A Systematic Review of the Bioactivity of Jatropha curcas L. (Euphorbiaceae) Extracts in the Control of Insect Pests

1. Introduction

Insecticides of synthetic origin are intended to control and eliminate insect pests that cause damage in agriculture and livestock, as well as those organisms that function as disease vectors, and against insects that cause damage to ornamental plants and animals. Their mechanisms of action are varied, but most commercial products contain neurotoxic active ingredients [1]. This is why the excessive use of synthetic chemical insecticides in recent decades has been partly responsible for various health and environmental problems, contamination of surface and groundwater and increased cost of production [2,3].

The presence of chemical insecticide residues in food generates serious consequences on human health that include blindness, cancer, liver and nervous system diseases, as well as long-term effects that reduce fertility, increase cholesterol levels, produce high infant mortality rates and various metabolic/genetic disorders [4]. Consequently, there is a global growing demand for food produced without the use of synthetic chemicals and the adoption of organic, agroecological, or environmentally sustainable agriculture [5]. For these reasons, more effective strategies for the control of insect pests are continually being sought. In addition, new compounds are not only intended to be more efficient but also to be implemented in an integrated pest management strategy and to have a favorable ecotoxicological profile that includes a short persistence in the environment [6].

Botanical extracts used as an alternative in the control of insect pests may have different effects, among which the most important are repellence, anti-feeding, oviposition deterrence, suppression of reproductive behavior, reduction of fecundity and fertility, and growth regulation. Additionally, botanical extracts stand out for their rapid degradation in the environment, lower production cost, and reduced toxicity, as well as more selective action mechanisms than synthetic chemical insecticides [7]. In this regard, several studies have demonstrated the insecticidal and deterrent potential of the plant Jatropha curcas L. (Euphorbiaceae) on pest insects through the use of its extracts, oils or compounds isolated from different parts of the plant, including its seeds, whose toxicity on insects is attributed to several components, including saponins, lectins, curcine, phytates, protease inhibitors, curcalonic acid and phorbol esters, among others [8,9]. Therefore, botanical extracts of J. curcas represent an alternative to achieve sustainable management in pest control, as they have nematicidal, fungicidal and antifeedant effects [10], as well as molluskicidal, insecticidal and acaricidal activities [11].

Although there is evidence on the potential use of the plant J. curcas in the control of insect pests, to date, there has been no systematic and orderly summary of the bioactivity of its botanical extracts against the groups of insects on which these extracts are effective and thus prevent damage in the main crops affected by such insects. Consequently, in the present study, a systematic review was carried out to synthesize the global evidence published regarding the use of botanical extracts of J. curcas on plague insects. The objectives of the present systematic review were 1) to identify and map the body of scientific evidence published on the use of botanical extracts of J. curcas against insect pests in different crops, 2) to summarize the body of evidence, and 3) to identify the main chemical compounds with insecticidal and insectistatic bioactivity extracted from the plant. The information generated from this study will be useful in guiding evidence-based decisions for any actor seeking alternatives for sustainable pest management control.

2. Materials and Methods

2.1. Protocol and guidelines followed

The topic addressed in this systematic review was established using an a priori protocol following the methodology proposed in the Preferred Reporting Items for Systematic Reviews and Meta-analysis protocol (PRISMA-P) statement [12], which is available upon request by contacting the corresponding author. In addition, the study was prepared and reported according to the Cochrane [13] and PRISMA [14] guidelines.

2.2. Inclusion criteria

In this systematic review, we included studies that reported results on the use of botanical extracts from the plant J. curcas in which their bioactivity was assessed either as insecticidal or insectistatic against insect pests of different crops. The insecticidal activity was considered the primary outcome and was defined as the control of the number of insects or colonies reported as the absolute value or percentage of mortality or larval and pupal viability reduction after exposure to the botanical extracts. Insectistatic activity was considered the secondary outcome and was defined as an effect on the growth or reproduction of the insect, anti-feeding effect, including a reduction in larval and pupal weight, lower fecundity and fertility, anti-oviposition effect, reduced hatching and hatchability of eggs, altered development, morphological malformations, and altered physiology. We included studies that assessed any type of botanical extract (including hexanoic, acetonic, methanolic, aqueous, ethanolic, or petroleum ether, among others) or secondary metabolite extracts from the plant J. curcas under in vitro, field, or greenhouse conditions. With respect to the type of studies included in our systematic review, only primary experimental studies published during the last 10 years as full text articles in English, Spanish, or Portuguese in peer-reviewed journals were considered.

