Can Essential Oils Be a Natural Alternative for the Control of Spodoptera frugiperda? A Review of Toxicity Methods and Their Modes of Action
Abstract
:1. Introduction
2. Essential Oils Evaluated against Spodoptera frugiperda
3. Routes of Entry of Essential Oils
4. Toxicological Methods against Spodoptera frugiperda
5. Toxicity of Essential Oils against Spodoptera frugiperda
5.1. Volatile Organic Compounds Tested against Spodoptera frugiperda
5.2. Comparison of Insecticidal Effects of EOs between S. frugiperda and the S. littoralis-S. litura-S. exigua Complex
5.3. Structure–Activity Relationship
6. Mode of Action of Essential Oil in Insects
6.1. Acetylcholinesterase (AChE)
6.2. GABA Receptor
6.3. Octopamine
6.4. Other Modes of Action
7. Final Considerations
- The method most used for evaluating the toxicity of EOs on S. frugiperda was topical application, where the bioactive compound enters the organism through the cuticle. Considering the field application method of traditional insecticides, this method of topical application simulates what happens when the insect pest is found in the cultivar and is reached by traditional spraying. Thus, this testing method could be recommended for laboratory study using mainly third-instar larvae, in order to obtain comparable results with already published articles.
- The most effective EOs were Ocimum gratissimum, Siparuna guianesis, Piper marginatum, Piper septuplinervium, Cymbopogon citratus, Citrus limon, and Ageratum conyzoides for the methods of topical application, contact toxicity, immersion, fumigant and ingestion, respectively. In general, these essential oils presented a high percentage of non-oxygenated volatile compounds, with the exception of C. citratus EO, thereby allowing us to predict that against this insect, terpene hydrocarbon-type compounds would present a greater toxicity. However, mostly only pure oxygenated compounds have been tested, with anethole being the most toxic of these. We suggest that mixtures of lipophilic and hydrophilic compounds could have a greater toxic effect as the former act as vehicles for the latter to cross the insect cuticle and facilitate their arrival at the active site.
- EOs and their pure compounds are approximately 1000 to 100,000 fold less toxic than most insecticides. Although it is known that these synthetic insecticides produce health and environmental problems, it is important to highlight that the effect of natural compounds is significantly lower, so they may not be widely accepted by rural producers. However, alternatives could be implemented such as the formulation of synergistic mixtures between EOs, or their more bioactive components, and traditional synthetic insecticides, in order to reduce their applied concentrations.
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Plant Family | Occurrence |
---|---|
Piperaceae | 13 |
Lamiaceae | 12 |
Verbenaceae | 10 |
Myrtaceae | 5 |
Asteraceae | 5 |
Rutaceae | 3 |
Poaceae | 3 |
Zingiberaceae | 2 |
Apiaceae | 1 |
Siparunaceae | 1 |
Geraniaceae | 1 |
Total | 56 |
Genera | Occurrence in Literature |
---|---|
Piper | 13 |
Ocimum | 9 |
Lippia | 9 |
Eucalyptus | 5 |
Hyptis | 3 |
Cymbopogon | 3 |
