether similar biological control practices will be effective in managing this pest in areas that have recently experienced invasion [183]. Despite this, two commercially available mirid bugs, Nezara viridula (Linnaeus, 1758) and Macrolophus pygmaeus (Rambur, 1839), have emerged as key biological control agents in Europe [184]. Pérez-Hedo, Riahi [185] also stated that the Nesidiocoris tenuis (Reuter, 1905), M. pygmaeus, and Dixyphus Hesperus (Knight, 1923) hold significant potential for enhancing P. absoluta pest management in horticultural crops. In 2020, the green lacewing, Chrysoperla carnea (Stephens, 1836), was first utilized as a promising biocontrol agent for P. absoluta and assessed its efficiency in controlled conditions and the field [186]. Laboratory results indicated that C. carnea consumed 36 ± 2 eggs within 24 h and 72 ± 4 eggs within 48 h, with 2% of larvae killed inside and 35% killed outside leaf galleries. Whereas, in field trials, the release of C. carnea reduced larval density by 4 to 6 times compared to control plots. The biocontrol plots showed lower pest density and damage, and significantly higher tomato yield compared to control plots, suggesting that C. carnea is an effective biological control agent for managing P. absoluta [186]. Future perspectives include expanding field trials, integrating with other biocontrol agents, developing commercial production methods, optimizing release timing, exploring its impact on other pests, and promoting sustainable, eco-friendly pest management strategies.

The association of parasitoids with P. absoluta is critically important for sustainable pest management, offering a natural, eco-friendly alternative to chemical insecticides that often fail due to pest resistance [187]. In 2019, Salas Gervassio, Aquino [188] re-examined the parasitoids of P. absoluta for optimized biological control in South America. They reported that over fifty species of morphospecies of Hymenoptera were associated with P. absoluta, but only half of these could be confirmed as parasitizing the pest. This limitation was attributed to incomplete or unreliable species identification, erroneous species names, and a lack of supporting literature [188]. The inoculative seasonal release of endoparasitoid, Pseudapantales dignus (Muesebeck, 1938) has proven to be an effective and reliable crop protection strategy, both in open fields and in greenhouses, as an augmentative biocontrol method [189]. In a semi-field greenhouse setup, the P. absoluta, P. dingus relative densities ranging from 2:1 to 10:5 were tested. The parasitism rates ranged from 23% to 61%, with the highest parasitism observed at a density of 10:3. At low host densities, parasitism was negligible due to reduced host localization cues. The higher parasitoid release rates resulted in decreased parasitism, potentially due to mutual interference among females, suggesting the potential of P. dingus for biological control, though its effectiveness varies with host density [189]. The abundance and functional diversity of natural enemies is also associated with the attractiveness of insectary plants [190]. The flowering plants, including Achillea millefolium (Linnaeus, 1753), Fagopyrum esculentum (Moench, 1802), Lobularia maritima (Linnaeus) Desvaux, 1814), and Sinapis alba (Linnaeus, 1753), were grown in proximity to tomato plants that significantly attract natural enemies, including Aeolothrips spp. Coccinella spp., Hoverflies, M. pygmaeus, N. tenuis, Necremnus tutae (Ribes & Bernardo, 2015), Orius spp. [190]. These insectary plants provide critical resources, including nectar, pollen, and alternative food sources that support the survival, fitness, and foraging behavior of these beneficials [191,192].