2.3. Information sources and search strategy

The search for studies was carried out exhaustively from September to November 2022 using different databases included in the Digital Library System of the Metropolitan Autonomous University (BIDI-UAM) and included the main search engines Scopus, ScienceDirect, Web of Science, SCiELO, and CAB Direct. To perform the specific electronic searches, we defined and used the following search terms in conjunction with Boolean operators (AND, OR, and NOT): (jatropa curcas OR j. curcas OR physic nut) AND (extracts OR botanical extracts OR hexanic OR acetonic OR methanolic OR aqueous OR ethanolic OR petroleum ether OR secondary metabolites) AND (crop pest insects OR insect control OR insecticide OR insectistatic OR bioactivity). All the records found through the search in the different databases were compiled and downloaded into EndNote 20 to manage the bibliographic records by a single reviewer.

In SCOPUS, we used the following search command: ( jatropha AND curcas OR j AND curcas OR physic AND nut ) AND ( extracts OR botanical AND extracts OR hexanoic OR acetonic OR methanolic OR aqueous OR ethanolic OR petroleum AND ether OR secondary AND metabolites ) AND ( crop AND pest AND insects OR insect AND control OR insecticide OR antistatic OR bioactivity ) AND ( LIMIT-TO ( SUBJAREA , "AGRI" ) ) AND ( LIMIT-TO ( DOCTYPE , "ar" ) ). In Web of Science, the following search command was used: ALL=((jatropa curcas OR j. curcas OR physic nut) AND (extracts OR botanical extracts OR hexanic OR acetonic OR methanolic OR aqueous OR ethanolic OR petroleum ether OR secondary metabolites) AND (crop pest insects OR insect control OR insecticide OR insectistatic OR bioactivity)) NOT Document types: Review Article.

2.4. Study selection process and data extraction

Study selection was performed as previously reported [15]. Briefly, a single reviewer removed duplicates both automatically and manually from the EndNote library. Next, the same reviewer conducted the selection process, removing studies based on title and abstract screening. After this step, the studies were retrieved in full text to assess final eligibility using a standardized format based on the inclusion criteria. The studies included in the narrative synthesis were extracted using a standardized format to find the main characteristics per study for data charting in an Excel spreadsheet. The data extracted included author, year of publication, objective and methodology of the study, geographical region where the study was conducted, parts of the plant used and type of extract obtained, type of insect pests and agricultural crops assessed, type of sample evaluated (eggs, larvae, pupae, or adult insects), and identification of secondary metabolites.

2.5. Risk of bias assessment

One reviewer assessed the risk of bias in individual studies using a previous modification of the Cochrane Collaboration's risk of bias tool [16]. Accordingly, each study was assessed for having a low, high, or unclear risk of bias in each of the following criteria: 1) adequate description of the botanical extract assessed in the study, 2) clear specification of the method used in bioassays, 3) consistency of report, 4) adequate analysis of the insecticidal and insectistatic activity, 5) clear description of the method used for obtaining extracts, and 6) selective presentation of results. The results from this evaluation are presented as the percentage of studies in each category of bias per criterion.

2.6. Summary of evidence

Similar to a previous study [17], data charting was used to obtain numerical counts of the frequency of each extracted characteristic from the studies and create contingency tables grouping different categories of information. Graphs were constructed with Prisma 10, whereas the Sankey diagram was obtained online at https://sankeymatic.com.

3. Results

3.1. Studies included in the evidence synthesis

The initial search yielded a total of 320 documents, with ScienceDirect and CAB abstracts being the electronic databases that contributed 71.8% of the records, while SCOPUS only contributed 2.5%. Additionally, 10 more records were added by cross-referencing to generate a total of 330 identified records, of which 16 duplicates were removed. Of the 314 remaining records, 212 were excluded after reviewing the title, and 59 more documents were excluded after reading the abstract. Thus, 43 documents passed the eligibility process and were retrieved in full text. Of these, after applying the inclusion criteria, four studies were eliminated for the reasons presented in the flow diagram depicted in Figure 1. In total, 39 publications were included in the narrative synthesis.