Foeniculum | 2 |
Corymbia | 2 |
Citrus | 2 |
Siparuna | 1 |
Ruta | 1 |
Pelargonium | 1 |
Mentha | 1 |
Malva | 1 |
Hyptis | 1 |
Eremanthus | 1 |
Tanacetum | 1 |
Artemisia | 1 |
Ageratum | 1 |
Zingiber | 1 |
Vanillosmopsis | 1 |
Total | 60 |
Plant Species | Occurrences in the Literature |
---|---|
Ocimum basilicum | 4 |
Lippia alba | 3 |
Piper marginatum | 3 |
Corymbia citriodora | 2 |
Cymbopogon citratus | 2 |
Eucalyptus staigeriana | 2 |
Foeniculum vulgare | 2 |
Hyptis marrubioides | 2 |
Lippia microphylla | 2 |
Lippia sidoides | 2 |
Ocimum gratissimum | 2 |
Piper arboreum | 2 |
Piper corcovadensis | 2 |
Piper hispidinervum | 2 |
Ageratum conyzoides | 1 |
Artemisia absinthium | 1 |
Citrus aurantium | 1 |
Citrus limon | 1 |
Citrus sinensis | 1 |
Cymbopogon winterianus | 1 |
Eremanthus erythropappus | 1 |
Eucalyptus citriodora | 1 |
Eucalyptus urograndis | 1 |
Eucalyptus urophylla | 1 |
Hyptis suaveolens | 1 |
Lippia gracilis | 1 |
Lippia origanoides | 1 |
Malva sp. | 1 |
Mentha sp. | 1 |
Ocimum selloi | 1 |
Pelargonium graveolens | 1 |
Piper aduncum | 1 |
Piper septuplinervium | 1 |
Piper subtomentosum | 1 |
Ruta graveolens | 1 |
Siparuna guianensis | 1 |
Tanacetum vulgare | 1 |
Vanillosmopsis arborea | 1 |
Zingiber officinale | 1 |
Total | 57 |
Positive Control Used in Bibliography | Occurrences in the Literature |
---|---|
neem extract (Azadirachta indica) | 2 |
deltamethrin | 3 |
α-cypermethrin | 1 |
β-cypermethrin | 1 |
fenpropathrin | 1 |
δ-cyhalothrin | 1 |
Indoxacarb | 1 |
chlorpyrifos | 1 |
Essential Oil | 50% Lethal Doses (LD50; mg/g Insect, CI) | Larval Stage | Reference |
---|---|---|---|
Ocimum gratissimum | 2.5 (1.7–2.6) × 10−4 *2 | 3rd | [59] |
Lippia gracilis | 1.2 (0.9–1.6) × 10−3 *2 | 3rd | [70] |
Artemisia absinthium | 7.1 (5.3–7.2) × 10−2 *2 | 2nd | [71] |
Hyptis marrubioides | 0.24 (0.21–0.26) *2 | 2nd | [72] |
Ocimum basilicum | 0.49 (0.45–0.53) *2 | 2nd | [72] |
Pelargonium graveolens | 1.13 (0.083–0.145) 2 | 3rd | [73] |
Lippia alba (LA-10) | 1.2 (0.84–1.57) *2 | 3rd | [73] |
Lippia alba (LA-57) | 1.21 (0.90–1.57) *2 | 3rd | [73] |
Ocimum gratissimum | 1.52 (1.36–1.67) 2 | 3rd | [60] |
Ocimum gratissimum (White wild basil) | 1.52 (1.36–1.67) 2 | 3rd | [61] |
Lippia alba (LA-22) | 1.56 (1.18–2.02) *2 | 3rd | [73] |
Ocimum gratissimum (Wild basil) | 2.84 (2.34–3.38) 2 | 3rd | [61] |
Eucalyptus staigeriana | 3.2 (2.41–4.07) 2 | 3rd | [60] |
Lippia sidoides | 3.21 (2.95–3.49) 2 | 3rd | [74] |
Piper hispidinervum | 3.39 (3.42–4.15) *2 | 3rd | [69] |
Piper hispidinervum | 3.56 (3.22–3.91) *3 | 3rd | [69] |
Piper corcovadensis | 3.58 (nd) 2 | 3rd | [75] |
Piper marginatum | 4.18 (nd) 2 | 3rd | [75] |
Eucalyptus citriodora | 4.58 (4.09–5.08) 2 | 3rd | [61] |
Corymbia citriodora | 4.59 (4.15–5.03) 2 | 2nd | [76] |
Piper hispidinervum | 4.62 (4.10–5.22) *1 | 3rd | [69] |
Ocimum basilicum | 4.86 (4.02–6.13) 2 | 3rd | [61] |
Foeniculum vulgare | 5.05 (4.13–5.96) 2 | 3rd | [61] |
Lippia microphylla | 5.35 (4.65–6.05) 2 | 2nd | [76] |
Ocimum basilicum | 6.27 (5.80–6.73) *2 | 3rd | [77] |
Piper arboreum | 10.91 (nd) 2 | 3rd | [75] |
Piper aduncum | 12 (7.1–18.0) 2 | 3rd | [78] |
Vanillosmopsis arborea | 172.86 (152.8–200.0) 2 | 3rd | [66] |
