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Review

Unleashing Nature’s Pesticide: A Systematic Review of Schinus molle Essential Oil’s Biopesticidal Potential

by
Laura Scalvenzi
1,*,
Andrea Durofil
2,
Carlos Cáceres Claros
3,
Amaury Pérez Martínez
1,
Estela Guardado Yordi
1,
Stefano Manfredini
4,
Erika Baldini
4,
Silvia Vertuani
4 and
Matteo Radice
1
1
Campus Puyo, Universidad Estatal Amazónica, Km 2 ½ Via Puyo-Tena, Puyo 160150, Ecuador
2
Ambrosialab, Via Mortara 171, 44121 Ferrara, Italy
3
Faculty of Agricultural Sciences, Universidad Mayor Real y Pontificia de San Francisco Xavier de Chuquisaca, Sucre 212, Bolivia
4
Department of Life Sciences and Biotechnology, University of Ferrara, 44121 Ferrara, Italy
*
Author to whom correspondence should be addressed.
Sustainability 2024, 16(23), 10444; https://doi.org/10.3390/su162310444
Submission received: 15 October 2024 / Revised: 14 November 2024 / Accepted: 21 November 2024 / Published: 28 November 2024
(This article belongs to the Section Sustainable Agriculture)
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Abstract

:
The past decade has witnessed an increase in scientific publications investigating the potential of essential oils as alternatives to synthetic pesticides for the control of plant and animal pests and disease vectors. The essential oil of Schinus molle has been the subject of various studies aimed at describing its insecticidal, acaricidal, and repellent properties. S. molle, although native to South America, is also widely distributed in countries bordering the Mediterranean. The objective of this systematic review was to analyze existing information on S. molle essential oil as a raw material for novel biopesticides and nanobiopesticides. We searched articles from PubMed, Scopus, and MDPI databases, and from 194 reports, we critically selected 33 articles produced between 2005 and 2024, representing all of the studies that aimed to evaluate the properties of the essential oil of this species as an insecticide, acaricide, and pesticide. The chemical composition varies significantly depending on origin, although two chemotypes associated with α-phellandrene and limonene appear to emerge. Data on adulticide activity and repellency are promising, and there are preliminary studies of microencapsulated forms of the essential oil that represent contemporary research trends currently under investigation. Furthermore, S. molle essential oil appears to demonstrate acetylcholinesterase inhibition effects that warrant further investigation. Finally, in this review, we have highlighted the potential of S. molle essential oil as a biopesticide, emphasizing the need to progress from a preliminary study phase to research conducted in application contexts. The conclusions of this review indicate future research trends aimed at the development of commercial products for organic and regenerative agriculture.

1. Introduction

The increasing global population exerts pressure on the food supply chain to enhance agro-industrial production, resulting in the extensive utilization of synthetic pesticides, which are essential for pest control, food loss mitigation, and stored product protection [1]. Furthermore, synthetic pesticides play a crucial role in controlling insects that serve as disease vectors affecting humans and animals [2]. However, the application of substantial quantities of synthetic pesticides over decades has been responsible for severe impacts on human health and has precipitated environmental crises in numerous countries [3,4]. The control of insects, mites, and other parasites is a fundamental activity in both the agricultural sector and as a public health measure. In both contexts, however, the ability of pests to develop resistance to synthetic pesticides has been highlighted, necessitating continuous research for new active molecules and control strategies [5,6,7]. To address current environmental and human concerns globally, the United Nations has promoted 17 Sustainable Development Goals (SDGs) which all countries should aim to achieve by 2050. SDG 2 focuses on the following objective: “End hunger, achieve food security and improved nutrition and promote sustainable agriculture”. From this perspective, organic agriculture should be encouraged to partially replace traditional agriculture, which is characterized by high inputs of synthetic pesticides and fertilizers [8,9]. Furthermore, crops for biofuel production have led to an increase in pesticide use, necessitating new strategies to achieve SDG 2 [10]. Additionally, reducing the use, risk, and dependence on synthetic pesticides in agriculture is one of the objectives set out in the ‘Farm to Fork’ strategy, one of the cornerstones of The European Green Deal, the plan for Europe to become the first climate-neutral continent by 2050 [11]. In this context, the development of plant-based insecticides, eco-friendly repellents, and acaricides represents an increasingly significant research trend, although further studies are required. Essential oils, plant extracts, and selected molecules from plants frequently demonstrate promising data regarding their biological activity and concurrently exhibit low toxicity for humans and other animals, high biodegradability, and a reduced environmental impact [12,13,14,15,16]. Essential oils (EOs) are oily, hydrophobic, and highly volatile liquids that may be extracted from various plant parts. EOs have been classified as secondary metabolites and play a crucial role in plants due to their repellent activity against herbivorous pests, as well as their attraction of pollinating species, antioxidant properties, and allelopathic activity [17,18]. Three biosynthetic pathways enable the production of EOs: sesquiterpenes derived from the mevalonate pathway, mono- and diterpenes from the methyl-erithrytol pathway, and the shikimic acid pathway, which leads to phenylpropenes [19]. Schinus molle L. (Figure 1) belongs to the Anacardiaceae family, known as “false” pepper and named as “aguaribay”, “pink pepper”, “pepper tree”, “Peru tree”, “molle”, “Californian pepper”, “Peruvian mastic”, “aroeira branca”, “aroeira-salsa”, “molho”, “pirú”, “yag lachi ntaka”, and “copalquahuitl” [20,21,22,23,24]. S. molle has monopodial growth habits and is a dioecious tree with aromatic leaves, which may be covered by sticky substances. The trunk is woody and incised; whitish latex flows from resiniferous canals. The flowers are panicle-arranged and unisexual, with an open corolla with 5 oval, oblong, downward slanting petals. The fruits are pink or red globose drupes, with a sweet taste, slightly pungent, and an epicarp that is dehiscent when dry [25]. S. molle is native to the American tropics but is common as a spice and ornamental plant in several countries in the Mediterranean area and Southern Europe [26]. Several ethnobotanical uses have been reported for S. molle due to its wound-healing, antibacterial, antifungal, analgesic, topical antiseptic, diuretic, antiviral, and antidepressant properties [26,27]. In Ethiopia, it has been traditionally cultivated in gardens as an insect repellent [28], while researchers from Brazil, Chile, and Ecuador have reported the insecticidal activity of the EO against Aedes aegypti and Musca domestica [20,22,24]. Based on these preliminary findings, the aim of the present systematic review was to elucidate the state of the art of the pesticide activity of S. molle EO and provide a novel perspective and research strategies on plant-based biopesticides.