The host specificity of parasitoid depends on their native or invasive nature. For instance, the native N. tutae is polyphagous and attacks multiple non-target species in the laboratory, such as Cameraria ohridella (Deschka & Dimic, 1986), Liriomyza bryoniae (Kaltenbach, 1858), and Leucoptera malifoliella (O. Costa, 1836) [193]. In contrast, the invasive endoparasitoid Dolichogenidea gelechiidivoris (Marsh, 1975) attacks only P. operculella. In greenhouse trials, N. tutae did not show a preference between P. absoluta and P. operculella. Whereas D. gelechiidivoris exhibited a preference for P. absoluta, with a significantly higher parasitism rate on tomato plants infested with P. absoluta compared to P. operculella on potato plants [193]. The difference in host preference between the two parasitoids stems from their ecological specialization and evolutionary history with P. absoluta. Nematodes are also the most promising biological control agent, which belongs to the Heterorhabditidae and Steinernematidae families [194,195]. Nematodes of the genera Steinernema and Heterorhabditis contain symbiotic bacteria belonging to the genera Xenorhabdus and Photorhabdus, respectively, which are responsible for causing mortality to insects [196]. The infective juveniles enter hosts through natural openings and release their symbiotic bacteria that eventually kill the host [196,197]. In this context, Kamou, Papafoti [198] investigated the effects of two entomopathogenic nematode species, Steinernema carpocapsae (Weiser, 1955) and Heterorhabditis bacteriophora (Poinar, 1976), as well as their bacterial symbionts, Xenorhabdus nematophila (Poinar & Thomas, 1965) and Photorhabdus luminescens (Poinar & Thomas, 1979), against P. absoluta larvae. The results indicated that the S. carpocapsae and H. bacteriophora were the most effective, causing approximately ninety-eight percent mortality of P. absoluta larvae. Regarding the bacteria, X. nematophila was the most effective, causing 69% mortality in young larvae, thereby suggesting its potential as a biocontrol agent in the field following augmentative release [198]. Many studies have also demonstrated that P. absoluta larvae are highly susceptible to entomopathogenic nematodes, which are used as a biocontrol agent [199,200,201,202]. Table 3 summarizes the efficacy of various natural enemies of P. absoluta.

Plant-mediated RNA interference (RNAi) is the most promising and innovative, and sustainable pest management strategy for controlling insect pests by targeting crucial insect genes through transgenic expression [203]. In Turkey, Hashmi, Tariq [204] utilized this technique, in which transgenic tomato plants were genetically engineered to produce double-stranded (dsRNA) targeting the two key genes acetylcholinesterase 1 (AChE1) and SEC23, which are essential for P. absoluta survival. When feeding on transgenic plants, this insect pest ingests dsRNA, which enters the insect cell via the digestive system. The dsRNA triggers the RNAi pathway, where it is processed into small interfering RNAs (siRNAs) that bind to the mRNA of target genes, resulting in gene silencing and preventing the production of vital proteins. The silencing of AChE1 and SEC23 leads to nerve dysfunction and disrupts insect physiology, respectively, making larvae more susceptible to insecticides, such as organophosphates. As a result, higher mortality, reduced growth, and developmental abnormalities ultimately provide an effective pest control method [204]. Current practical limitations of plant-mediated RNAi remain substantial despite its promise for pest control. Field deployment is constrained by delivery inefficiency, because RNAi performance depends on sufficient dsRNA accumulation in plant tissues [205], while insects cannot amplify the RNAi signal and many species rapidly degrade ingested dsRNA through gut nucleases, reducing silencing efficiency [206,207]. Target selection is also a major challenge, as not all essential genes respond equally well to silencing, and RNAi sensitivity differs across insect groups [208,209]. In addition, nuclear transformation may produce low and unstable dsRNA expression, whereas plastid transformation, although often more effective, is currently feasible in only a limited number of crop species [210].

The large-scale application of plant-mediated RNAi is still more experimental than operational and remains largely confined to laboratory or small-scale settings, while commercialization requires broader field validation, resistance management, and crop-specific optimization [203]. Biosafety and regulatory scrutiny remain important because human safety, non-target effects, and ecological assessment must be addressed, yet these evaluations are complicated by the lack of full genomic information for many non-target organisms [211,212]. Scalability is further limited because not all crops are easily transformed and a single transgenic strategy may not control multiple pests effectively [109]. Although RNAi may have relatively low upfront development costs, the costs of large-scale commercial deployment still require careful consideration before widespread adoption [213,214].

Table 3. Natural enemies of Phthorimaea (Tuta) absoluta and their reported efficacy.