3.2. Main characteristics of the studies included in the systematic review

Among the 39 studies included in our review, 24 were published in English, followed by 3 and 2 studies published in Portuguese and Spanish, respectively. The studies were from 14 different countries distributed across three continents, with Africa contributing the highest number of publications (18), followed by the Americas (11) and Asia (10) (Figure 2a). In conjunction, Nigeria (9), India (7), Brazil (7), Sudan (4), and Mexico (3) provided 78.94% of the studies, whereas the remaining nine countries contributed one study each (Appendix Table A1). According to Figure 2b, 52.63% of the studies (20) were published from 2015 to 2021, thus indicating a high interest in the topic in recent years.

As summarized in Appendix Table A1, the 39 studies included in the systematic review assessed the insecticidal and insectistatic activity of a variety of botanical extracts from J. curcas against different insect pests. These studies reported mortality, population number, anti-feeding activity, anti-oviposition, hatchability of eggs, morphological/developmental effects, repellency, and physiological effects as the main outcomes. The studies assessed the bioactivity of botanical extracts of J. curcas on eight different taxonomic orders of insect pests that included 44 individual bioassay results for different insect pest species from these orders (Figure 2d). Lepidoptera, Coleoptera, and Hemiptera were the main taxonomic orders, as these included 36/44 bioassays.

3.3. Risk of bias within the studies

As summarized in Figure 2c, among the 39 studies assessed for risk of bias, 23.07% showed a high risk of bias in the selective presentation of results. However, 15.38 and 17.94% of the studies were rated as having an unclear risk of bias for not presenting a clear description of the method used for obtaining the botanical extract and the selective reporting of results, respectively. In the remaining criteria, between 94.87 and 100% of the studies were rated as having a low risk of bias.

3.4. Summary of evidence by order of plague insects

3.4.1. Lepidoptera

1.

Plutella xylostella

Amoabeng, et al. [18] evaluated the aqueous extract of J. curcas leaves sprayed on cabbage (Brassica oleracea (L.)) plants at a concentration of 3% (w/v) under open field conditions. The plants contained third instar larvae of Plutella xylostella (L.) (Lepidoptera: Plutellinae), which were reduced by 66% with the treatment. Ingle, et al. [19] evaluated methanolic extracts of leaves, seeds, seed hulls, bark, and root of J. curcas at a concentration of 5% (w/v) against third instar larvae of P. xylostella in bioassays of ingestion in cabbage leaf discs. After 72 hours, the methanolic extract of seed husk was more effective, causing 100% mortality. In another study, the aqueous latex extract obtained from J. curcas stems was evaluated at concentrations of 25 and 50% (v/v) sprayed on experimental plots of cabbage crops for controlling P. xylostella larvae infestation. The treatment showed a minimal reduction of 11% in the number of larvae at the higher concentration [20].

2.

Spodoptera frugiperda

Devappa, et al. [21] assessed phorbol ester-enriched fractions of J. curcas seed oil against Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), the main pest of the maize crop. Two bioassays were performed against third instar larvae of the insect, one of topical toxicity (0.0313, 0.0625, 0.125, 0.25, 0.5, 1, and 20 mg/ml-1) and the other by ingestion (0.0625, 0.125, and 0.25 mg/ml-1). The treatment induced toxicity by contact with an LC₅₀ of 0.83 mg/ml-1, and the treated corn leaves (0.25 mg/ml-1) showed decreased feed consumption by 33% and reduced growth by 42% and feed conversion efficiency by 38%. Ribeiro, et al. [22] assessed seven methanolic leaf extracts of different accessions (PM-2, PM-7, PM-10, PM-11, PM-12, PM-14 and EMB) of J. curcas against neonate larvae of S. frugiperda in an ingestion bioassay (1,000 mg/kg-1). The EMB accession extract showed the best result for larval mortality (range 56.67-60%). Ingle, et al. [23] examined methanolic extracts of leaves, bark, seeds, and seed hulls of J. curcas against third instar larvae of S. litura in ingestion bioassays at 5% (w/v). After 72 hours, the methanolic extract from the leaves showed 60% mortality of the larvae compared to the other extracts.

3.

