Abstract
In Africa and Asia, fall armyworm (Spodoptera frugiperda) and South American tomato pinworm (Tuta absoluta) have become severe invasive pests of maize and tomato, respectively. They rapidly develop resistance to commercial pesticides. Therefore, there is an urge to integrate new eco-friendly pesticides into the management programs. Bamboo-leaf prickly ash, Zanthoxylum armatum (Za), is known to have insecticidal activities. We tested Za’s n-hexane extract against these two pests. Median lethal concentrations (LC50) at 96 h after treatment (HAT) against second-instar S. frugiperda and T. absoluta larvae were 4.41 and 4.42 mL/L, respectively. At ≥ 22.0 mL/L concentration, the extract showed a 100% ovicidal effect against both the pest species. LCQTOF analysis revealed that fatty acids constituted ~ 95% of this extract; carboxylic acids and secondary metabolites such as alkaloids and flavonoids accounted for the remaining portion. Extract’s foliar application also showed oviposition deterrence against these two pests. At ≥ 22.0 mL/L extract concentration, no S. frugiperda oviposition was observed. At ≥ 6.0 mL/L, extract reduced the T. absoluta oviposition by > six folds. To understand the basis of this deterrence, we conducted Za extract’s GCMS analysis. It revealed that monoterpenes, sesquiterpenes, and their derivatives were the most abundant constituents (55%), followed by fatty acids and their derivatives (34%), and aromatic compounds (10%). We infer that this extract is a unique combination of antibiosis- and antixenosis-causing, shelf life-increasing, and activity-enhancing compounds. It can be a highly useful biopesticide for integrating into the S. frugiperda and T. absoluta management programs.
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Introduction
Fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), and South American tomato pinworm, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), are American origin pests. S. frugiperda is a severe pest of maize; nevertheless, it is polyphagous and devours > 350 plant species, including important crops such as rice, sorghum, sugarcane, cotton, and legumes (Firake and Behere 2020; Montezano et al. 2018). T. absoluta, primarily a tomato pest, also infests other solanaceous plants such as potato, eggplant, black nightshade, fierce thornapple, and tree tobacco (Cherif and Verheggen 2019). Recently, these two pest species invaded Africa and Asia and caused massive economic losses (Tarusikirwa et al. 2020; Firake and Behere 2020; Desneux et al. 2021). Both pests are resistant to several synthetic pesticides (Mota-Sanchez and Wise 2019). Therefore, there is an urgent need for new pesticides’ integration into the management programs of invasive S. frugiperda and T. absoluta.
Botanical pesticides’ demand for environmentally friendly pest management programs is rapidly increasing (Umesh et al. 2021). Pesticide resistance in insects is often associated with the detoxification enzymes involved in target site insecticidal mechanisms (Torres et al. 2018). Synthetic pesticides often act on specific target sites in the insect body; therefore, the chances of resistance development against them are high. Since the botanical extracts used as pesticides contain blends of secondary metabolites, they act on multiple target sites reducing the insects’ resistance development possibilities (Kostyukovsky et al. 2002; Isman 2006; Priestley et al. 2003).
Prickly ash, Zanthoxylum armatum D.C. (Rutaceae) (hereafter referred to as ‘Za’), is a widely distributed edible plant species known for its ethnomedicinal value and commercially important bioactive compounds (Nooreen et al. 2019; Firake et al. 2014). Extracts of different plant parts of Zanthoxylum spp. are rich in various secondary metabolites with insecticidal properties (Sandjo et al. 2014) and often serve as a source for isolating active botanicals for sustainable pest management. Za extracts have been reported to show insecticidal properties against aphids (Heinrichs 1981; Raturi et al. 2014), mosquitoes (Kokate et al. 2001), stored grain pests (Wang et al. 2011), and lepidopteran pests (Kumar et al. 2016a; Kaleeswaran et al. 2018, 2019). Za extracts also exhibit remarkable antifeedant, ovicidal, and repellent actions against several lepidopteran pests (Kaleeswaran et al. 2019; Kumar et al. 2016a, 2016b). The essential oil of Za contains alcohols, aldehydes, alkanes, and monoterpenoids (Lawless 2013; Patiño et al. 2012).