Natural Enemy	Group	Type of Control Agent	Target Stage of P. absoluta	Reported Efficacy/Performance	Study Condition	Region/Country	Key Findings	References
Trichogramma achaeae	Hymenoptera: Trichogrammatidae	Parasitoid (Egg)	Eggs	Parasitism and emergence unaffected by resistant or susceptible genotypes, but egg size influenced the proportion of female parasitoids. Fewer female parasitoids from resistant plants.	Isolation and tomato leaflets	Spain	Solanum arcanum negatively impacted parasitism and emergence due to high glandular trichomes.	[215]
Necremnus tutae	Hymenoptera: Eulophidae	Parasitoid (Larval)	Larvae (Second to third instar)	Fewer parasitoids emerged on S. arcanum compared to other genotypes.	Infested leaflets with larvae	Spain	S. arcanum and Solanum neorickii negatively affected parasitism performance.
Macrolophus pygmaeus	Hemiptera: Miridae	Predator	Eggs and larvae	Predation lower on S. arcanum due to high glandular trichomes. Higher predation on S. neorickii and other genotypes.	Egg and larval predation on tomato genotypes	Spain	S. arcanum hinders predator efficacy, while S. neorickii allowed better predation success.
Black Soldier Fly Oil & Neem Oil	Insect-derived/Plant-derived	Biorational (Ovicidal, Larvicidal, Antifeedant)	Eggs and larvae	Moderate ovicidal suppression (20–55% mortality); higher larval mortality (33.8–92.9%); leaf penetration deterrence and increased larval mortality in treated plants.	Semi-field screenhouse trials	Kenya	Significant egg mortality and larval mortality in both P. absoluta and Spodoptera frugiperda. Insect oil exhibited lower LC50 than neem oil in larvicidal bioassays.	[216]
Neochrysocharis formosa (thelytokous (TH) strain)	Hymenoptera: Eulophidae	Parasitoid	1st instar larvae	High parasitism rates and effective host-stinging on 1st instar larvae. Parasitism and stinging rates are higher compared to AR strain, especially in lower density settings.	Laboratory/controlled conditions	China	TH strain is more effective at controlling P. absoluta in early infestations due to higher preference for 1st instar larvae and efficient parasitism.	[217]
Neochrysocharis formosa (arrhenotokous (AR) strain)	Hymenoptera: Eulophidae	Parasitoid	1st and 2nd instar larvae	Parasitism less effective than TH strain, with host-stinging and feeding behavior being more prominent at higher densities.	Laboratory/controlled conditions	China	AR strain exhibits lower attack rates compared to the TH strain, especially when larvae are more than 1st instar.
Dolichogenidea gelechiidivoris	Hymenoptera: Braconidae	Parasitoid (Larval)	1st, 2nd, 3rd, and 4th instars	Parasitized and successfully developed in all four host larval instars. Females preferentially oviposited in early instars (1st and 2nd).	Laboratory conditions at 26 ± 4 °C	Kenya	High parasitism in early instars, with significant differences between early (1st and 2nd) vs. late (3rd and 4th) instars in terms of egg deposition and cocoon formation.	[218]
Necremnus artynes	Hymenoptera: Eulophidae	Parasitoid (Larval	Larvae (2nd and 3rd instars)	Significant increase in longevity with buckwheat, Fagopyrum esculentum and sugar solution. Host-feeding was not as effective in increasing longevity	Greenhouse, laboratory conditions	Belgium	Longevity was significantly enhanced by F. esculentum and sugar solution. Host-feeding did not significantly increase longevity.	[219]
Bracon hebetor	Hymenoptera: Braconidae	Parasitoid	4th and 5th instars	The highest parasitism rates and fecundity observed on Galleria mellonella larvae. Lower parasitism rates for P. absoluta and Phthorimaea operculella.	Laboratory/greenhouse conditions	Faisalabad/Pakistan	Best performance on G. mellonella, poor performance on P. absoluta. Longevity and egg-laying capacity are affected by diet and host conditions.	[220]
Nesidiocoris tenuis	Hemiptera: Miridae	Predator	All stages	Presence significantly reduced P. absoluta population growth. However, exposure to lambda-cyhalothrin affected predation behavior and longevity.	Laboratory/greenhouse conditions	Alenya/France	Effective as a predator against P. absoluta, but its behavior and longevity are negatively impacted by chemical treatments, especially lambda-cyhalothrin.	[221]
Dicyphus errans	Hemiptera: Miridae	Predator	Eggs, 1st-instar larvae	Effective in preying on P. absoluta eggs (up to 12.4 eggs/day). Females consumed more eggs and larvae than males.	Laboratory conditions	Italy/Europe	Females consumed significantly more eggs (73.6%) compared to males (57.6%). Preference for 1st-instar larvae.	[222]
Dolichogenidea gelechiidivoris	Hymenoptera: Braconidae	Parasitoid (Larval)	All developmental stages	The parasitoid performed well in all regions except for coastal areas under the current climatic scenario and is predicted to improve under future scenarios.	Field conditions, climate modeling	Kenya	The fuzzy model predicted good performance across regions, with significant improvements in the Rift valley and coastal regions under future climate scenarios.	[223]
Macrolophus pygmaeus	Hemiptera: Miridae	Predator	Eggs, larvae	Intraguild predation (IGP) occurs when Macrolophus pygmaeus feeds on parasitized eggs, mainly early in the development of parasitoid larvae.	Laboratory/greenhouse conditions	Mediterranean regions	Exhibited preference for parasitized eggs in the early stages (yellow eggs), leading to reduced parasitoid survival rates.	[224]
Trichogramma achaeae	Hymenoptera: Trichogrammatidae	Parasitoid (Egg)	Eggs	Significant increase in pest control when combined with M. pygmaeus, despite some negative effects from intraguild predation.	Laboratory/greenhouse conditions	Mediterranean regions	Combining Trichogramma parasitoids with M. pygmaeus improves pest control compared to using either agent alone.
Stenomesius japonicus	Hymenoptera: Eulophidae	Parasitoid (Larval)	3rd instar larvae	Effective in controlling P. absoluta larvae, with high parasitism rates observed when alone. However, parasitism decreased in the presence of the omnivorous predator.	Laboratory/greenhouse conditions	France	When combined with M. pygmaeus, parasitism rates were negatively affected by intraguild predation but still had significant pest control.	[225]
Macrolophus pygmaeus	Hemiptera: Miridae	Predator (Generalist)	Eggs and larvae	Strong immediate effect on P. absoluta eggs and larvae. However, its population was lower when in competition with S. japonicus as it faced intraguild predation	Laboratory/greenhouse conditions	France	M. pygmaeus had a stronger initial impact on pest populations, but its longer-term effectiveness was reduced by competition with S. japonicus.