Helicoverpa armigera

Diabaté, et al. [24] used an aqueous extract of J. curcas seeds sprayed at 50 and 80 g/L on tomato plots to control Helicoverpa armigera (H.) (Lepidoptera; Noctuidae) larvae in field trials and reported a similar reduction in the number of larvae in comparison to chemical pesticides. One study reported the effect of methanolic extracts from different parts of J. curcas used in an ingestion bioassay of cotton leaves at 5, 10, and 15% (w/v) against third instar larvae of H. armigera. The extracts showed antifeedant activity and reduced the weight of larvae by 42% after 48 hours, whereas 15% of the extract caused the highest mortality (60%) of larvae [19]. Jagdish, et al. [25] included J. curcas oil alone or in combination with Neem to control H. armigera and Thysanoplusia orichalcea (I.) (Lepidoptera: Noctuidae) in chickpea-cilantro intercropping system. Two treatments that included J. curcas oil were the most effective in reducing the larval population of both insect pests.

4.

Copitarsia decolora

Figueroa-Brito, et al. [26] used an aqueous extract of J. curcas seed powder in bioassays of ingestion at 1 and 5% (v/v) against Copitarsia decolora (G.) (Lepidoptera: Noctuidae) and reported a 46% reduction in larval viability when 5% of the aqueous extract was used. Additionally, Figueroa-Brito, et al. [27] assessed the use of J. curcas acetone seed extracts (shell, kernel, and almond nut) against neonate larvae of C. decolora in experimental bioassays (250, 500, 1,000, 1,500 and 2,000 ppm) and greenhouse tests (250, 500 and 1,000 ppm) on B. oleracea plants. The acetonic extracts from almond nut and kernel plus shell at 500 and 1,500 ppm, respectively, caused the highest percentage of deformations in pupae and adults and induced a 50% mortality of larvae. In greenhouse tests, 250 ppm almond nut showed the highest reduction (33.8%) in damage to the plant.

5.

Other species

Guerra-Arévalo, et al. [28] evaluated five concentrations (10, 20, 30, and 40% (v/v)) of J. curcas resin on leaf discs of Swietenia macrophylla (K.) mahogany (Meliaceae) to control the third instar larvae of Hypsipyla grandella (Z.) (Lepidoptera: Pyralidae). At a 40% concentration, the resin caused 67% larval mortality and 30% larval activity. Ishag and Osman [29] reported the effect of aqueous and oily extracts of J. curcas seeds on the hatchability of Erias insulana (B.) (Lepidoptera: Noctuidae) eggs in a contact bioassay at 5, 10, 15, and 20% (v/v) concentrations, in which the highest concentration reduced the hatchability of the eggs by 64%.

Sharma [30] assessed the effect of an acetone extract (0.0, 0.625, 1.25, 2.5, 5.0, and 10.0 (v/v)) obtained from leaves of J. curcas on the growth and development of Spilarctia oblicua (R.) (Lepidoptera: Noctuidae) larvae. The concentration of 5.0% produced the highest larval mortality (33.3%) and the largest reduction in pupation (36.6%). Kona, et al. [31] investigated the effect of petroleum ether extract of J. curcas seeds against eggs and larvae of the tomato leafminer Tuta absoluta (M.) (Lepidoptera: Gelechiidae) in contact bioassays at 62.5, 125, 250, 500, and 1,000 mg/L for freshly laid eggs and 2,000, 4,000, 6,000, and 8,000 mg/L for larvae. The highest mortality of eggs (25%) was found at 125 mg/L of the plant extract, whereas larval mortality was 85 and 100% at 4,000 and 8,000 mg/L, respectively.

Ugwu [32] evaluated a petroleum ether extract of J. curcas seeds against the legume pod borer Maruca vitrata (F.) (Lepidoptera: Crambidae). The extract was sprayed at 10 mL/L water on cowpea (Vigna unguiculata (L.)) seedlings in which the treatment reduced the larval population by 59.12%. de Oliveira, et al. [33] reported the effect of a 3% aqueous extract of J. curcas oil on the hatching of Diatraea saccharalis (F.) (Lepidoptera: Pyralidae) caterpillars in a contact toxicity bioassay. After applying the treatment, only 60% hatching was observed in conjunction with an increase in the embryonic period. Khani, et al. [34] examined the efficacy of a petroleum ether extract of J. curcas seeds against third instar larvae and eggs of the rice moth larvae Corcyra cephalonica (S.) (Lepidoptera: Pyralidae). The extract was tested at 2, 4, 6, 8, and 10% (w/v) in contact bioassays in which an LC₅₀ of 13.22 µL/ml was found, with 12 and 20 µL/ml of the extract causing a mortality of 66.5 and 98%, respectively, whereas 10 µL/ml reduced hatchability by 92% and inhibited adult emergence.