2. Research Strategy

The present systematic review was carried out using the Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) methodology [29]. The data mining process was performed by selecting articles from the following scientific databases: PubMed (https://pubmed.ncbi.nlm.nih.gov/, accessed on 1 June 2024), Scopus (https://www.scopus.com/, accessed on 1 June 2024), and MDPI (https://www.mdpi.com/, accessed on 1 June 2024). Three researchers extracted data independently, avoiding duplicate data. The bibliographical references were managed using Mendeley software online. The following key words were searched alone and in combination: “Schinus molle essential oil”, “insecticidal”, and “pesticide”. The authors decided to consider the literature published in English without limitations on the year of publication. Data from patents, symposiums, and congress abstracts were excluded. Articles that reported the keywords in the title and/or in the abstract sections were considered, while articles which referred to the review topic as secondary were avoided. The selected articles were analyzed and grouped into 5 tables.
The data mining and article selection processes are summarized in a flowchart (Figure 2). Tables were organized in order to address the following information: (a) the country where the research was performed; (b) the part of the plant used for the extraction; (c) the extraction method; (d) the main compounds of the S. molle EO; (e) the kind of assay reported in the study; (f) the pest involved in the study; (g) the type of pesticide activity reported; (h) references. As reported in Figure 2, by adopting the above-mentioned inclusion and exclusion criteria, it was possible to select 33 eligible articles.

3. Results

3.1. Aim of Selected Studies and Geographical Distribution

Based on the aforementioned criteria, 33 papers explicitly addressing the potential of S. molle EO in pest management as the primary research focus were identified. These studies encompass crop protection (14 articles), veterinary applications (5 articles), control of active and passive disease vectors (8 articles), and behavioral response investigations (3 articles). We also considered those nanotechnology systems which use essential oils (3 articles). It is noteworthy that two studies related to veterinary applications and one pertaining to crop protection utilized advanced formulations of S. molle EO, employing microencapsulation techniques. Figure 3 presents further details.
According to the selection criteria, we counted eight articles from Argentina and this country seems to lead the research interest in S. molle EO as a potential biopesticide. Both Brazil and Egypt have been reported to have four articles, followed by Ecuador (three articles), Chile, Peru, Saudi Arabia, Tunisia, and Turkey (two articles), and Algeria, Ethiopia, Mexico, and Morocco (one article), as shown in Figure 4. Most of the studies were carried out in Latin American countries. In fact, the plant is native to that continent, and it may explain the prevalence of the studies in South America. The species has then spread to North Africa and other regions in the world.
Figure 5 shows the time distribution of the selected studies, indicating a time span between 2005 and 2024. With eight and five articles respectively, 2022 and 2017 were the years of highest scientific production in relation to the fields of this study.

3.2. Biopesticide Activity of S. molle EO in Crop Protection

The use of EOs as biopesticides represents a promising area of phytochemical research, and there is a substantial body of scientific research that has reported encouraging data. EOs have been investigated to elucidate their repellent, antifeedant, oviposition deterrent, insecticidal, and growth-regulating effects on crop pests. These findings may facilitate the development of novel bio-based control strategies, particularly in the context of organic farming [30,31]. Despite their proven efficacy, the excessive application of synthetic pesticides has highlighted issues related to water and soil pollution, adverse effects on human and animal health, and the emergence of pest resistance, necessitating the development of alternative intervention strategies [32,33]. A pivotal role in biopesticide research has been played by the interaction of EOs and herbal extracts with octopamine and acetylcholinesterase pathways. EOs may influence the metabolism of insect pests by disrupting the function of the aforementioned molecules, causing irreversible damage to neurotransmission and neuromuscular functions [34]. EOs may interfere with insect body functions following absorption through the integument or via ingestion, inducing malformations, reduced fertility, neurotoxic activity, and respiratory system alterations at various developmental stages [35].
A large part of the studies related to S. molle EO were carried out against pest insects, mostly belonging to Coleoptera, Lepidoptera, and Hemiptera orders; just one study was performed on an arachnid (Tetranychus urticae).
The primary extraction methodology employed was hydro distillation, with leaves being the most frequently utilized plant parts. Extensive data exist regarding the chemical composition of the oil, and the presence of certain molecules appears to be recurrent in samples from diverse geographical regions and countries. The most prevalent compounds are α-phellandrene and limonene, followed by β-phellandrene and p-cymene. The insecticidal effect of α-phellandrene has been previously reported by various researchers [36,37], and although the activities of EOs can generally be attributed to a synergistic effect of the components, the aforementioned studies support the hypothesis of a potential role of α-phellandrene in the biopesticide activity of S. molle EO. As reported by Feng and Ibáñez et al. [38,39], limonene is listed as a potential alternative to synthetic pesticides and herbicides and a promising bio-based ingredient in food preservation. In both studies, encapsulation techniques facilitate improved solubility in aqueous systems and enhanced efficacy, promoting controlled release. Regarding p-cymene, Balahbib et al. [40] has identified that it is a significant intermediate for numerous industrial syntheses, including conventional pesticides. However, for this monoterpene and β-phellandrene, no studies have been conducted concerning their potential as biopesticides. It is noteworthy that preliminary data on the biopesticidal activity of individual molecules represent an initial step in potential application development, as laboratory conditions differ substantially from those encountered in the field or at food storage sites. In the case of limonene, previous studies have demonstrated greater insecticidal efficacy of the EO as a whole compared to the individual molecule [39]. Consequently, evaluations regarding the chemotype of different varieties of S. molle EO necessitate further scientific investigation. The variety of pests examined encompasses a wide range of harmful organisms affecting agricultural production and foodstuffs at various stages of the production chain. Pronounced adulticidal and repellent activity is evident across the spectrum, accompanied by promising preliminary data on certain insect developmental stages (eggs, nymphs, and larvae) and effects such as potent feeding deterrent action. Data on biological activity are encouraging but difficult to compare because they were obtained from different species and by using a wide range of methodologies and types of applications (contact, immersion, fumigation, ingestion, etc.). Biopesticide activities were expressed by various tests, including repellency and mortality, at different development stages of pests (from egg hatching inhibition to adulticide activity) and showed promising data at different dosages and with different contact methods. The findings shown in Table 1 confirm the potential of S. molle EO as a biopesticide and draw further lines of research, taking into account its major components or specific chemotypes from different geographical areas.