LC₅₀, Lethal concentration that kills 50% of the population.

Table 3. Natural enemies of Phthorimaea (Tuta) absoluta and their reported efficacy.

Natural Enemy	Group	Type of Control Agent	Target Stage of P. absoluta	Reported Efficacy/Performance	Study Condition	Region/Country	Key Findings	References
Trichogramma achaeae	Hymenoptera: Trichogrammatidae	Parasitoid (Egg)	Eggs	Parasitism and emergence unaffected by resistant or susceptible genotypes, but egg size influenced the proportion of female parasitoids. Fewer female parasitoids from resistant plants.	Isolation and tomato leaflets	Spain	Solanum arcanum negatively impacted parasitism and emergence due to high glandular trichomes.	[215]
Necremnus tutae	Hymenoptera: Eulophidae	Parasitoid (Larval)	Larvae (Second to third instar)	Fewer parasitoids emerged on S. arcanum compared to other genotypes.	Infested leaflets with larvae	Spain	S. arcanum and Solanum neorickii negatively affected parasitism performance.
Macrolophus pygmaeus	Hemiptera: Miridae	Predator	Eggs and larvae	Predation lower on S. arcanum due to high glandular trichomes. Higher predation on S. neorickii and other genotypes.	Egg and larval predation on tomato genotypes	Spain	S. arcanum hinders predator efficacy, while S. neorickii allowed better predation success.
Black Soldier Fly Oil & Neem Oil	Insect-derived/Plant-derived	Biorational (Ovicidal, Larvicidal, Antifeedant)	Eggs and larvae	Moderate ovicidal suppression (20–55% mortality); higher larval mortality (33.8–92.9%); leaf penetration deterrence and increased larval mortality in treated plants.	Semi-field screenhouse trials	Kenya	Significant egg mortality and larval mortality in both P. absoluta and Spodoptera frugiperda. Insect oil exhibited lower LC50 than neem oil in larvicidal bioassays.	[216]
Neochrysocharis formosa (thelytokous (TH) strain)	Hymenoptera: Eulophidae	Parasitoid	1st instar larvae	High parasitism rates and effective host-stinging on 1st instar larvae. Parasitism and stinging rates are higher compared to AR strain, especially in lower density settings.	Laboratory/controlled conditions	China	TH strain is more effective at controlling P. absoluta in early infestations due to higher preference for 1st instar larvae and efficient parasitism.	[217]
Neochrysocharis formosa (arrhenotokous (AR) strain)	Hymenoptera: Eulophidae	Parasitoid	1st and 2nd instar larvae	Parasitism less effective than TH strain, with host-stinging and feeding behavior being more prominent at higher densities.	Laboratory/controlled conditions	China	AR strain exhibits lower attack rates compared to the TH strain, especially when larvae are more than 1st instar.
Dolichogenidea gelechiidivoris	Hymenoptera: Braconidae	Parasitoid (Larval)	1st, 2nd, 3rd, and 4th instars	Parasitized and successfully developed in all four host larval instars. Females preferentially oviposited in early instars (1st and 2nd).	Laboratory conditions at 26 ± 4 °C	Kenya	High parasitism in early instars, with significant differences between early (1st and 2nd) vs. late (3rd and 4th) instars in terms of egg deposition and cocoon formation.	[218]
Necremnus artynes	Hymenoptera: Eulophidae	Parasitoid (Larval	Larvae (2nd and 3rd instars)	Significant increase in longevity with buckwheat, Fagopyrum esculentum and sugar solution. Host-feeding was not as effective in increasing longevity	Greenhouse, laboratory conditions	Belgium	Longevity was significantly enhanced by F. esculentum and sugar solution. Host-feeding did not significantly increase longevity.	[219]