3.4.2. Coleoptera

1.

Sitophilus zeamais

Silva, et al. [35] conducted two bioassays against adult insects of Sitophilus zeamais (M.) (Coleoptera: Curculionidae) and Rhyzorpertha dominica (S.) (Coleoptera: Bostrychidae) using 5 and 10% (w/v) aqueous extracts and powders from seeds and pericarps from J. curcas. The higher concentration induced the highest mortality of S. zeamais and R. dominica insects by 75 and 100%, respectively. Babarinde, et al. [36] evaluated oils from J. curcas seeds pretreated with different extraction methods (roasting, cooking, and crude extract) against adult insects of the corn weevil S. zeamais. After fumigation (50, 100, 150 and 200 µl/L) and contact toxicity (0.30, 0.60, 0.90, 1.20, and 1.50 µl/cm²) bioassays, 200 μl/L of the oil from roasted seeds increased mortality by 84.68%, which was the highest among the treatments. Jide-Ojo [37] assessed aqueous leaf extract and seed oil from J. curcas on S. zeamais at 0, 5, 10, 50, and 100 ppm concentrations. Seed oil at 100 ppm increased protection against grain damage by 93%, inhibited oviposition by 90%, decreased adult hatching by 92.3%, and caused 90% mortality. Finally, seed powders from J. curcas were used for controlling adult insects of S. zeamais at 0.0, 2.5, 5.0, 7.5, and 10.0 g through an ingestion bioassay. Treatment with 10 g of seed powder caused an increase in the number of dead insects in comparison to the control group, which showed no mortality [38].

2.

Callosobruchus maculatus

Opuba, et al. [39] exposed adult insects of the stored cowpea seed beetle Callosobruchus maculatus (F.) (Coleoptera; Chrysomeloidea) to an aqueous extract of J. curcas leaves in an ingestion bioassay. The extract was sprayed at 1.0, 2.0, and 3.0% (w/v) on cowpea seeds containing adult insects, and the results showed that all the treatments induced high mortality (range 94-98%) and that 1% of the extract reduced the oviposition rate by 81.04%. Uddin Ii and Abdulazeez [40] used powder and aqueous extract of J. curcas seeds in the control of C. maculatus. The treatments were applied by contact at different filtrations (1.5, 2.0, and 2.5% (w/v)) on cowpea seeds containing newly emerged adult insects. The extract at 2.5% for 48 hours increased mortality, reduced oviposition, and decreased adult emergence. Finally, Kolawole and Kolawole [41] performed an ingestion bioassay using cowpea seeds infected with adult insects of C. maculatus to assess the effect of an ethanolic extract of J. curcas seeds at 0, 5,000, 10,000, 15,000, and 20,000 ppm. The highest concentration of the extract increased oxidative stress by 22.42% and lipid peroxidation, which are indicative of damage to the vital organs of the insects.

3.

Triboleum castaneum

Pant, et al. [42] examined a combined aqueous extract of J. curcas and Pongamia glabra (L.) (Fabaceae) for the control of Triboleum castaneum, an insect pest of stored grains. The extract was mixed with eucalyptus oil to obtain a nanoemulsion that was used in direct contact bioassays at 300, 600, 900, 1,200, and 1,500 ppm. The LC₅₀ was 0.1646 mg/l, with 300 and 1,500 ppm causing an insect mortality between 88 and 100%. Another study assessed methanolic, chloroformic, petroleum ether, and n-hexane extracts of J. curcas leaves in toxicity bioassays at 5, 10, and 15% (v/v) against adult insects of T. castaneum and R. dominica. At 72 hours posttreatment, 15% of the methanolic extract induced the highest mortality in T. castaneum and R. dominica (37.32 and 49.17%, respectively) [43].

4.

Podagrica uniforma

Onunkun [44] reported the effect of an aqueous extract of J. curcas seeds on adult insects of Podagrica uniforma (Jac.) and P. sjostedti (Jac.) (Coleoptera: Chrysomeloidea), which are two species of flea beetles that infest okra crops (Abelmoschus esculentus (L.)) (Malvaceae). An ingestion bioassay using 10% (w/v) of the extract showed a reduction in beetle populations by 64%.

3.4.3. Hemiptera

1.