3.3. Biopesticide Activity of S. molle EO for Veterinary Application

Parasite control in farm animals is essential for both animal welfare and production. In cattle production, for instance, ticks serve as the primary vector for pathogens and negatively impact skin quality, milk production, and overall animal mortality. The economic losses associated with parasitic infestations are estimated to be in the order of billions of dollars annually. EOs may present a promising alternative, primarily due to their target selectivity, as they can act on octopaminergic and acetylcholinesterase receptors, which are prevalent in arthropods but not in mammals [13,52]. Despite preliminary promising data, including veterinary applications, EOs require further research to develop new commercial products. Major limitations include the scarcity of efficacy information, a lack of standardization in biological activity tests, and challenges in scaling up production to reach enough quantities at competitive costs.
Data on S. molle EO activity of veterinary interest primarily focused on acaricide activity (Ixodida and Trombidiformes orders). Information regarding the chemical composition of EO and other extraction parameters (distillation method and botanical part used) warrants further investigation, as studies remain limited. Notably, the research conducted on Varroa destructor by Ruffinengo et al. [53] reported an adulticide activity at 24 h with an LD50 = 2.7 µL/mg. The findings of Rey-Valeirón et al. [24] are also significant due to the pronounced activity of the EO on Rhipicephalus sanguineus which surpasses that of the positive control cypermethrin. The results presented in Table 2 suggest potential avenues for further research in the biological control of bee parasites and the development of plant-based products for livestock and companion animals.

3.4. Biopesticide Activity of S. molle EO as a Tool Against Active and Passive Vectors of Diseases

Aedes-borne viruses (Chikungunya, yellow fever, dengue, Zika) and malaria afflict vast tropical areas in Africa, Asia, Latin America, and the Caribbean, posing a global health threat [57,58,59,60].
Additionally, global warming and other factors, such as population movement, urbanization, and global trade, appear to facilitate the expansion of vector-borne diseases into regions traditionally less susceptible to these risks [61,62,63,64,65]. According to Roiz et al. [66], the proliferation of the arbovirus vectors Aedes aegypti and Aedes albopictus presents not only a public health concern but also a significant economic impact. The authors analyzed data from 166 countries and territories over a 45-year period, identifying an estimated health cost of USD 94.7 billion, due to diseases caused or transmitted by the previous mentioned vectors. This figure is likely an underestimate, emphasizing the necessity of implementing public policies aimed at mitigating the spread of arbovirus vectors. As noted for pest management in crop production, synthetic pesticides represent a conventional strategy to control vector-borne diseases; however, they exhibit adverse health and environmental effects that require evaluation and monitoring [67,68]. Furthermore, synthetic larvicides induce resistance in certain mosquito species such as A. aegypti, Culex pipiens, and Anopheles stephensi [69]. Substantial scientific evidence demonstrates the efficacy of EOs and herbal extracts against major vectors of tropical diseases, particularly in the case of A. aegypti, arguably the most significant vector of arboviral diseases. The mechanism of action can be primarily described as larvicidal activity, which involves the alteration of insect morphogenesis, and in some instances, 100% larval mortality has been reported at 48 h [70,71]. As noted by Luz et al. [72], a review of the scientific literature related to 225 plant species indicated that more than 60% of tested EOs were capable of inducing toxicity against A. aegypti. These findings suggest that EOs and natural products may be considered a crucial factor in developing new strategies against arboviral diseases.
The hydro distillation methodology was predominantly reported as the primary method, and leaves were identified as the most frequently utilized plant component. α-phellandrene and β-phellandrene were cited as principal compounds in two instances; however, data from the sole in silico study indicated α-muurolene, γ-cadinene, and β-cadinene as the primary active compounds, underscoring the significance of investigating the correlation between the chemical composition and biological activity of EOs. S. molle EO was evaluated twice against A. aegypti and C. pipiens; however, only seven studies were conducted on vector-borne disease topics. Considering the data presented in Table 3, further scientific investigation is warranted. The studies performed by Massebo et al. [73] highlighted larvicide activity against A. aegypti with LD50 (at 24 h) values of 9.6 ppm and 14.5 ppm for leaves and seeds, respectively. Also, data reported by Abdelgaleil et al. [74] (LC50 = 12.8 mg/L) may be considered an interesting starting point for the control of C. pipiens. The study conducted by De Oliveira et al. [75] suggests a promising route for research exploring the synergistic effects between EOs and entomopathogenic fungi as a potential alternative to synthetic pesticides in biological control strategies. Metarhizium anisopliae and S. molle EO demonstrated a synergistic larvicidal effect, resulting in only 2% survival of mosquitoes. The data presented in Table 3 are insufficient to draw definitive conclusions regarding the efficacy of S. molle EO in the treatment of arbovirus vectors and other tropical diseases; nevertheless, this area of research has produced intriguing preliminary results and warrants further investigation.