Based on Za extract’s multiple actions, such as higher contact toxicity, antifeedant effect, ovicidal, and repellent actions against insects, we tested the hypothesis that it is insecticidal against invasive and multi-pesticide resistant S. frugiperda and T. absoluta. Further, we hypothesized that this active extract is secondary metabolite rich and tested this hypothesis by conducting extract’s Gas Chromatography-Mass Spectrometry (GCMS)- and LC-Quadrupole Time-of-Flight (LCQTOF)-based metabolomics.
Materials and methods
Plant material and extraction
Fresh Za fruits bought from the Ummulong (Meghalaya state, India; 25.5198°N, 92.1524°E) market were washed with tap water, shade-dried, pulverized, and extracted in n-hexane using the Soxhlet method. The pulverized 50 g sample was extracted using 500 mL n-hexane by heating under reflux for 70 cycles (8 h) with the heating mantle temperature of 55 °C. Extracts were concentrated using a rotary evaporator at 55 °C. Concentrated extracts were poured into the glass Petri dishes (Borosil: 100 × 17 mm) and incubated in a hot air oven at 37 °C for 48 h for the complete evaporation of n-hexane. These concentrates were weighed and stored in airtight containers at 4 °C until future use.
S. frugiperda and T. absoluta mass rearing
Larvae of S. frugiperda and T. absoluta were collected using insect-handling forceps from maize and tomato plants, respectively, from entomology fields of ICAR Research Complex for NEH Region, Umiam, Meghalaya (GPS: 25.682°N, 91.916°E). S. frugiperda larvae were reared in sterile 100-mL polypropylene containers (Tarsons®, India). They were fed primordial leaves of maize whorls [surface-sterilized with an aqueous solution of sodium hypochlorite (0.05%) and rinsed with distilled water] and were incubated at laboratory-controlled conditions (25 ± 1 °C, 75 ± 5% RH, and 12-h photoperiod). Adults were fed 50% honey solution. After 36 h of emergence, mated females were released in the cages for oviposition on the potted 25- to 30-day-old maize plants. Fresh egg masses collected from these cages were used for further experiments.
Tuta absoluta-infested tomato leaves were collected from the entomology field at Umiam. Larvae were reared on fresh tomato leaves in sterile 100-mL polypropylene containers under laboratory-controlled conditions (25 ± 1 °C temperature, 75 ± 5% relative humidity, and 12-h photoperiod). After emergence, adults were collected with the help of an aspirator and released into the cage containing 50 potted tomato plants (30 to 40 days old). T. absoluta was allowed to multiply inside the cage.
Throughout this work, both the pest species cultures were maintained, and all the experiments were conducted at 25 ± 1 °C temperature, 75 ± 5% relative humidity, and 12-h photoperiod. Cultures were maintained, and the oviposition deterrence analyses were conducted in the cages (45 × 45 × 45 cm with a white nylon mesh of 160 µm aperture).
Za extract’s larvicidal activity
Second-instar S. frugiperda and T. absoluta larvae were used for testing Za extract’s larvicidal activity, as recommended by the Insecticide Resistance Action Committee (IRAC) for various pesticides (Porter 2012, 2011). Rangefinder assays were conducted to determine the Za extract concentrations causing 20%-80% larval mortality. Accordingly, seven concentrations 22.0, 11.0, 5.5, 2.75, 1.38, 0.69, and 0.0 mL/L (control) were prepared for the toxicity tests against S. frugiperda and 24.0, 12.0, 6.0, 3.0, 1.5, 0.7, and 0.0 mL/L (control) for the toxicity tests against T. absoluta, as previously described by Kaleeswaran et al. (2018).
Bio-efficacy of the extract against the second-instar S. frugiperda larvae was tested using the topical application technique (McLaughlin et al. 1998). Molting first-instar S. frugiperda larvae were separated from the culture, and each of these larvae was kept in separate 100-mL bioassay containers (Tarsons®, India). Emerged second-instar larvae were fed on maize leaf disks for 12 h. For the bioassay, each 12-h-old second-instar larva was provided a new maize leaf disk and was allowed to settle for 5 min. Later, one µl of each extract concentration was separately spread on different larvae’s dorsal surfaces using a microtip.