Brevicoryne brassicae

Botti, et al. [45] evaluated an aqueous seed oil extract of J. curcas at different concentrations (0, 0.5, 1.0, 1.5, 2.0, 2.5, and 3.0% (v/v)) for the management of a major cabbage pest, the aphid Brevicoryne brassicae (L.) (Hemiptera: Aphididade). The extract was sprayed on cabbage leaf discs containing adult aphids of B. brassicae, with 40 and 60% mortality of aphids in the first 24-48 hours after application at a concentration of 3.0%. Another study used an aqueous latex extract from J. curcas extracts against B. brassicae. The extract was evaluated at 25 and 50% (v/v) and sprayed on experimental plots of B. oleracea cabbage crops, where a moderate reduction was observed at the 50% concentration [20]. Finally, another study reported the effect of a 3% (w/v) aqueous extract of J. curcas leaves against adult aphids of B. brassicae in mesh cages containing B. oleracea cabbage plants, where the extract showed a reduction in aphid infestation [18].

2.

Other species

Orozco-Santos, et al. [46] used different types of oils and plant extracts of J. curcas to control Diaphorina citri (K.) (Hemiptera: Liviidae) nymphs on lime trees Citrus aurantifolia (L.) (Rutaceaer). The extract and seed oil were evaluated in an ingestion bioassay at 1 and 4% (v/v). At 2-6 days posttreatment, the seed oil reduced the nymph number between 76.3 and 92.5%. Sumantri, et al. [47] assessed an aqueous extract of J. curcas seeds on adult insects of Nezara viridula (L.) (Hemiptera: Pentatomidae), the main insect pest of soybean Glycine max (L.) (Fabaceae). Using an ingestion bioassay with 0.25 and 0.5% (v/v) of the extract, the LC₅₀ was 0.026% with an insect mortality of 80 and 100% per treatment.

Holtz, et al. [48] reported the insecticidal potential of different parts and seed oil of J. curcas against nymphs and adult insects of Planococcus citri (R.) (Hemiptera; Pseudococcidae). In contact and ingestion bioassays with 0.0, 0.5, 1.0, 1.5, 2.0, 2.5, and 3.0% (w/v) of the extracts, there was a high mortality (>90%) at 1.5, 2.0, and 3.0% concentrations. Yadav, et al. [49] investigated the effect of a methanolic extract of J. curcas leaves on aphids of Melanaphis sacchari (Z.) (Hemiptera: Aphididade) in an ingestion bioassays using sorghum leaves. The extract showed a mortality rate of 68.35% and a control efficiency of 56.57%. Ugwu [50] used crude and aqueous extracts of J. curcas against Phytolyma fusca (A.) (Hemiptera: Homotomidae) under laboratory and field conditions. Using a bioassay of residual action and contact toxicity with 75 and 100% (w/v) of the extract, the treatment had a residual effect of 3.33 and 4.33 at 40 min and a 1.67 contact effect on P. fusca.

3.4.4. Diptera

Silva, et al. [51] evaluated the toxicity of a 10% (w/v) aqueous extract of J. curcas leaves on larvae of the fruit fly Ceratitis capitata (W.) (Diptera: Tephritidae) using an ingestion bioassay and found that the treatment was toxic and effective because it caused a high larval mortality of 95.6%. Rampadarath, et al. [52] tested the larvicidal activity of ethyl acetate extract with methanol from bark, roots, leaves, and seeds of J. curcas against Bactrocera zonata (S.) and B. cucurbitae (C.) larvae (Diptera: Tephritidae). Ingestion bioassays using 200, 400, and 800 mg/l (w/v) of the extract were performed on larvae, and the results showed a significant effect because larval mortality ranged between 66.67 and 70%.

3.4.5. Homoptera

Diabaté, Gnago, Koffi and Tano [24] assessed an aqueous extract of J. curcas seeds sprayed at 50 and 80 g/L on tomato plots for the control of adult insects of Bemisia tabaci (G.) (Homoptera: Aleyrodidae) in field trials. The treatment at 80 g/L reduced the number of insects between 0.13 and 2.26 among the experimental conditions. Another study reported the effect of green fruit seed extracts and seed oils from fresh and dry fruits of J. curcas on adult green aphids Myzus persicae (S.) (Homoptera: Aphididae). Cabbage leaves (B. oleracea (L.) treated with 0.0, 0.5, 1.0, 1.5, 2.0, 2.5, and 3.0% (w/v) of the extract in an ingestion bioassay were tested, with 61 and 71% mortality after 48-72 h at 2.5% [53].