3.5. Development of Nanobiopesticides

Despite the ever-increasing scientific production, the development and diffusion of eco-friendly repellents and biopesticides based on EOs, compared with the corresponding synthetic products, is still limited. Several factors limit the development of plant-based products, primarily including reduced efficacy duration at equivalent dosages, high volatility, and variability in chemical composition. Furthermore, although EOs are products of natural origin already widely used in other commercial sectors (cosmetics, food, detergent, etc.), specific studies pertaining to toxicity and environmental impact are essential and cannot be circumvented [80].
In this context, the development of formulations that enhance the stability and persistence of the product directly influences the efficacy, release control, and competitiveness of plant-based products, and nanotechnologies may offer a promising alternative [81]. Several studies have focused on the application of nanotechnology in pest and vector management, coining the term “nanobiopesticides” [35,82,83]. One definition of nanotechnology cited by the FDA [84] refers to the National Nanotechnology Initiative Program and states that “Nanotechnology is the understanding and control of matter at the nanoscale, at dimensions between approximately 1 and 100 nanometers, where unique phenomena enable novel applications”. In accordance with this definition, nanobiopesticides are generally considered plant-derived products with pesticidal activity (plant extracts, EOs, single molecules of plant origin, etc.) that can be incorporated into organic or inorganic systems that facilitate the development of nanoparticles, nanoemulsions, or nanocapsules. The commercial development of nanobiopesticides still necessitates studies related to various aspects concerning efficacy (field application, greenhouse, etc.) and environmental impact (non-target organisms, environmental persistence), rendering it premature to define the regulatory aspects that would facilitate their authorization and marketing [23]. Considering that the Farm to Fork strategy mandates the reduction in synthetic pesticides [85], the frontier of nanotechnologies in the context of parasite control and borne-disease vector management remains a promising area of research with significant potential for future applications, particularly because preliminary data suggest greater efficacy, reduced dosage requirements, controlled release, and the possibility of utilizing ingredients (extracts, biopolymers, etc.) generally recognized as safe.
Data regarding the utilization of S. molle EO in nanoformulations are promising but limited (three articles) (Table 4). Consequently, it was not feasible to identify trends related to extraction techniques or chemical composition. Regarding pesticide activity, the study conducted by Sánchez et al. [56] emphasized that research relating to insect mortality requires further investigation. In the case of Macrosiphum euphorbiae (aphid), the lethality of the microencapsulated S. molle EO appeared to be lower than the value obtained in other studies conducted with direct contact. This finding appears to contradict those obtained from other studies of microencapsulated EO; however, the authors posited that controlled release could explain the lower efficacy in the short time frame (24 h) but greater persistence in the context in which the oil was applied. Furthermore, the powdery consistency of the microencapsulated oil should facilitate greater adhesion to certain anatomical parts of aphids, such as legs and antennae. The hypothesis of controlled release involving long-term insecticidal activity, with lower efficacy in the short term but higher persistence in the studied system, also appears to be corroborated by the study of López [86]. In this instance, the mortality of Haematobia irritans exposed to pure S. molle EO was 96% after 2 h, while microencapsulated EO exhibited 36% mortality at the same time exposure. However, the microencapsulated system may retain 71% of EO after 366 h, preventing rapid EO evaporation. Microencapsulated S. molle EO can therefore persist for a longer duration in the application zone, allowing for a more sustained pesticidal effect.
Finally, the study by Ruffinengo [87] indicated that microencapsulated S. molle EO may be applied as a biological treatment to protect bees (Apis mellifera) from the parasite Varroa destructor. Preliminary data showed low insecticidal activity against the parasite but also a marked attractive effect. Considering the low toxicity toward bees, further studies could be directed to the development of selective “biological traps” to be tested for biological control of V. destructor in the context of beekeeping.
Thus, the complexity of studies on the biocidal activity of nanobiopesticides is evident and clearly requires further repetition and articulated experimental protocols. However, this line of research seems essential to overcome some limitations in the direct application of oils for insect control.

3.6. Behavioral and Antennal Responses of Pest Insects to Volatile Compounds from S. molle EO

Integrated pest management is not solely resolved in the repellent, larvicidal, or insecticidal effect of synthetic or naturally occurring molecules. The development of diversified strategies to protect foodstuffs or limit tropical disease vectors requires complementary interventions that include pheromone traps, light traps, push–pull agricultural technology, crop rotation, etc. [88,89,90,91,92]. Fruit extracts, EO and their pure compounds play a pivotal role in many interactions between plants and insects, stimulating the scientific community to study the behavioral and antennal responses of pest insect to volatile compounds. The repellent or attractant effects and the mating disrupting activity have been investigated by numerous researchers to identify biochemical-based mechanisms potentially useful for the development of novel trap strategies [93,94,95,96]. In this context, studies utilizing olfactometer bioassays have been conducted in two countries employing S. molle EO, with preliminary results presented in Table 5.
In contrast with the previous tables, the data available on behavioral and antennal responses of pest insects were not sufficient to establish relationships and assess an exhaustive discussion.
The research carried out by Silva et al. [96] showed the attractive effect of EOs S. molle on Lobesia botrana, a common grapevine pest, varying from 1 × 103 to 1 × 104 μg mL−1 for the female and male, respectively. This discovery deserves further study in order to identify S. molle as a potential producer of non-host plant volatiles (NHPVs) and propose the presence of the species in the proximity of vine rows as a tool for an integrated pest control strategy. Plants producing NHPVs interfere with the olfactory processes of phytophagous insects, inducing repellent, attractive, or masking effects which influence the life cycle of the insects themselves, egg-laying, reproductive behavior, and feeding. A similar study conducted by Kasmi [97] on the pea crop pest Acyrthosiphon pisum yielded conflicting data. EO from leaves of S. molle showed no attractive effects, while the oil obtained from fruits did. Again, the study highlighted how the chemical composition of the oil according to different anatomical parts, its chemotype, and context conditions were crucial to understanding plant–insect interactions. According to both studies reported in Table 5, S. molle EO from leaves and fruits caused grapevine moth (L. botrana) and aphid (A. pisum) to respond positively in terms of being attracted by the volatile compounds. For these reasons, both EOs should be investigated for the development of chemical traps for organic pest control. Nonetheless, the authors mentioned that further studies, such as antenna electrography coupled with GC/MS, are essential to consolidate these preliminary data.
Table 5. Data on the activity of S. molle EO regarding the behavioral and antennal responses of pest insects.
Table 5. Data on the activity of S. molle EO regarding the behavioral and antennal responses of pest insects.
CountryPartExtractionMain CompoundApplicationPest (Target)Biological ActivityRef
AlgeriaAPHDβ-phellandrene (25.1%),
α-phellandrene (16.0%), and
p-cymene (10.9%)		Fumigation and Repellency/Attractivity assaySitophilus zeamais
(Col.: Curculionidae)		Adulticide (LC50 = 170.1 μL/L). Repellency (at 17.9 and 23.9 μL/L). Attractivity (at 1.19 and 2.39 μL/L).[98]
ChileLHDLimonene (17.6%),
α-phellandrene (14.3%), and
δ-cadinene (9.4%)		Olfactometer bioassayLobesia botrana (Lep.: Tortricidae)Positive behavioral response at
1 × 103 µg/mL (female) and
1 × 104 µg/mL (male).		[96]
TunisiaFHD6-epi-shyobunol (16.2%), Spathulenol (8.2%), and 4-epi-Cubebol (7.8%)Olfactometer bioassayAcyrthosiphon pisum
(Hem.: Aphididae)		Positive response (significant).[99]
Lβ-eudesmol (14.8%), Elemol (13.7%), and
α-Eudesmol (12.8%)		Negative response
(not significant).
AP—aerial part; L—leaf; F—fruit; HD—hydro distillation.

