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Essential Oils and Spodoptera frugiperda: History
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Contributor: Virginia L. Usseglio , José S. Dambolena , María P. Zunino

Spodoptera frugiperda is a major pest of maize crops. Essential oils (EOs) are a possible source of novel pesticides, due to the fact that they have contact, fumigant, attractant and repellent activities against several insect pests.

  • natural insecticides
  • insect pest
  • phytochemicals

1. Introduction

The demand for food commodities has increased exponentially with population growth. It is estimated that the world population will be between 9.4 and 10.1 billion people in 2050 [1], implying a 35% increase in the demand for food [2]. Maize (Zea mays L.) is among the most cultivated cereals in the world, with a global production of 1185.90 million metric tons being expected in 2022–2023 [3]. However, crop losses occur due to the action of pests, such as insects and fungi [4]. To maximize crop yields, pest control currently involves the application of approximately 2 million tons of synthetic pesticides per year, of which 29.5% corresponds to insecticides [5].
The fall armyworm (FAW) Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) is among the most common pests of maize plants in the tropical regions of the Americas [6]. In addition, as a result of the expansion of agricultural frontiers, it is now considered to be an invasive pest in African countries, China, India and Australia [7][8][9][10][11][12]. Spodoptera frugiperda is a holometabolous insect [6][13]. From its eggs, the first of six larval stages emerges. These larvae are initially light green, after which they become dark green with three longitudinal yellowish and dark brown lines. Then, 15–25 days after emergence from the egg, the sixth stage larvae pupate, preferably in the soil for between 7 and 13 days, until completing the cycle again with the emergence of new adults [6][13].
The use of Bt maize varieties designed to resist chewing phytophagous insects, such as FAW, has been carried out since 1996 [14]. However, due to the continuous use of these maize varieties, numerous instances of resistance of S. frugiperda to the Cry1 protein of Bacillus thuringiensis (Bt) have been reported [15][16][17][18][19][20][21][22][23]. Therefore, the search for new pest control strategies has to be continued. Related to this, the search for sustainable alternatives is becoming more ever popular [15], with the exploitation of natural products obtained from the secondary metabolism of plants being an ecofriendly attractive alternative [20][21][22].
Essential oils (EOs) are a possible source of novel pesticides, due to the fact that they have contact, fumigant, attractant and repellent activities against several insect pests [24][25][26][27][28].

2. Essential Oils Evaluated against Spodoptera frugiperda

An analysis was carried out which indicated the 11 most used plant families for obtaining EOs for toxicological studies on FAW (Table 1). More than 50% of the 27 selected articles referred to EOs obtained from just three plant families: Piperaceae, Lamiaceae and Verbenaceae, in order of decreasing frequency.
Table 1. Occurrence of families whose essential oil has been studied as an insecticide against Spodoptera frugiperda.
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
In total, 21 plant genera were identified in the bibliographical analysis (Table 2). The most frequently studied genus was Piper (13), from the Piperaceae family, followed by the genera Ocimum (9) and Lippia (9), both from the Lamiaceae family. In all, the evaluation identified a total of 57 plant species (Table 3). Of these, Ocimum basilicum, commonly known as “basil”, was the most used species, followed by Piper marginatum, the “marigold pepper, Ti Bombé or Hinojo”, and the “purple sage” Lippia alba.
Table 2. Plant genera whose essential oils have been evaluated as insecticides against Spodoptera frugiperda.
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
Table 3. Plant species whose essential oils are evaluated as insecticides against Spodoptera frugiperda.
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
Most of the EOs used were extracted from the aerial parts of the plants, mainly the leaves, which were used dry or fresh. In general, the EOs were obtained from the aerial plant parts by the steam dragging distillation technique. However, EOs were obtained by cold pressing when extracted from the shell of the fruits belonging to the Citrus species. It is interesting to note that 35% of the articles analyzed (27) did not specify the plant organ used for the EO extraction.
From the compositional analysis of the 57 EOs tested, 56 different main organic compounds were identified. The molecular structures of compounds mentioned in more than 5% of the literature are shown in Figure 1, with geranial, geraniol, linalool, α-pinene and limonene being the most frequent. The volatile organic compounds (VOCs) cited as being the major components of the 57 EOs used as insecticides against FAW. However, only 31% of the 27 articles analyzed complemented their toxicity studies with the use of pure EO compounds. Thymol and linalool were the most evaluated EO compounds (used in 17% of the studies), followed by limonene and geraniol (12%) (Figure 1). 
Plants 12 00003 g001
Figure 1. Volatile volatile organic compounds (VOCs) used to evaluate toxicity against Spodoptera frugiperda. The percentages indicate the proportion of appearance of these compounds in the literature. Percentages were calculated based on 23% of articles (of 27 selected) that test pure VOCs.
Commercial insecticides can be a very useful tool for comparing the insecticidal effect of EOs. Nevertheless, only 41.6% of the articles used a commercial synthetic insecticide as the positive control, with 4% using the commercial natural insecticide neem extract (Azadirachta indica). Deltamethrin (12.5%), a synthetic pyrethroid pesticide used in livestock, aquaculture and agriculture due to its low residue and high toxicity, as well as because of its great efficacy, was the most frequently used synthetic insecticide as the positive control [29] (Table 4). Concerning the negative control, the one most used was acetone.
Table 4. Commercial insecticides used as positive controls against Spodoptera frugiperda.
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
In the remaining 54.2% of the articles, positive controls were not used.