Tuta absoluta larvae feed on the mesophyll tissue of tomato leaves, leading to typical mines/blotches on the leaves (Sankarganesh et al. 2017). For them, the IRAC-approved leaf dip bioassay method (Porter 2012) was used to determine the toxicity of the Za extract. Tomato leaf disks of 2 cm diameter dipped in the Za extract were placed in the bioassay Petri dishes (Make: Himedia, India). When reared at 25 °C, T. absoluta larvae enter the second instar within 2.5 days after hatching (Bajracharya and Bhat 2018; Rasheed et al. 2018). Therefore, the 3-day-old larvae were considered as second instars. They were carefully removed from the mines, and blotches of the infested tomato leaves and were placed on the tomato leaf disks (one larva/disk).
Assay for each Za extract concentration (treatment) contained 120 larvae (n = 120). Data on larval mortality were recorded at 48, 72, and 96 h after the treatment. During the experimental period, ad libitum feeding was ensured. Insects were considered ‘dead’ if they failed to respond when probed with a fine paintbrush.
Za extract’s ovicidal activity
Freshly laid (12-h-old) egg masses were collected from S. frugiperda culture cages. Eggs were separated into batches of 50 eggs. Eggs of each batch were topically applied with 1 µl Za extract. T. absoluta (12-h-old) fresh eggs on tomato leaves were sprayed with different Za extract concentrations. Each treatment batch consisted of 16–26 eggs, and each treatment was replicated five times.
The number of hatched eggs in each treatment was recorded, and hatchability (%) was determined using the following formula (Brari and Thakur 2017).
Za extract’s LCQTOF-based metabolomics
For the LCQTOF-based metabolomics analysis of the nonvolatile constituents of the Za extract, our previously described procedure (Umesh et al. 2021) was used. Za extract (10 µl) was injected into an X500R UPLC system coupled with an ESI-QTOF mass spectrometer (AB SCIEX Pte. Ltd.). Metabolites were separated using a Phenomenex Gemini® C18 column (50 mm × 4.6 mm, 5 μm, 110 Å). Mobile phase component ‘A’ was Milli-Q water with 0.1% formic acid (Sigma-Aldrich, India) (vol/vol) and component ‘B’ was methanol (J T Baker®, India) with 0.1% formic acid (vol/vol). A constant flow rate of 0.5 mL/min and a gradient of ‘B’ with 5% (0 min), 5% (1.5 min), 95% (10 min), 95% (11 min), 5% (12 min), and 5% (15 min) were used. MS scans for masses between 100 and 900 Da were performed in positive and negative ionization modes with 5000 V spray voltage, 400 °C curtain gas temperature, and 10 V collision energy. Fragmentation was performed using a 45 V collision energy spread. Fragment masses between 50 and 900 Da were scanned using the TOF mass analyzer.
Data were processed using the SCIEX OS software’s (version 1.6) peak finding algorithm to generate a list of nontarget peaks. A mass tolerance of 10 ppm, an area ratio (sample/control) threshold of 10 was followed, and the stringency of the peak detection method was set to a medium level to avoid the inclusion of masses with low intensity and without MS/MS fragmentation. Unknown masses were assigned a chemical formula using an in-built formula finder algorithm which accounts for bromide, chloride, fluorine, iodine, phosphorous, and sulfur atoms along with carbon, hydrogen, nitrogen, and oxygen for an elemental composition assignment following the MS and MS/MS spectrum using the precursor ion's mass accuracy and isotopic pattern (Maag et al. 2015; Llorca and Rodríguez-Mozaz 2013; Ramos et al. 2019). Compound annotation was done based on their predicted chemical formula and fragment masses along with their relative intensities using the online mass spectral databases—MassBank (Horai et al. 2010) and RIKEN MSn spectral database (ReSpect) for phytochemicals (Blaženović et al. 2018; Sawada et al. 2012), PubChem (Kim et al. 2016), and ChemSpider (Pence and Williams 2010; Little et al. 2011). Quantitation was done by normalizing the peak areas with that of the internal standards [solasodine (100 ng/mL) (Sigma-Aldrich, India) and adonitol (100 ng/mL) (Sigma-Aldrich, India) for positive and negative ionization modes, respectively].