4. Discussion

4.1. Mode of Action of EOs in Biopesticide Activity: Preliminary Findings Concerning S. molle EO

The phenomenon of resistance to synthetic insecticides is dependent on the continuous overexpression of detoxifying enzymes. Pests consistently develop pronounced overexpression of enzymes, partly due to the presence of their intestinal bacteria. This abundance of biochemical alternatives results in metabolic resistance and detoxification of common pesticides [100]. As reported by Senthil-Nathan [98], EOs appear to inhibit the detoxifying enzymes of pests, offering a plant-based alternative against common pesticide resistance.
The activity of EOs toward insects and mites involves multiple mechanisms of action which are contingent upon the method of application and the various receptors present on the animals. In cases of direct contact and ingestion, the scientific literature has primarily investigated neurotoxic effects, considering the inhibitory action of acetylcholinesterase enzyme (AChE) as the principal mechanism of action. The inhibition of AChE induces postsynaptic overstimulation, resulting in paralysis and death of the insect. Several studies have identified that EOs and their components selectively interfere with the insect cholinergic system, thus exhibiting significantly lower toxicity to mammals [16,101]. Other mechanisms of action of EOs involve the inhibition of cytochromes P450 and interference effects on the octopamine system, the synapse mediated by GABA, and Na-K-ATPase or Na+ and K+ channels [69,80]. Comparable conclusions can be drawn for the acaricidal effect of EOs; similar research has highlighted how the presence of monoterpenes can yield promising results in the case of mites resistant to common synthetic pesticides. S. molle EO was able to exert promising acaricidal effects against Rhipicephalus sanguineus, even better than the positive control cypermethrin [102]. As reported by De Souza et al. [44], S. molle EO showed considerable acetylcholinesterase inhibition (IC50 = 0.047 mg/mL), also compared with carvacrol as the standard (IC50 = 0.029 mg/mL). A study performed by Aboalhaija et al. [26] on S. molle EO from leaves exhibited moderate AChE inhibition activity compared to the positive control (Tacrine). Despite extensive studies were conducted on S. molle EO as a biopesticide, data elucidating its mechanism of action must be further investigated.

4.2. Product Development, Feasibility, Scalability, and Technology Readiness Level (TRL) Trends

Despite the extensive scientific literature dedicated to the potential of EOs as biopesticides, the development and commercialization of products on a large scale remains a significant challenge. There are issues of both a technical–scientific and regulatory–commercial nature. EOs typically demonstrate in vitro efficacy at low concentrations, comparable to those obtained from synthetic pesticides. Their persistence is reduced due to their higher volatility, and their lipidic nature presents challenges for dispersion in aqueous systems. The reduced persistence diminishes their efficacy in some cases, necessitating more frequent treatments, but simultaneously reduces their adverse effects on ecosystems [23,82]. The variability in chemotypes and differences in composition common to crop production also complicate the standardization of formulations. Notwithstanding the aforementioned challenges, particularly considering the application of microencapsulation and nanoemulsion techniques, the data reported in this study are encouraging regarding the feasibility of developing biopesticides based on S. molle EO. According to Arnouts et al. and Héder et al. [103,104], the Technology Readiness Levels approach (TRLs) may facilitate the development of novel research strategies and public policies that focus on the maturity level of a technology. This approach involves nine technology readiness levels (from TRL1 to TRL9) which may describe the development trajectory of a technology, from basic findings to proven successful results in a commercial environment. The TRL 1–TRL 4 range has been associated with laboratory-scale development; from TRL 5 to TRL 7, the technology is validated at a pilot scale which can confirm preliminary “in vitro” results, while the TRL 8–TRL 9 scale certifies full technology development which may be proposed for commercial development. Based on this concept, all of the selected articles in the present review should be classified in a range between TRL 1 and TRL 4 level, which is defined as preliminary research laboratory validation. These data are quite common for EO research; however, S. molle EO warrants further research focused on “in-field” studies and prototypes that require validation in an operational environment. In light of the results presented in this study, S. molle EO could yield scalable results in terms of TRLs with subsequent microencapsulation studies, considering the study presented in Table 4 concerning spray-drying technology.