3. Routes of Entry of Essential Oils

The physicochemical properties of the EO molecules modulate the routes of entry into the organism [30][31]. EOs are lipophilic complex mixtures of hydrocarbon compounds of 10 to 15 carbon atoms with different functional groups, such as phenols, aldehydes, ketones, alcohols and hydrocarbons [24]. Lipophilicity is among the most important parameters to take into account when selecting bioactive compounds and the methods to test them, because the insect cuticle forms a physical defense barrier [32][33][34]. Thus, the lipophilicity property of EOs makes it easier for them to reach their target within the body [34][35][36][37]. It is widely known that organophosphate insecticides, such as Dichlorvos (DDVP), penetrate through the integument until they reach the hemolymph and, subsequently, their site of action [38][39]. In turn, there is a correlation between resistance to insecticides and cuticular penetration [40][41][42]. The non-polar nature of the insect cuticle, composed mainly of aliphatic hydrocarbons, chitin and waxes, could favor the entry of lipophilic compounds, such as those present in EOs [33][40][43][44]. Thus, this is a critical property to be considered when choosing a method to assess the toxicity of EOs on S. frugiperda.
Another important factor to consider in EOs is their high volatility. Therefore, the way of applying the EOs and their persistence over time must be considered when evaluating their toxicity, not only in terms of the method of application, but also of the development temperature of the test [45]. Related to this, Papachristos and Stamopoulos [46] were the first to determine the importance of the temperature at which the test is carried out on the rate of vapor release and the absorption levels of EOs, and also on the effectiveness of the enzymatic machinery for detoxification of insects.
By considering the physicochemical properties of EOs, three main routes of access of these to the target insect could be determined (Figure 2A)—ingestion, inhalation and direct contact with the integument.
Plants 12 00003 g002
Figure 2. (A) Routes of entry of EOs to lepidopteran larvae. Orange arrow: entry through the respiratory spiracles. Purple arrow: entry through ingestion of treated food. Blue arrow: entry by direct contact with the integument. (B) Optimal moments of chemical control thought the larval stages of S. frugiperda. Red segments indicate the optimal stage for chemical control. (Modified from Programa Manejo de Resistencia de Insectos (MRI) and the Insecticide Resistance Action Committee (IRAC Argentina) [47].)
The toxicity of EOs was mainly tested on larval stages (96%), while a few articles (4%) evaluated the toxicity on eggs. The FAW has six different larval stages (Figure 2B). Of these, 61% of the EO toxicity studies were carried out on the third stage, while the remaining ones were performed on the second (22%), first (14%) or fourth (3%) stages. There were no studies reporting EO toxicity being carried out on the fifth or sixth stage larvae. This is in agreement with numerous manuals about the control of S. frugiperda, which have indicated that 4 to 10 days after oviposition is the optimal time to apply chemical controls (Figure 2B) because the larvae are newly hatched, and also to minimize the damage that these insects can cause to the maize crop [48][49][50][51].

This entry is adapted from the peer-reviewed paper 10.3390/plants12010003

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