Za extract’s oviposition deterrence
Spodoptera frugiperda oviposition begins from 20-day age of the maize seedlings, and active larval feeding can be seen on ≥ 40-day-old plants (Pitre et al. 1983); therefore, 40- to 45-day-old maize plants were used in the experiments. Plants sprayed with different Za extract concentrations were kept inside the cages (30 plants/concentration/cage). Three replicate cages were set. After 30 min, 30 mated (24 h after mating) S. frugiperda females (n = 30) were released inside these cages; during the assay, they were fed with 50% honey solutions ad libitum. After 96 h, egg masses on each maize plant were counted.
For T. absoluta oviposition analysis, potted tomato plants (45-day-old; n = 30) were uniformly sprayed with different Za extract concentrations. After 30 min of spraying, three plants of each treatment were kept inside every oviposition cage. Mated T. absoluta females (12 h after mating) (n = 50/cage) were released in each cage; during the assay, they were fed with 50% honey solutions ad libitum. Five replicate cages were set. After 72 h, the number of eggs per plant was enumerated.
Za extract’s GCMS analysis
Plants’ volatile organic compounds (VOCs) are often involved in oviposition deterrence. To find whether the Za hexane extract also contained VOCs, it was subjected to a GCMS analysis. Extracts were centrifuged (12,000×g, 20 min, 4 °C). Clear supernatants were concentrated to 200 ± 20 µl and dehydrated using anhydrous sodium sulfate (Sigma-Aldrich, India). Lipids with high molecular weight were removed from the extracts by precipitation at -80 °C followed by centrifugation (12,000×g, 20 min, 4 °C). Extracts were stored in GC autosampler vials at − 20 °C until further use. 7890B GC coupled with 7000D triple quadrupole MS-QQQ (Agilent Technologies, India) was used. Extract (2 µl) was injected in a spitless mode via a multimode inlet. DB5 column (30 m × 0.32 mm ID × 0.25 µm film thickness; Agilent J&W Scientific, India) was used for metabolite separation. Both inlet and detector temperatures were kept constant at 250 °C, and the carrier helium gas flow was set at 2 mL/min. GC oven program was set as follows: (1) 1.5 min hold at 60 °C, (2) temperature was increased to 180 °C with a rate of 2.5 °C/min, (3) further increase to 280 °C with a rate of 20 °C/min, and (4) hold for 5 min. MS parameters were set as follows: (1) electron impact (EI) ionization with 70 eV energy and (2) scanning range—30 to 600 m/z, at seven cycles/sec scan speed. Metabolites were identified using the mass spectral search program integrated with Wiley Registry 11th Edition—NIST 2017 Mass Spectral Library (version 2.0); they were quantified by normalizing their peak areas with the internal standard nonyl acetate’s peak area (Sigma-Aldrich, India) (Pandit et al. 2009).
Statistical analyses
Corrected mortality data (Abbott 1925) in bioassay experiments were subjected to Probit analysis (Finney 1971) to determine median lethal concentrations (LC50) of the extract by using Polo Plus: Probit and Logit analysis (LeOra 2003). Initially, data related to the ovicidal action of Za extract on both the pest species were subjected to arcsine transformation. T. absoluta oviposition deterrence data were subjected to square root transformation. Further, the data were analyzed using one-way ANOVA (CRD). Before conducting the ‘F’ test, the homogeneity of variances among the treatments was tested using Levene’s test, and the data normality was tested using the Jarque–Bera test. One-way ANOVA was conducted, and the statistical significance was determined by Tukey’s post hoc test (p ≤ 0.05), using SPSS 21.0 software for windows.