3.4.6. Isoptera

Addisu, et al. [54] reported the use of an aqueous seed extract of J. curcas for controlling the worker termite Macrotermes spp. (H.) (Isoptera: Termitidae), an insect pest that attacks timber tree crops. A topical application bioassay using 10, 20, 30, and 35% (w/v) of the extract showed a total mortality of 100% 72 hours after treatment with 20 and 35%.

3.4.7. Othoptera

Bashir and El Shafie [55] evaluated the insecticidal and antifeedant efficacy of J. curcas oil against third instar nymphs of the desert locust Schistocerca gregaria (F.) (Orthoptera: Acrididae), a phytophagous insect of great economic importance. The seed oil at 5, 10, 15, and 20% (v/v) concentrations was tested in bioassays in which all the concentrations caused nymph mortality ranging from 22.4 to 59.2%. In addition, 10% of the extract delayed the development time and reduced the percentage of egg hatching, whereas 5% of the extract caused an antifeeding effect of 50%. Bashir and El Shafie [56] reported the effect of 10% (v/v) J. curcas seed oil against third instar nymphs and adult development of S. gregaria in a contact bioassay, whereas 5% (v/v) of the extract was assessed for its phage-deterrent effect. The 5% extract produced an antifeedant effect of 78.92%, with a nymphal mortality of 43.39% and 42.2% reduction of female fecundity found at 10% of the extract.

3.4.7. Thysanoptera

Ugwu [32] examined the insecticidal efficacy of petroleum ether extracts of J. curcas seeds against legume flower thrips Megalurothrips sjostedti (T.) (Thysanoptera: Tripidae). The extract was sprayed at a concentration of 10 ml/L on cowpea seedlings in experimental plots at one-week intervals for six weeks. After this period, the treatment produced a 52.07% reduction in the percentage of M. sjostedti thrips.

3.5. Chemical compounds identified in the botanical parts of Jatropha curcas

In total, six studies reported the main chemical compounds identified in the botanical extracts of J. curcas. Two studies using gas chromatography and mass spectrometry found fatty acids such as palmitic acid, palmitoleic acid, oleic acid, linoleic acid, stearic acid, octadecenal, and vaccenic acid as the main compounds in seeds of the plant [27,36]. Another study identified sterols, diterpenic alcohol, and hydrocarbons in fractions of aqueous extracts from fresh and dried leaves of J. curcas through gas chromatography‒mass spectrometry and nuclear magnetic resonance spectroscopy (H¹ y C¹³) [22]. In one study, fractions enriched with phorbol esters from seed oil of J. curcas were obtained and purified using ultrafast chromatography and high-performance liquid chromatography [21]. Another two studies used phytochemical screening on seeds and leaves of J. curcas to identify secondary metabolites that included alcaolids, tanins, saponins, flavonoids, terpenoids, steroids, and fenols in leaves and seeds from the plant [37,38].

4. Discussion

The summary of evidence presented in our systematic review allowed us to achieve our three objectives. First, we identified 39 studies that described the bioactivity of botanical extracts from different parts of J. curcas for controlling insect pests. These studies were conducted in different parts of the world, with East and West Africa accounting for 46% of the studies, followed by Latin America with 28% and South Asia with 25%. Second, the studies included in this review reported the effect of botanical extracts against insect pest species distributed across eight taxonomic orders, with Lepidoptera species accounting for most of the individual bioassays reported in the studies (18/44), mainly in the Noctuidae genus, followed by Coleoptera (10/44) and Hemiptera (8/44). In contrast, Isoptera and Thysanoptera were less frequently included in the bioassays. Third, the aqueous and methanolic extracts from seeds and leaves and the seed oil of J. curcas showed the greatest insecticidal and insectistatic activity against polyphagous pests, insect pests of stored grains, grain flea beetles, aphids of cabbage and sorghum, citrus crops, and fruit flies, among others.

J. curcas is a small drought-resistant tree that thrives in many parts of tropical and subtropical regions [57]; thus, we found no studies from Europe, North America, and North Asia. The studies that included stored grain pest insects from Coleoptera were found mainly in East and West Africa, where people make their living from agriculture, which is largely traditional, and grains constitute the major part of their diet, such as sorghum, maize, rice, wheat, millet, cowpea, beans, chickpea, and groundnut [58]. Therefore, the introduction and dissemination of exotic pest insects into new habitats where they inflict damage to stored agricultural products represents a serious burden [59]. Consequently, producers are looking for new low-cost alternatives for controlling insect pests of stored grains. This growing interest in exploring botanical extracts from plants with insecticidal and insectistatic activity, such as J. curcas, helps explain the fact that 20/39 studies included in our review were published during a six-year period (2015-2021).