Essential Oil | 50% Lethal Concentration (LC50; μL/cm2, CI) | Larval Stage | Reference |
---|---|---|---|
Siparuna guianensis | 0.034 (0.033–0.034) μL/cm2 *1 | 3rd | [79] |
Siparuna guianensis | 0.038 (0.036–0.047) μL/cm2 *2 | 3rd | [79] |
Ocimum gratissimum | 0.171 (0.150–0.193) μL/cm2 | 3rd | [59] |
Lippia gracilis | 1.55 (1.51–1.59) μL/cm2 | 3rd | [70] |
Essential Oils | EO Application Method | Lethal Concentration 50 (LC50) | Concentration | Mortality (%) at 96 h | Larval Stage | Reference |
---|---|---|---|---|---|---|
Cymbopogon citratus | On ventral part of the leaf | 0.19 (0.13–0.38) μL/cm2 | 1st | [71] | ||
Zingiber officinale | 0.25 (0.20–0.35) μL/cm2 | 1st | [71] | |||
Mentha sp. | 0.33 (0.16–1.93) μL/cm2 | 1st | [71] | |||
Ruta graveolens | 0.62 (0.49–1.02) μL/cm2 | 1st | [71] | |||
Malva sp. | 0.67 (0.58–0.82) μL/cm2 | 1st | [71] | |||
Artemisia absinthium | 2.09 (1.64–2.96) μL/cm2 | 1st | [71] | |||
Citrus limon | Mixed in artificial diet | 98.29 ppm * | 2nd | [81] | ||
Citrus aurantium | 100 ppm * | 2nd | [81] | |||
Ocimum selloi | 600 (580–620) ppm * | 3rd | [83] | |||
Citrus sinensis | ND | 0.1 mg/g of diet | 0 | 2nd | [82] | |
1 mg/g of diet | 5 | 2nd | ||||
10 mg/g of diet | 0 | 2nd | ||||
0.1 mg/g of diet | 10 | 2nd | ||||
1 mg/g of diet | 5 | 2nd | ||||
10 mg/g of diet | 0 | 2nd | ||||
Ageratum conyzoides | By immersion of the maize or rice leaf in EOs solutions | 3430 ppm * | 1st | [80] | ||
Piper hispidinervum | 9400 (7900–11,100) ppm | 1st | [69] | |||
16,200 (14,400–18,400) ppm | 1st | |||||
17000 (13,700–21,100) ppm | 1st | |||||
17,900 (15,900–20,200) ppm | 1st | |||||
18,200 (16,800–19,700) ppm | 1st | |||||
28,300 (24,300–32,900) ppm | 1st |
Essential Oil | 50% Lethal Concentration (LC50; μL/L of Air) | Larval Stage | Reference |
---|---|---|---|
Piper septuplinervium1 | 9.4 (7.72–11.4) * | 2nd | [84] |
Piper subtomentosum2 | 13.2 (10.3–16.6) * | 2nd | [84] |
Corymbia citriodora3 | 44.85 (36.89–52.81) * | 2nd | [76] |
Lippia microphylla3 | 116.52 (95.77–137.27) * | 2nd | [76] |
Piper subtomentosum3 | 146 (116–180) * | 2nd | [84] |
Compound | 50% Lethal Doses (LD50) (mg/g of Insect, CI) | Mortality (% ± SD) 1 | Larval Stage | LogP | Reference |
---|---|---|---|---|---|
γ-cyhalothrin 2 | 1.4 (1.08–1.78) × 10−5 * | 3rd | 6.20 | [78] | |
Chlorpyrifos 2 | 2.4 (0.83–4) × 10−4 * | 2nd | 4.77–3.71 | [72] | |
Deltamethrin 2 | 2.45 (1.13–3.76) × 10−4 * | 3rd | 6.20 | [93] | |
Deltamethrin 2 | 2.46 (1.14–3.78) × 10−4 * | 3rd | 6.20 | [77] | |
Deltamethrin 2 | 3.07 (2.58–3.35) × 10−3 | 3rd | 6.20 | [74] | |
Decis 25 2 (Deltamethrin) | 3.17 (2.20–4.57) × 10−3 * | 3rd | 6.20 | [93] | |
Commercial product 2 | 3.2 (2.2–4.6) × 10−3 * | 3rd | [77] | ||
trans-anethole | 0.027 (0.021–0.032) | 3rd | 3.17 | [61] | |
citronellal | 0.07 (0.06–0.08) | 3rd | 3.48 | [61] | |
Fenpropathrin 2 | 0.18 (0.17–0.23) * | 3rd | 5.48 | [78] | |
α-cypermethrin 2 | 0.19 (0.12–0.28) * | 3rd | 6.27 | [78] | |
β-cypermethrin 2 | 1.03 (0.016–1.37) * | 3rd | 6.27 | [78] | |
linalool | 2.10 (1.65–2.56) * | 3rd | 3.28 | [93] | |
α-pinene | 2.40 (2.06–2.67) * | 3rd | 4.37 | [59] | |
thymol | 3.19 (2.93–3.45) * | 3rd | 3.28 | [59] | |
thymol | 4.91 (4.35–5.56) | 3rd | 3.28 | [74] | |