Results
Za extract’s larvicidal activity
Za extract’s median lethal concentrations (LC50) against the second-instar S. frugiperda at 48, 72, and 96 h after treatment (HAT) were 7.97, 5.39, and 4.41 mL/L, respectively (Table 1). Similarly, LC50s against second-instar T. absoluta were 9.84, 5.55, and 4.42 mL/L at 48, 72, and 96 HAT, respectively (Table 2).
Za extract’s ovicidal activity
Za extract showed substantial ovicidal activities (Fig. 1). S. frugiperda egg hatchability (%) was significantly reduced at > 2.75 mL/L Za treatment, and a 100% ovicidal effect was observed at the 22 mL/L concentration (Fig. 1A). Egg hatching (%) of T. absoluta was also significantly reduced at > 1.5 mL/L, and a 100% ovicidal effect was observed between 15 and 24 mL/L concentrations (Fig. 1A).
Za extract’s LCQTOF-based metabolomics
A total of 202 masses were detected in the untargeted LCMS analysis, and these accounted for 1002 nmol/g DW. Based on the precursor ion mass, chemical formula, and MS/MS spectrum, 26 compounds were annotated (Supplementary Information: Table S1). These compounds covered 22% of detected masses. The putatively characterized masses belonged to various chemical classes such as fatty acids and their derivatives, carboxylic acids, terpenoids, flavonoids, alkaloids, lignans, amino acids, and ketones.
Fatty acids and their derivatives constituted 95% of total annotated masses and 21% of total detected masses (Supplementary Information: Table S1). The major component of this class detected was a polyunsaturated fatty acid amide α-sanshool (148.18 ± 108.2 nmol/g), which accounted for 15% of total detected masses. The second most abundant fatty acid found was γ-linolenic acid (60.96 ± 22.21 nmol/g).
Six carboxylic acids were identified, constituting 3.57% of the total characterized masses (Supplementary Information: Table S1). Azelaic acid (6.6 ± 2 nmol/g) was the most abundant among them, accounting for 84%, followed by suberic acid (0.63 ± 0.22 nmol/g; 8%), and sebacic acid (0.6 ± 0.38 nmol/g; 7.7%). Other compounds in this class included mandelic acid, citric acid, and 2-isopropylmalic acid, constituting 0.39% of this compound class.
Four secondary metabolite classes found were lignans, terpenes, alkaloids, and flavonoids; they together constituted 1.28% of the total characterized masses (Supplementary Information: Table S1). Lignans accounted for 46%, with kobusin (0.68 ± 0.46 nmol/g) being the most abundant, followed by eudesmin (0.35 ± 0.26 nmol/g). The next abundant chemical class was terpenes and their derivatives, constituting 0.04% of the total characterized masses. Cymene (0.08 ± 0.01 nmol/g), a monoterpene, showed the highest concentration among terpenes and terpenoids, followed by a sesquiterpene alcohol cis-nerolidol (0.007 ± 0.001 nmol/g), and a carotenoid alloxanthin (0.0001 ± 0.00004 nmol/g). Alkaloids and flavonoids constituted only 0.03% and 0.01%, respectively. N-methylcorydaldine (0.06 ± 0.01 nmol/g) was the most abundant alkaloid, which showed a > 25-fold higher concentration than the next most abundant alkaloid berberine (0.002 ± 0 nmol/g). Two flavonoids, namely daidzein (0.02 ± 0.01 nmol/g) and catechin (0.0001 ± 0.00004 nmol/g), were found in the extract. An acetamide, namely melatonin (0.0004 ± 0.0001 nmol/g), was also detected.
Trace quantities of amino acids (N-acetyl-l-leucine, l-5-oxoproline, and d-2-aminobutyric acid) and ketones (xanthoxylin and 1-methyl-2-pyrrolidone) were detected, constituting 0.23% of the total identified masses (Supplementary Information: Table S1).
Za extract’s oviposition deterrence
Za extract’s foliar spraying significantly reduced S. frugiperda and T. absoluta oviposition (Fig. 2). S. frugiperda did not oviposit on maize plants treated with 22 mL/L Za extract (Fig. 2A). Oviposition decreased as the extract concentration increased beyond 2.75 mL/L. Extract concentrations < 2.75 mL/L did not affect the oviposition.