4.3. Critical Assessments of Papers Reviewed

A critical assessment of the selected articles facilitated the identification of potential research gaps and the proposal of new trends. The evaluation was conducted according to the following criteria: (a) Is the article explicit about the purpose of the study? (b) Are the materials and methods clearly, reproducibly, and comprehensively described? (c) Is the chemical characterization of the S. molle EO comprehensive? (d) Are the biological activity data exhaustive and do they encourage further studies on S. molle EO? (e) Are there prerequisites for the development of biopesticides or industrial products to control pests in the selected areas? Are the results scalable within the TRL approach?
All of the selected articles comply with points (a) and (b); however, a minority do not report the composition of the EO (point c). Although this was not considered an exclusion criterion in the present review, it is strongly recommended that subsequent studies further investigate this information, also with a view to identifying any particularly bioactive chemotypes. The biological activity data set is robust, consistent, and diverse (point d), and the description of the methods is comprehensive and allows for their reproducibility. Of particular relevance are the studies shown in Table 4, as they represent the initial results aimed at enhancing oil activity with nanotechnology, a trend that appears to be decisive for the future application of biopesticides on a large scale. Lastly, in relation to point (e), the presence of laboratory studies traceable to a TRL between 1 and 4 is noted; however, no research extends to trials in more extensive application contexts, which are more significant for simulating potential application areas (e.g., greenhouses, crops, food storage areas, areas of potential development of larvae or disease vector insects, etc.). As a final assessment, despite the substantial initial base of data on insecticidal/acaricidal and repellent activity, the selected articles collectively highlight the need to address certain gaps related to biological activity and scalability. Nevertheless, there exists a solid foundation for further studies and the development of research aimed at increasing TRLs.

5. Conclusions

The species S. molle has shown potential as a novel biopesticide, with numerous studies investigating its larvicidal, repellent, insecticidal, and acaricidal activities. The authors aim to focus on the potential applications of this EO and highlight the need for further research to fully understand its bioactivity. This paper calls for more extensive studies on S. molle EO, particularly as a potential novel biopesticide or nanobiopesticide.
In this regard, the following approaches could be implemented: (1) collecting and systematizing data belonging to the most prevalent and bioactive chemotypes; (2) designing new studies to verify larvicidal, repellent, insecticidal, and acaricidal activity in an industrially relevant environment (e.g., food storage) or in contexts with a widespread presence of vector-borne diseases; (3) expanding existing studies on acetylcholinesterase inhibition and other potential neurotoxic effects on insects and mites; (4) enhancing formulation studies concerning nanobiopesticides; (5) promoting further research into the behavioral and antennal responses to S. molle EO with the aim of developing traps suitable for organic and regenerative agriculture.

Author Contributions

Conceptualization, L.S. and M.R.; methodology, A.D., M.R., S.M. and A.P.M.; writing—original draft preparation, L.S., M.R., S.V. and A.D.; writing—review and editing, L.S., M.R., E.G.Y., E.B., S.M. and C.C.C.; supervision, S.V., E.B., S.M. and M.R. All authors have read and agreed to the published version of the manuscript.

Funding

The APC was funded by the Universidad Estatal Amazónica, Ecuador. This research received no external funding.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

No new data were created in this study.

Acknowledgments

This research was supported by the Universidad Estatal Amazónica (Ecuador Republic).

Conflicts of Interest

The author Andrea Durofil is a collaborator of Ambrosialab S.r.l., an accredited Spinoff of the University of Ferrara. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as potential conflicts of interest.