linalool | 5.20 (4.21–6.27) | 3rd | 3.28 | [61] | |
limonene | 32.24 (27.73–36.55) | 3rd | 4.45 | [61] | |
1,8-cineole | 2.0 ± 2.0 | 3rd | 2.82 | [73] | |
limonene | 4.00 ± 2.44 | 3rd | 4.45 | [73] | |
Azamax 2 | 14.00 ± 5.09 | 3rd | [73] | ||
geraniol | 30.00 ± 8.84 | 3rd | 3.28 | [73] | |
citral | 64.00 ± 7.07 | 3rd | 3.17 | [73] | |
carvone | 84.00 ± 5.09 | 3rd | 2.27 | [73] | |
linalool | 90.00 ± 3.16 | 3rd | 3.28 | [73] |
Compound | 50% Lethal Concentration (LC50, CI) | Larval Stage | LogP | Reference |
---|---|---|---|---|
Contact toxicity per se | ||||
Indoxacarb (Rumo 300 g a.i./L; DuPont do Brasil S.A.) | 0.0009 (0.0006–0.0018) μL/cm2 *1 | 3rd | 2.77 | [79] |
0.0015 (0.0009–0.0021) μL/cm2 *2 | 3rd | [79] | ||
thymol | 0.255 (0.195–0.317) μL/cm2 | 3rd | 3.28 | [59] |
α-pinene | 2.5 (2.11–2.91) μL/cm2 | 3rd | 4.37 | [59] |
Fumigant toxicity | ||||
camphene | 0.00067 μL/L * | 2nd | 4.37 | [84] |
α-pinene | 0.0066 (0.0056–0.0079) μL/L * | 2nd | 4.37 | [84] |
β-pinene | 0.016 (0.011–0.032) μL/L * | 2nd | 4.37 | [84] |
Immersion | ||||
Geraniol | 3793 (173–1281) ppm | 2nd 3 | 3.28 | [88] |
Essential Oil | Main Compounds (Relative Percentage) | Reference | ||
---|---|---|---|---|
Ingestion | ||||
Cymbopogon citratus | Geranial (47.53%) | Neral (32.5%) | nd | [71] |
Citrus limon | Limonene * (nd) | nd | nd | [81] |
Ageratum conyzoides | Precocene (87%) | β- caryophyllene (7.1%) | α-humulene (1.2%) | [80] |
Fumigation | ||||
Piper septuplinervium | α-pinene * (21%) | β-pinene * (13.8%) | Citronellal * (10.3%) | [84] |
Topical application | ||||
Ocimum gratissimum | Thymol * (33.2%) | p-cymene (22.5%) | γ-terpinene (21%) | [59] |
Contact toxicity | ||||
Siparuna guianesis | β-myrcene (74.94%) | 2-undecanone (9.36%) | bicyclo-germacrene (1.52%) | [79] |
Immersion | ||||
Piper marginatum | Exalatacin (9.12%) | α-pinene * (8.45%) | α-phellandrene (6.97%) | [75] |
Essential Oils | Non-Oxygenated Terpenes (%) | Oxygenated Terpenes (%) | Reference |
---|---|---|---|
Ingestion | |||
Ageratum conyzoides | 98.2 | nd | [80] |
Cymbopogon citratus | nd | 79.03 | [71] |
Fumigation | |||
Piper septulinervium | 81.4 | 11.7 | [84] |
Topical application | |||
Ocimum gratissimum | 60.2 | 37.6 | [59] |
Contact toxicity | |||
Siparuna guianesis | 80.83 | 10.39 | [79] |
Immersion | |||
Piper marginatum | 52.72 | 18.35 | [75] |
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Usseglio, V.L.; Dambolena, J.S.; Zunino, M.P. Can Essential Oils Be a Natural Alternative for the Control of Spodoptera frugiperda? A Review of Toxicity Methods and Their Modes of Action. Plants 2023, 12, 3. https://doi.org/10.3390/plants12010003
Usseglio VL, Dambolena JS, Zunino MP. Can Essential Oils Be a Natural Alternative for the Control of Spodoptera frugiperda? A Review of Toxicity Methods and Their Modes of Action. Plants. 2023; 12(1):3. https://doi.org/10.3390/plants12010003
Chicago/Turabian StyleUsseglio, Virginia L., José S. Dambolena, and María P. Zunino. 2023. "Can Essential Oils Be a Natural Alternative for the Control of Spodoptera frugiperda? A Review of Toxicity Methods and Their Modes of Action" Plants 12, no. 1: 3. https://doi.org/10.3390/plants12010003