Tuta absoluta oviposition reduced with the sprayed extract’s increasing concentration beyond 3.0 mL/L. Oviposition was reduced by > sixfold at ≥ 6.0 mL/L extract concentrations (Fig. 2B).
Za extract’s GCMS analysis
Za extract showed remarkable oviposition deterrence. Since the volatile components generally confer such a deterrence, we analyzed the VOC composition of the extract using GCMS. Twenty-nine VOCs were detected; they belonged to three major chemical classes, namely terpenes and terpenoids (monoterpenes, sesquiterpenes, and their derivatives), fatty acids, and aromatics (Supplementary Information: Table S2).
Monoterpenes and derivatives constituted the most abundant class accounting for 48% of the blend. Among the 12 compounds of this class, cis-4-thujanol (62.38 ± 9.549 nmol/g) showed the highest concentration, followed by a monoterpene β-phellandrene (55.08 ± 10.00 nmol/g). A trans isoform of 4-thujanol, trans-sabinene hydrate (28.43 ± 4.106 nmol/g), was also detected. Other major monoterpenes were γ (38.82 ± 6.75 nmol/g) and α (25.24 ± 3.749 nmol/g) isomers of terpinene. Alcohol derivatives (+)-4-terpineol (16.99 ± 2.152 nmol/g) and δ-terpineol (8.56 ± 1.565 nmol/g) were also detected.
Eight sesquiterpene and sesquiterpenoid compounds were detected, which accounted for 7% of the VOC blend (Supplementary Information: Table S2). The most abundant compound of this class was caryophyllene oxide (23.6 ± 2.23 nmol/g), followed by caryophyllene (4.88 ± 0.80 nmol/g). Others were α-selinene, γ-cadinene, τ-cadinol, humulene-1,2-epoxide, 11,11-dimethyl-4,8-dimethylenebicyclo[7.2.0]undecan-3-ol, and 10,10-dimethyl-2,6-dimethylenebicyclo[7.2.0]undecan-5β-ol.
Fatty acids and their methyl ester derivatives constituted the second most abundant class (34% of the blend) (Supplementary Information: Table S2). Palmitoleic acid (153.81 ± 10.3 nmol/g) constituted 74% of this class. It showed a ≥ sevenfold higher concentration than the next most abundant fatty acid methyl linolenate (20.29 ± 2.369 nmol/g). Other fatty acids such as myristic acid, isopropyl myristate, methyl palmitoleate, and methyl palmitate constituted 16.22% of this class.
Aromatic compounds represented 10% of the blend (Supplementary Information: Table S2). Cinnamic acid (5.6 ± 1.06 nmol/g) and its methyl ester (58.69 ± 13.34 nmol/g) were predominant. (1R,7S, E)-7-Isopropyl-4,10-dimethylenecyclodec-5-enol (3.81 ± 0.59 nmol/g) was the only alkenol, which constituted < 1% of the total blend.
Discussion
Za is one of the most studied Rutaceae species for its biocidal activities. Among all the solvents, Za extract in n-hexane exhibited the maximum contact toxicity against S. litura (Kaleeswaran et al. 2018), Pieris brassicae L. (Lepidoptera: Pieridae) (Kaleeswaran et al. 2019), Plutella xylostella L. (Lepidoptera: Plutellidae) (Kumar et al. 2016b), Culex pipiens pallens L. (Diptera: Culicidae), and Aedes aegypti L. (Diptera: Culicidae) (Kim and Ahn 2017). Therefore, we tested the Za n-hexane extract against S. frugiperda and T. absoluta. Moreover, since peeling the small Za fruit’s pericarp is an onerous task and Za seed essential oil also exhibits larvicidal activities (Tiwary et al. 2007), we tested the entire fruits in this work. Our results substantiate that even the whole fruits’ extract shows high insecticidal potential with similar LC50 values, as previously reported. Kumar et al. (2016b) found that Za leaf extract’s LC50 against P. xylostella was 3.0 mL/L. Kaleeswaran et al. (2019) showed that Za pericarp extract’s LC50 against P. brassicae second-instar larvae was 1.5 mL/L. Kaleeswaran et al. (2018) found that this extract’s LC50 against S. litura second-instar larvae was 1.7 mL/L; at this concentration, this extract was also ovicidal and reduced the S. litura egg hatching by > 75%. Brari and Thakur (2017) demonstrated that 30 mL/L Za leaf extract was also ovicidal against the seed pest Callosobruchus analis (F.) (Coleoptera: Chrysomelidae) and reduced its egg hatching by > 50%. Besides, leaf extracts of allied species Z. simulans Hance (Qi et al. 2015) and Z. limonella (Dennst.) Alston (Soonwera et al. 2021) are also ovicidal against Haemonchus contortus (Rudolphi) Cobb (Rhabditida: Trichostrongylidae) and Periplaneta americana L. (Blattodea: Blattidae), respectively. Za extract's foliar application was highly effective as an oviposition deterrent against S. frugiperda and T. absoluta, indicating its field-level application potential. Moreover, several researchers have also demonstrated Za extract’s insect repellent activities (Zhang et al. 2017; Das et al. 1999; Hieu et al. 2010), suggesting that it can be a promising biopesticide.