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Figure 1. Front view of Schinus molle tree in urban context (figure by authors).
Figure 1. Front view of Schinus molle tree in urban context (figure by authors).
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Figure 2. Flowchart of review process.
Figure 2. Flowchart of review process.
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Figure 3. The percentage distribution of the focus of the topics in the selected articles.
Figure 3. The percentage distribution of the focus of the topics in the selected articles.
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Figure 4. Geographical distribution of selected articles.
Figure 4. Geographical distribution of selected articles.
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Figure 5. Chronological distribution of selected studies.
Figure 5. Chronological distribution of selected studies.
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Table 1. Data on the activity of S. molle EO as a biopesticide for crop protection.
Table 1. Data on the activity of S. molle EO as a biopesticide for crop protection.
CountryPartExtractionMain CompoundApplicationPestBiopesticide ActivityRef
ArgentinaLHDlimonene (15.7%);
α-phellandrene (13.8%);
elmol (9.0%).		Contact (contaminated surface), Fumigation, Topical, Repellency assayRhizopertha dominica
(Col.: Bostrichidae)		Adulticide (contact: LC50 = 41.2 mg/cm2; fumigation: LC50 = 0.6 mg/cm2; topical: LC50 = 0.88 mg/cm2). Repellency rate (at 1 h 67% at 120.0 μg/cm2).[41]
Flimonene (40.3%);
α-phellandrene (24.5%);
β-myrcene (16.3%).		Adulticide (contact: LC50 = 236.4 mg/cm2; fumigation: LC50 = 0.8 mg/cm2; topical: LC50 = 8.88 mg/cm2). Repellency rate (at 1 h 67% at 120.0 μg/cm2).
ArgentinaFSDlimonene (40.3%);
α-phellandrene (24.5%);
β-myrcene (16.4%).		Repellency/Attractivity assay, and antifeeding activity, Fumigant activitySitophilus oryzae
(Col.: Curculionidae)		Strong feeding deterrent action (62%).[42]
LSDlimonene (15.7%);
α-phellandrene (13.8%);
elmol (9.0%).		Repellent effects
(0.04 and 0.4% w/w).
Fumigant activity (not toxic).
BrazilLSDα-pinene (60.0%);
limonene (11.3%);
β-pinene (9.2%).		IngestionAnticarsia gemmatalis (Lep.: Erebidae)Larvicide (at 24 h 30.0% at 2.0% v/v).[43]
Braziln.r.HDlimonene (25.6%);
bycyclogermacrene (22.9%);
sabinene (19.7%).		ContactDrosophila suzukii
(Dip.: Drosophilidae)		Adulticide (at 24 h LC50 = 19.3 µL/mL and LC95 = 518.5 µL/mL).[44]
ChileFSDβ-pinene (15.4%);
α-phellandrene (15.0%);
p-cymene (10.9%).		Contact, Repellency assaySitophilus zeamais
(Col.: Curculionidae)		Adulticide (LC50 = 38.2 mL/kg and LC90 = 91.0 mL/kg). Repellency rate (70% at 4% v/m).[20]
EcuadorLSDBicycloelemene (n.r);
trans-caryophyllene (n.r);
bicyclogermacrene (n.r).		ImmersionPremnotrypes vorax
(Col.: Curculionidae)		Egg eclosion inhibition (at 24 h 47.5% at 5% m/v).
Larvicide (at 48 h 25% at 10% m/v).
Adulticide (at 24 h 25% at 10% m/v).		[45]
EgyptLHDα-phellandrene (29.9%);
β-phellandrene (21.1%);
elemol (13.0%).		FumigationTribolium confusum
(Col.: Tenebrionidae) 		Egg toxicity (at 7 days LC50 = 2.22 µL/L). Larvicide (at 7 days 55.1 µL/L). Adulticide (at 24 h LC50 = 46.9 µL/L).[46]
EgyptLHDα-phellandrene (29.8%);
β-phellandrene (21.1%).		IngestionAphis nerii (Hem.: Aphididae)Adulticide (at 24 h LC50 = 0.12 mg/L and LC95 = 3.28 mg/L).[47]
MexicoLHDo-cymene (29.0%);
α-pinene (15.5%);
camphene (14.0%).		IngestionBactericera cockerelli
(Hem.: Triozidae)		Nymphicide (at 24 h 4th-instar LC50 = 329.4 ppm, LC90 = 662.3 ppm and 5th-instar LC50 523.8 ppm, LC90 = 1029.9 ppm).[48]
Sitophilus zeamais
(Col.: Curculionidae)		Adulticide (at 5th day LC50 = 781.5 ppm and LC90 = 1641.3 ppm).
MoroccoFHDlimonene (23.2%);
spathulenol (14.3%);
β-ocimene (13.3%).		Contact, Fumigation, Repellency assaySitophilus oryzae
(Col.: Curculionidae)		Adulticide (contact: at 24 h LC50 = 50.0 μL/cm2; fumigation: at 8 days 50% mortality at 5 μL/L). Repellency rate (30% at 150 µL/cm2).[21]
LHDlimonene (18.5%);
longifolene (8.5%);
γ-terpinene (8.2%).		Adulticide (contact: at 24 h LC50 = 100.0 μL/cm2; fumigation: at 8 days 75% mortality at 5 μL/L). Repellency rate (30% at 150 µL/cm2).
Saudi ArabiaFHDp-cymene (32.8%);
β-pinene (19.0%);
α-terpinene (18.3%).		Topical, Repellency assayTribolium castaneum
(Col.: Tenebrionidae)		Adulticide (at 2 days 53.3% at 750.0 μL/mL). Repellency rate (73.6% at 750 μL/mL).[28]
TopicalTrogoderma granarium
(Col.: Dermestidae)		Adulticide (at 2 days 50% at 750.0 μL/mL).
LHDp-cymene (69.4%);
carvotanancetone (2.5%);
calamenene (2.3%).		TopicalTribolium castaneum
(Col.: Tenebrionidae)		Adulticide (at 2 days 50.0% at 750.0 μL/mL).
Topical, Repellency assayTrogoderma granarium
(Col.: Dermestidae)		Adulticide (at 2 days 46.7% at 750.0 μL/mL). Repellency rate (72.3% at 750 μL/mL).
TunisiaFHDα-phellandrene (20.4%);
limonene (17.7%);
t-muurolol (11.0%).		FumigationEctomyelois ceratoniae
(Lep.: Pyralidae)		Adulticide (at 24 h LC50 = 7.9 μL/L).[49]
Ephestia kuehniella
(Lep.: Pyralidae)		Adulticide (at 24 h LC50 = 170.7 μL/L). Egg hactchability (74.6% at 459.5 μL/L).
Lα-phellandrene (17.1%);
elemol (13.3%);
t-muurolol (13.2%).		FumigationEctomyelois ceratoniae
(Lep.: Pyralidae)		Adulticide (at 24 h LC50 = 176.5 μL/L).
TurkeyAPHDlimonene + β-phellandrene (13.7%);
elemol (11.6%);
p-cymene (9.6%).		FumigationTetranychus urticae
(Trom.: Tetranychidae)		Adulticide (at 96 h LC50 = 12.3 µL/L and LC90 = 36.8 µL/L).
Larvicide (at 96 h LC50 = 8.4% µL/L and LC90 = 16.1 µL/L).		[50]
USAn.r.SDn.r.IncubationRhynchophorus ferrugineus (Col.: Curculionidae)Cell mortality (at 24 h LC50 = 483.1 ppm).[51]
AP—aerial part; L—leaf; F—fruit; HD—hydro distillation; SD—steam distillation; n.r.—not reported.
Table 2. Data on the activity of S. molle EO for veterinary application.
Table 2. Data on the activity of S. molle EO for veterinary application.
CountryPartExtractionMain CompoundApplicationPestBiological ActivityRef
Argentinan.r.SDβ-phellandrene (28.3%);
α-phellandrene (11.5%); camphene (7.9%).		Contact
(contaminated surface)		Varroa destructor (Mes.: Varroidae)Adulticide (at 24 h LD50 = 2.7 µL/mg)[53]
ArgentinaF, L, BSDsabinene (51.0%);
β-pinene (11.2%);
α-pinene (9.5%).		Contact and IngestionVarroa destructor (Mes.: Varroidae)Efficiency: 11.3% mortality[54]
ArgentinaF, L, BSDsabinene (34.3%);
α-pinene (8.4%);
terpinen-4-ol (8.2%).		ImmersionRhipicephalus microplus
(Ixo.: Ixodidae)		Larvicide (LC50 = 4.4 µL/mL)[55]
EcuadorFHDp-cymene (40.0%);
limonene (19.5%);
myrcene (7.7%).		ContactRhipicephalus microplus
(Ixo.: Ixodidae)		Larvicide (at 24 h LC90 = 1.3% v/v)[56]
EcuadorFHDp-cymene (40.0%);
limonene (19.5%);
myrcene (7.7%).		ContactRhipicephalus sanguineus (Ixo.: Ixodidae)Larvicide (at 24 h LC50 = 0.2% v/v and LC90 = 0.8% v/v)[24]
B—branch; L—leaf; F—fruit; HD—hydro distillation; SD—steam distillation; n.r.—not reported.
Table 3. Data on the activity of S. molle EO as a potential tool against active and passive vectors of diseases.
Table 3. Data on the activity of S. molle EO as a potential tool against active and passive vectors of diseases.
CountryPartExtractionMain CompoundApplicationPestActivityRef
ArgentinaLHDn.rFumigationMusca domestica
(Dipt.: Muscidae)		Adulticide
(LC50 = 46.9 mg/dm3).		[76]
BrazilLHDsabinene and bicyclogermacreneInsecticidal activity in silico and in vitro
Contact		Aedes aegypti
(Dipt.: Culicidae)		Larvicide
(S50 (median survival time) =
1 day at 0.01% v/v).		[75]
BrazilLSDsylvestrene (27.1%),
myrcene (26.4%), and sabinene (20.8%)		ContactCulex quinquefasciatus
(Dipt.: Culicidae)		Larvicide
(at 24 h LC50 = 60.1 µg/mL).		[2]
EgyptLHDα-phellandrene (29.8%),
β-phellandrene (21.1%), and
elemol (13.0%)		ImmersionCulex pipiens
(Dipt.: Culicidae)		Comparative toxicity against all stages (LC50 = 12.8 mg/L).[74]
Egyptn.r.HDn.r.Contact, FumigationCulex pipiens
(Dipt.: Culicidae)		Larvicide
(at 24 h LC50 = 141.0 mg/L). Adulticide
(at 24 h LC50 = 6.92 mg/L).		[77]
EthiopiaLHDn.r.ContactAedes aegypti
(Dipt.: Culicidae)		Larvicide (at 24 h LC50 = 9.6 ppm; LC90 = 15.0 ppm).[73]
Anopheles arabiensis
(Dipt.: Culicidae)		Larvicide (at 24 h LC50 = 21.0 ppm; LC90 = 37.3 ppm).
SContactAedes aegypti
(Dipt.: Culicidae)		Larvicide (at 24 h LC50 = 14.5 ppm; LC90 = 28.5 ppm).
Anopheles arabiensis
(Dipt.: Culicidae)		Larvicide (at 24 h LC50 = 26.5 ppm; LC90 = 45.4 ppm).
PeruLHDα-phellandrene (32.7%),
D-limonene (12.6%), and
β-phellandrene (12.2%)		Insecticidal activity in silicoJuvenile hormone-binding protein (mJHBP) from Aedes aegypti
(Dipt.: Culicidae)		α-muurolene and γ-cadinene had the best biding energy on mJHBP (ΔG = −9:7 kcal/mol), followed by β-cadinene
(ΔG = −9:5 kcal/mol).		[78]
TurkeyLHDδ-cadinene (11.3%),
α-cadinol (10.8%), and
α-phellandrene (6.9%)		Repellency assay Blatta orientalis
(Blatt.: Blattidae)		Repellency (93.3% at 35.4 µg/cm2).[79]
L—leaf; S—seed; HD—hydro distillation; SD—steam distillation; n.r.—not reported.
Table 4. Data related to the application and biopesticide activity of S. molle EO in nanotechnology systems.
Table 4. Data related to the application and biopesticide activity of S. molle EO in nanotechnology systems.
CountryPartExtractionMain CompoundFormula/TechnologyDimensionApplicationPestActivityRef
Perun.r.n.r.D-limonene and
α-phellandrene		EO and chitosan (1:2) microencapsulation with the spray-drier (1% w/w)78.4 μmContact (contaminated surface)Macrosiphum euphorbiae
(Hem.: Aphididae)		Adulticide
(LC50 = 1.4 mg/cm2)		[54]
ArgentineaAP, FHDβ-phellandrene (28.3%) and
α-phellandrene (11.5%)		EO and Arabic rubber
microencapsulation with atomizer
(10% w/w)		200.0 μmContact (contaminated surface), Evaporation, and Repellency assayVarroa destructor
(Mes.: Varroidae)		Adulticide
(at 24 h, 0.25 g, contact: 30%; evaporation: 20%); Attractant effect		[87]
ArgentinaL, BSDn.r.EO and gum Arabic/maltodextrin (1:4) microencapsulation with the spray-drier (1% w/w)10–40 μmContactHaematobia irritans
(Dipt.: Muscidae)		Adulticide (at 2 h 32% at 100 mg/mL)[86]
AP—aerial part; B—branch; L—leaf; F—fruit; HD—hydro distillation; SD—steam distillation; n.r.—not reported.
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Scalvenzi, L.; Durofil, A.; Cáceres Claros, C.; Pérez Martínez, A.; Guardado Yordi, E.; Manfredini, S.; Baldini, E.; Vertuani, S.; Radice, M. Unleashing Nature’s Pesticide: A Systematic Review of Schinus molle Essential Oil’s Biopesticidal Potential. Sustainability 2024, 16, 10444. https://doi.org/10.3390/su162310444