Bracon hebetor	Hymenoptera: Braconidae	Parasitoid	4th and 5th instars	The highest parasitism rates and fecundity observed on Galleria mellonella larvae. Lower parasitism rates for P. absoluta and Phthorimaea operculella.	Laboratory/greenhouse conditions	Faisalabad/Pakistan	Best performance on G. mellonella, poor performance on P. absoluta. Longevity and egg-laying capacity are affected by diet and host conditions.	[220]
Nesidiocoris tenuis	Hemiptera: Miridae	Predator	All stages	Presence significantly reduced P. absoluta population growth. However, exposure to lambda-cyhalothrin affected predation behavior and longevity.	Laboratory/greenhouse conditions	Alenya/France	Effective as a predator against P. absoluta, but its behavior and longevity are negatively impacted by chemical treatments, especially lambda-cyhalothrin.	[221]
Dicyphus errans	Hemiptera: Miridae	Predator	Eggs, 1st-instar larvae	Effective in preying on P. absoluta eggs (up to 12.4 eggs/day). Females consumed more eggs and larvae than males.	Laboratory conditions	Italy/Europe	Females consumed significantly more eggs (73.6%) compared to males (57.6%). Preference for 1st-instar larvae.	[222]
Dolichogenidea gelechiidivoris	Hymenoptera: Braconidae	Parasitoid (Larval)	All developmental stages	The parasitoid performed well in all regions except for coastal areas under the current climatic scenario and is predicted to improve under future scenarios.	Field conditions, climate modeling	Kenya	The fuzzy model predicted good performance across regions, with significant improvements in the Rift valley and coastal regions under future climate scenarios.	[223]
Macrolophus pygmaeus	Hemiptera: Miridae	Predator	Eggs, larvae	Intraguild predation (IGP) occurs when Macrolophus pygmaeus feeds on parasitized eggs, mainly early in the development of parasitoid larvae.	Laboratory/greenhouse conditions	Mediterranean regions	Exhibited preference for parasitized eggs in the early stages (yellow eggs), leading to reduced parasitoid survival rates.	[224]
Trichogramma achaeae	Hymenoptera: Trichogrammatidae	Parasitoid (Egg)	Eggs	Significant increase in pest control when combined with M. pygmaeus, despite some negative effects from intraguild predation.	Laboratory/greenhouse conditions	Mediterranean regions	Combining Trichogramma parasitoids with M. pygmaeus improves pest control compared to using either agent alone.
Stenomesius japonicus	Hymenoptera: Eulophidae	Parasitoid (Larval)	3rd instar larvae	Effective in controlling P. absoluta larvae, with high parasitism rates observed when alone. However, parasitism decreased in the presence of the omnivorous predator.	Laboratory/greenhouse conditions	France	When combined with M. pygmaeus, parasitism rates were negatively affected by intraguild predation but still had significant pest control.	[225]
Macrolophus pygmaeus	Hemiptera: Miridae	Predator (Generalist)	Eggs and larvae	Strong immediate effect on P. absoluta eggs and larvae. However, its population was lower when in competition with S. japonicus as it faced intraguild predation	Laboratory/greenhouse conditions	France	M. pygmaeus had a stronger initial impact on pest populations, but its longer-term effectiveness was reduced by competition with S. japonicus.

LC₅₀, Lethal concentration that kills 50% of the population.