Since this extract showed both antibiosis and antixenosis, we conducted the LCQTOF- and GCMS-based characterization of this extract. These metabolomics analyses revealed that this extract has a high concentration of fatty acids, carboxylic acids, terpenes, and terpenoids. More importantly, it contained insecticidal compounds. Fatty acids and derivatives constituted a significant portion of total detected metabolites. Among them, isobutyl amide α-sanshool, known to have antifeedant (Yang et al. 2013) and insecticidal (Miyakado et al. 1989) properties, was predominant. Aromatic and aliphatic carboxylic acids constituted a considerable portion of the Za extract’s nonvolatile component. Cinnamic acid and its methyl derivative were in high concentrations, congruent to the previous reports (Kayat et al. 2016). Allyl derivatives of cinnamate have a known effect against S. littoralis Boisduval (Lepidoptera: Noctuidae) even in low concentrations (Hikal et al. 2017). Mandelic acid, Za extract’s one of the major constituents, has been reported to be antifeedant and insecticidal against brown planthopper Nilaparvata lugens Stål (Hemiptera: Delphacidae) (Jin et al. 2011). When applied with fatty acyl esters, sebacic acid improved insecticide persistence and water resistance (Mehr et al. 1985). Other secondary metabolites such as phenylpropanoids (flavonoids, lignans, etc.) and alkaloids detected in the Za extract are also known to act as antifeedants, deterrents, and growth inhibitors (Harmatha and Dinan 2003; Ujváry 1999). For example, sesamin showed antifeedant activity against Spilarctia obliqua Walker (Lepidoptera: Erebidae) (Srivastava et al. 2001). Eudesmin and sesamin consumption by Anticarsia gemmatalis Hübner (Lepidoptera: Erebidae) larvae caused adult malformation (Nascimento et al. 2004). Catechin showed larvicidal effects against mosquitoes (Elumalai et al. 2016).