AMA Style

Scalvenzi L, Durofil A, Cáceres Claros C, Pérez Martínez A, Guardado Yordi E, Manfredini S, Baldini E, Vertuani S, Radice M. Unleashing Nature’s Pesticide: A Systematic Review of Schinus molle Essential Oil’s Biopesticidal Potential. Sustainability. 2024; 16(23):10444. https://doi.org/10.3390/su162310444

Chicago/Turabian Style

Scalvenzi, Laura, Andrea Durofil, Carlos Cáceres Claros, Amaury Pérez Martínez, Estela Guardado Yordi, Stefano Manfredini, Erika Baldini, Silvia Vertuani, and Matteo Radice. 2024. "Unleashing Nature’s Pesticide: A Systematic Review of Schinus molle Essential Oil’s Biopesticidal Potential" Sustainability 16, no. 23: 10444. https://doi.org/10.3390/su162310444

APA Style

Scalvenzi, L., Durofil, A., Cáceres Claros, C., Pérez Martínez, A., Guardado Yordi, E., Manfredini, S., Baldini, E., Vertuani, S., & Radice, M. (2024). Unleashing Nature’s Pesticide: A Systematic Review of Schinus molle Essential Oil’s Biopesticidal Potential. Sustainability, 16(23), 10444. https://doi.org/10.3390/su162310444

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