In Table 1, we present a summary of the significant results of the insecticidal and insectistatic activity of J. curcas extracts on insect pests and the main crops in which the bioassays were conducted. This information may be used to guide evidence-based decisions on the use of botanical extracts from J. curcas as an alternative for sustainable pest management control. Accordingly, seed oil and the aqueous and methanolic extracts from seeds and leaves of J. curcas showed both effective insecticidal and insectistatic activity against postharvest pests such as C. maculatus and S. zeamais, polyphagous pests such as E. insulana, S. frugiperda, H. armiguera, C. decolora, C. cephalonica, and D. saccharalis, and the desert locust S. gregaria (Table 1).

The insecticidal bioactivity of the botanical extracts from J. curcas induced a higher mortality and a greater reduction in the colonies or number of insect pests, whereas the insectistatic bioactivity was characterized by an increased antifeedant activity, decreased oviposition, reduced hatching of eggs, low hatchability, higher percentage of malformation of adult insects, and developmental defects of larvae and pupae (Table 1). These results coincide with previous reports that concluded that seed oil, petroleum ether, and cethonic extracts from J. curcas seeds and leaves presented biocidal activity, including insecticidal effects against different species of insects, mainly from the orders Lepidoptera, Homoptera, and Coleoptera [60,61,62].

Additionally, our systematic review showed that both the type of solvent used to obtain the botanical extract of J. curcas and the method of application (contact or food) are fundamental to increase the insecticidal and insectistatic bioactivity on different species of insect pests. In a previous review by Muniz, et al. [63], the authors concluded that although all organs of the J. curcas plant are toxic, the degree of toxicity varies according to the formulation of the extract, the nature of the active substance, the administration procedure, and the individual sensitivity of the insect pest. On the other hand, it is of vital importance to know how secondary metabolites affect the behavior, development and reproduction of pest insects [64].

The identification of the major chemical compounds present in the different extracts obtained from the botanical parts of the J. curcas plant is an important first step in understanding the effect they have on insect life at the molecular level. Other studies have reported that aqueous extracts of seeds and leaves obtained from plants belonging to the Euphorbiaceae family are also effective against plague insects of the orders summarized in this review. In one study, R. comunis (Euphorbiaceae) at a concentration of 20% (w/v) caused 67% mortality in P. xylostella larvae [65]. An aqueous extract of Euphorbia thymifolia (Euphorbiaceae) showed a 100% antifeedant effect at a concentration of 10% (w/v) on the stored grain pest insect R. dominica [66]. Our results and those from other studies that show a higher efficacy of the aqueous extracts of seeds and leaves of plants from the Euphorbiaceae family suggest that these botanical extracts should be used as a new alternative for the control and agroecological management of insect pests by producers from different parts of the world. Additionally, as leaves and seeds are more abundant for collection and obtaining aqueous extracts, they tend to benefit producers because of their easy method for obtaining them, without requiring the purchase of other chemical solvents that could cause toxic problems for producers, which makes them a new alternative in an integrated pest management program that is easy to apply, environmentally friendly, sustainable, and low-cost [67].

5. Conclusions

Our systematic review allowed us to obtain a body of evidence and thus evaluate the scope and nature of the scientific publications reporting the use of botanical extracts obtained from different parts of J. curcas, which present bioactivity in the control of insect pests of different taxonomic orders. In addition, our summary of evidence allowed us to analyze, synthesize and disseminate the main characteristics and findings of these studies. The evidence from our study demonstrates the growing interest in controlling insect pests in an effective, economically profitable, and environmentally friendly manner. We found that aqueous and methanolic extracts obtained from leaves, seeds, and seed oil of J. curcas provide an alternative in the control of insect pests, showing increased insecticidal activity in the different taxonomic orders of insect pest species. The results summarized in this review can support future experimental work and inform evidence-based technical decision-making by agricultural producers. However, future research is needed to evaluate the bioactivity of the main secondary metabolites of J. curcas and their main mechanisms of action (humoral, metabolic, and molecular) that regulate the control of insect pests of different taxonomic orders worldwide.