Previous studies suggested that Za extracts are rich in essential oils, which can be responsible for this extract’s pungency and insecticidal, bactericidal, and fungicidal activities (Pavela 2010; Choi et al. 2002). Our GCMS analysis revealed that > 65% of the VOC blend consisted of terpenes and derivatives. These results agreed with the Za extract’s earlier reported GCMS profiles. Tiwary et al. (2007) identified 28 compounds, most of which were oxygenated monoterpenes (75%) and monoterpenes (22%). Bisht et al. (2014) found 26 compounds in the Za leaf essential oil, which contained the terpenoids such as linalool (14.53%) and 1,8-cineole (6.92%) as major components. Barkatullah et al. (2013) also identified β-linalool (53.05%) and α-limonene diepoxide (11.39%) from the Za leaf essential oil. Hieu et al. (2010) found the acetylcholinesterase (AChE) inhibiting α-pinene and α-terpineol in their extracts. Monoterpenoids are considered to be responsible for the extracts’ anti-insect properties because of their efficient insect AChE inhibition (López et al. 2015). Wang et al. (2019) also found the dominance of oxygenated monoterpenes [mainly linalool (73.74%), sylvestrene (9.46%), and terpinen-4-ol (6.92%)] in the Za extract; they reported that linalool and terpinen-4-ol exhibited significant contact toxicity and repellent activities against three stored grain pests, viz. Tribolium castaneum Herbst (Coleoptera: Tenebrionidae), Lasioderma serricorne Fabricius (Coleoptera: Ptinidae), and Liposcelis bostrychophila Badonnel (Psocodea: Liposcelididae). We identified several terpenes and derivatives which are known to have potential insecticidal properties; for example, β-phellandrene (Yeom et al. 2015), terpinene and derivatives (Liao et al. 2017), thujanol (Blažytė-Čereškienė et al. 2016), limonene derivatives (Thomas and Bessiere 1989), eucalyptol (Sfara et al. 2009), caryophyllene (Cárdenas-Ortega et al. 2015; Noudjou et al. 2007), selinene (Chu et al. 2011), cadinene (Ouyang et al. 2015), and humulene (Benelli et al. 2018).
Several studies report the insecticidal and repellent properties of the plant essential oils; however, the field-level application is often limited due to their high evaporation rate. Botanical extracts can provide a solution in such case. Notably, fatty acids from such extracts can retain the volatile essential oil components and reduce their evaporation rate (Maia and Moore 2011). Their usage in microcapsule formation for volatile trap development is a recent focus in this field (Maia and Moore 2011; Perlatti et al. 2013). Second, fatty acids synergize the insect repellence of terpenoids. Compounds such as oleic acid, linoleic acid, and their methyl esters synergize the repellency of monoterpenoids against gravid females of stable flies (Hieu et al. 2014). Fatty acids naturally impart stickiness to the extract, due to which the addition of a synthetic sticker can be avoided (Devi and Khatkar 2018). Thus, Za extract’s fatty acid richness can be advantageous in field-level applications. Similarly, polyunsaturated fatty acids (Za fruit extract had linolenic acid) have the potential to act as UV protectant (Nguyen et al. 2012). Za extract’s alkaloids such as berberine can protect photolabile groups of unstable compounds such as unstable essential oil components (Cohen et al. 2001; Turek and Stintzing 2013). Terpenes and terpenoids showed more substantial effects against insects when used in combinations (Hummelbrunner and Isman 2001; Pavela 2010; Scalerandi et al. 2018), suggesting that the synergistic effects of compounds in the extract enhance the effectiveness. Together, it can be inferred that the botanical extract-based biopesticides can be advantageous over the single-target pesticides.
Biopesticides are considered as desired alternatives to synthetic pesticides considering the high health and environmental hazards. Za is an edible species, routinely used in spices, condiments, and herbal medicines. It is also used for skin applications as a cosmetic and leech repellent (Singh and Singh 2011). Since all its constituents are already a part of the natural ecosystem, a formulation made from the identified active ingredients is likely to be highly biodegradable. Thus, a formulation made of Za's active biodegradable components can be ideal for integrating into pest management programs to reduce health hazards and pollution.
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Acknowledgements
The authors thank the Director, ICAR Research Complex for NEH Region, for providing necessary laboratory and field facilities and Miss. Darisha Pakma and Miss Naphibanri Lyngdoh for technical assistance.
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The funding for the institute project ‘Monitoring, diagnosis and management of invasive alien insect pest species in North East India, PIMS code: IXX14424’ by the Indian Council of Agricultural Research, New Delhi, is duly acknowledged. The authors thank the Education Ministry, India, for funding the GCMS and UPLC-ESI-QTOF facilities. RG and MK thank the Council of Scientific and Industrial Research for Ph.D. fellowships.
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Firake, D.M., Ghosh, R., Kumar, M. et al. Bioactivity of Zanthoxylum armatum fruit extract against Spodoptera frugiperda and Tuta absoluta. J Plant Dis Prot 130, 383–392 (2023). https://doi.org/10.1007/s41348-022-00652-1
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DOI: https://doi.org/10.1007/s41348-022-00652-1