8.2. Use of Sex Pheromones

Pheromone traps are a critical, sustainable tool for managing insect pests by utilizing synthetic pheromones to attract and capture male moths [226]. Yang, Cai [227] synthesized the pheromones (3E,8Z,11Z)-3,8,11-tetradecatrienyl acetate (1) and (3E,8Z,11Z)-3,8,11-tetradecatrienyl acetate (2) in seven-step process. The synthesis begins with tetrahydropyranyl (THP)-protected 4-bromo-1-butanol, followed by alkylation with 3-butyn-1-ol, reduction with lithium aluminum hydride (LiAIH4), acetylation, oxidation to form an aldehyde, and finally a Witting reaction with phosphate salts to yield the desired pheromones. Jabamo, Ayalew [228] reported that using sex pheromone reduced P. absoluta damage on tomato. However, sex pheromone and insecticide resulted in enhanced effect against P. absoluta. In 2021, the Yili region in Xinjiang, China, was invaded by P. absoluta and in response, the use of sex pheromone-based control techniques proved to be an effective method for managing this pest in the region [229]. However, polygyny in the Yili population is likely to reduce the effectiveness of sex pheromone-based control methods, suggesting caution for growers relying on this technique. Because in polygyny multiple P. absoluta females mate with a single male, it skews the sex ratio and reduces the effectiveness of sex pheromone-based control methods. The increased number of females diminishes the disruption of mating, potentially allowing continued pest reproduction despite pheromone intervention [229]. The appropriate timing of using pheromone traps is also a key factor in successful implementation of this technique. In this context, Zhang, Zhang [230] found that P. absoluta responded most strongly to sex pheromone lures from 05:30 a.m. to 08:30 a.m., with 95.8% of males captured during this period. The peak response occurred at 07:30 a.m., with 80.8% of males caught, highlighting the optimal time for using sex pheromone traps, aiding the development of more effective integrated pest management strategies. The more information regarding pheromone traps performance in monitoring and management of P. absoluta in

Table 4. Pheromone trap types and their performance in monitoring and management of Phthorimaea (Tuta) absoluta.

Formulation	Active Pheromone Component(s)	Trap Type	Purpose	Reported Performance	Duration/Operational Note	Crop System	Country/Region	References
Delta traps with pheromones	(3E,8Z,11Z)-tetradecatrien-1-yl acetate and (3E,8Z)-tetradecadien-1-yl acetate	Delta trap	Monitoring population	Effective in capturing males to monitor P. absoluta	Replaced every 4 weeks	Greenhouse tomatoes	Albania	[231]
Pheromone lures	(3E,8Z,11Z)-tetradecatrien-1-yl acetate, (3E,8Z)-tetradecadien-1-yl acetate	Delta Trap	Monitoring Population	High attraction to P. absoluta moths in tomato and potato fields	Traps monitored daily for moth capture	Tomato & Potato	United States of America/Panama	[232]
Synthetic 0.8 mg pheromone	(3E,8Z,11Z)-tetradecatrien-1-yl acetate	Delta trap	Monitoring population	Captured significantly more males; highest capture rate observed in golden light traps	Replace pheromone every 4–6 weeks depending on temperature	Tomato	Pakistan	[233]
Tomato leaf miner lure	(Z)-11-hexadecenal and other similar component	Delta, Wota-T, Solar Light trap	Monitoring and mass trapping	Best performance in white-colored delta traps; significant differences observed with color and height placement	Delta traps changed every 5 weeks, Wota-T traps adjusted at 1–4 ft heights	Tomato	Nepal	[234]
Qlure-TAU® Pheromone Capsule	(3E,8Z,11Z)-tetradecatrien-1-yl acetate	Plastic Container with Pheromone Capsule	Monitoring and Mass Trapping	White traps attracted the highest number of P. absoluta moths across all tested months	Traps serviced weekly; height fixed at 30 cm; color-specific analysis	Tomato	Egypt/Giza	[235]
Tomato leaf miner lure	(3E, 8Z, 11Z)-3,8,11-tetradecatrienyl acetate	Pan Water Traps	Monitoring male P. absoluta	No significant preference by color in most trials; green traps performed best	Pheromone lures replaced every 5–6 weeks, traps serviced every 1–2 weeks	Tomato	Tunisia	[236]
Synthetic sex pheromone capsule	(3E, 8Z, 11Z)-3,8,11-tetradecatrienyl acetate	Deltasan, Tutasan	Monitoring and mass trapping	Tutasan trap more effective during fruiting and ripening stages	Pheromone lures replaced weekly	Tomato	Côte d’Ivoire	[237]
Tuta Optima® 0.8 mg	Synthetic sex pheromone for T. absoluta	Water pan trap, Palm weevil bucket trap, Sticky delta trap	Monitoring and mass trapping	Water pan trap most effective with 406 males/trap; green traps attracted the most males	Traps checked regularly; water traps used	Tomato	Egypt	[238]
Tomato leaf miner lure	(3E, 8Z, 11Z)-tetradecatrien-1-yl acetate, (3E, 8Z)-tetradecadien-1-yl acetate	Delta, Water Pan	Monitoring and Mass Trapping	Delta traps and water-filled bowls with pheromone traps effectively capture P. absoluta	Traps monitored weekly, pheromone replaced as per environmental conditions	Tomato, Solanaceous Crops	Global (Africa, Europe, Middle East, and Asia)	[239]
Tomato leaf miner lure	(3E,8Z,11Z)-tetradecatrien-1-yl acetate, (3E,8Z)-tetradecadien-1-yl acetate	Delta, Water Pan, Sticky Trap	Monitoring and Mass Trapping	Sticky traps significantly outperformed delta and water pan traps in capturing P. absoluta males	Traps serviced weekly (replacing pheromones and sticky sheets)	Tomato	United Arab Emirates	[106]
P. absoluta synthetic lure	(3E, 8Z, 11Z)-tetradecatrien-1-yl acetate, (3E, 8Z)-tetradecadien-1-yl acetate	Delta, Water pan trap	Monitoring and mass trapping	Effective in monitoring P. absoluta populations, achieving 35–70% reduction in pest density	Traps serviced regularly; lures replaced every 4–6 weeks	Tomato	Nigeria, Kenya, Benin	[240]
2.8 mg of pheromone compound mixture	(3E, 8Z, 11Z)-tetradecatrien-1-yl acetate	Wing Trap	Monitoring and Mass Trapping	The best trapping effect achieved at 0.5m height with ladder suspension method	Traps serviced regularly, lures replaced monthly, sticky boards every 3 days	Tomato	China/E-Shan	[241]

.

8.3. Cultural Control

For both open field and greenhouse tomatoes, routine monitoring and removal of infested leaves in the early stages help reduce the initial pest population. Although labor-intensive, these practices are effective and straightforward. Other cultural control methods include intercropping, crop sanitation, crop rotation, deep plowing, and proper weed management [242,243]. Rotating tomato crops with non-solanaceous crops is essential for disrupting the life cycle of P. absoluta and can help in reducing pest infestation. This management strategy limits the chances of pest development and spread to the next generation [242]. Moreover, enhancement of resilience towards tomato crops requires proper supplements by either incorporating organic matter, such as manure, or synthetic nitrogenous fertilizers that nurture heavy crops that naturally resist P. absoluta attack and subsequent damage [244,245]. Additionally, applying dustable sulfur over tomato crops negatively affects the infestation and oviposition of P. absoluta due to its repellent effect [246]. Intercropping, the practice of growing multiple crops together, is a crucial sustainable pest management technique that reduces insect infestations by increasing agro-ecosystem diversity [247]. Zarei, Fathi [248] reported that intercropping tomatoes with sainfoin, Onobrychis viciifolia (Scop. 1771) significantly disrupting pest colonization and enhacing predators (O. niger and N. tenuis) activytity. O. viciifolia also provides resources to these predaotrs. Additonaly intercropping boosts soil fertility, leading to higher crop yields.

9. Conclusions and Future Perspectives

This review highlights the importance of adopting IPM strategies to control P. absoluta. Effective management involves combining multiple methods such as biological control agents, including parasitoids and predators, with the strategic use of pheromone traps and cultural practices like intercropping and crop rotation. Combining these methods offers the best long-term results for pest control, minimizing the need for chemical pesticides and promoting sustainable agricultural practices. However, the variability in pest control effectiveness based on environmental conditions, pest populations, and ecological factors calls for continued refinement and local adaptation of these techniques. The ongoing development of novel approaches, including CRISPR/Cas9 and plant-mediated RNAi as genetic-based solutions, holds great potential for the future of pest management. Future field trials for P. absoluta management will focus on integrating RNAi with traditional methods, enhancing pheromone traps, and exploring ecological interactions and cultural practices like intercropping.