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Article

Essential Oils from Cameroonian Aromatic Plants as Effective Insecticides against Mosquitoes, Houseflies, and Moths

by
Joice G. Nkuimi Wandjou
1,
Cecilia Baldassarri
1,
Marta Ferrati
1,
Filippo Maggi
1,
Roman Pavela
2,3,
Nole Tsabang
4,
Riccardo Petrelli
1,
Renato Ricciardi
5,
Nicolas Desneux
6,* and
Giovanni Benelli
5,*
1
Chemistry Interdisciplinary Project (ChIP), School of Pharmacy, University of Camerino, 62032 Camerino, Italy
2
Crop Research Institute, Drnovska 507, 161 06 Prague 6, Czech Republic
3
Department of Plant Protection, Czech University of Life Sciences Prague, Kamycka 129, 165 00 Prague 6, Suchdol, Czech Republic
4
Department of Animal Biology, University of Dschang, Dschang, Cameroon
5
Department of Agriculture, Food and Environment, University of Pisa, Via del Borghetto 80, 56124 Pisa, Italy
6
Université Côte d’Azur, INRAE, CNRS, UMR ISA, 06000 Nice, France
*
Authors to whom correspondence should be addressed.
Plants 2022, 11(18), 2353; https://doi.org/10.3390/plants11182353
Submission received: 26 July 2022 / Revised: 22 August 2022 / Accepted: 23 August 2022 / Published: 9 September 2022
(This article belongs to the Special Issue Insecticidal Activity of Plant Secondary Metabolites)
Versions Notes

Abstract

:
Recently, spices have attracted the attention of scientists and agrochemical companies for their potential as insecticidal and acaricidal agents, and even as repellents to replace synthetic compounds that are labeled with detrimental impacts on environment and human and animal health. In this framework, the aim of this study was to evaluate the insecticidal potential of the essential oils (EOs) obtained from three Cameroonian aromatic plants, namely Monodora myristica (Gaertn.) Dunal, Xylopia aethiopica (Dunal) A. Rich., and Aframomum citratum (J. Pereira) K. Schum. They were produced by hydrodistillation, with yields of 3.84, 4.89, and 0.85%, respectively. The chemical composition was evaluated by GC-MS analysis. The EOs and their major constituents (i.e., geraniol, sabinene, α-pinene, p-cymene, α-phellandrene, and β-pinene) were tested against the polyphagous moth pest, i.e., Spodoptera littoralis (Boisd.), the common housefly, Musca domestica L., and the filariasis and arbovirus mosquito vector, Culex quinquefasciatus Say. Our results showed that M. myristica and X. aethiopica EOs were the most effective against M. domestica adults, being effective on both males (22.1 µg adult−1) and females (LD50: 29.1 µg adult−1). The M. myristica EO and geraniol showed the highest toxicity on S. littoralis, with LD50(90) values of 29.3 (123.5) and 25.3 (83.2) µg larva−1, respectively. Last, the EOs from M. myristica and X. aethiopica, as well as the major constituents p-cymene and α-phellandrene, were the most toxic against C. quinquefasciatus larvae. The selected EOs may potentially lead to the production of cheap and effective botanical insecticides for African smallholders, although the development of effective formulations, a safety evaluation, and an in-depth study of their efficacy on different insect species are needed.

1. Introduction

Spices are aromatic plants or their specific parts, including bark, flowers, fruits, and seeds, owning a peculiar aroma given by flavoring-odorous compounds such as volatile terpenes and phenylpropanoids. Aromatic plants have attracted the attention of explorers since ancient civilizations because of their numerous culinary and medical applications [1]. Most of the plants classified as ‘spices’ come from aromatic plants growing in tropical regions, notably Asia and Africa, from where they have been brought to Europe since ancient times, becoming an important economic activity; the main examples are cinnamon (Cinnamomum verum J. Presl) and clove (Syzygium aromaticum (L.) Merr. & L.M. Perry), which are still sold today and used all over the world for numerous purposes.
Nowadays, aromatic plants have numerous applications in the food industry, perfumery, and pharmaceuticals. In addition, some attracted the attention of scientists and agrochemical companies for their potential as insecticidal and acaricidal agents and even as repellents [2,3,4,5]. Aromatic plants contain essential oils (EOs) that have shown a wide insecticidal spectrum with limited impact on non-target organisms such as pollinators and biological control agents [6,7,8,9,10]. They can act as fumigants, contact toxicants, antifeedant and repellent agents [1,11,12,13,14,15,16], and could be an effective alternative to regular chemical pesticides [17,18]. Thus, developing commercial insecticides using spice derivatives could be a good strategy to replace synthetic compounds, which are nowadays labeled with detrimental impacts on the environment and human and animal health [19].
In this framework, we reported a comprehensive evaluation of the insecticidal potential of the essential oils obtained from three Cameroonian aromatic plants, namely Monodora myristica (Gaertn.) Dunal, Xylopia aethiopica (Dunal) A.Rich., and Aframomum citratum (J. Pereira) K. Schum., against a panel of economically relevant insect vectors and agricultural pests.
M. myristica, also called calabash nutmeg or African nutmeg, is a perennial plant from the Annonaceae family. This plant is widespread in Africa, Asia, Central and South America, and Australia, and is unable to grow out of its natural habitat [20]. In Africa, it is commonly found in Cameroon, Nigeria, Ghana, Liberia, Angola, Uganda, and west Kenya where its seeds, because of their aromatic flavor, are used as a spice in food preparation [20,21]. These seeds of about 1.5 cm long have demonstrated many healthy properties such as being antihypertensive, anti-headache, stomachic, and antiemetic [20,21].
X. aethiopica, known as Africa guinea pepper or Ethiopian pepper, is also a plant from the Annonaceae family, native to tropical Africa [22]. This plant is restricted mainly to the Guinean zone, from Senegal to Angola and Mozambique in the east; it grows in wet and swampy soils [23]. In Cameroon, it is found in the forest, forest edges, forest galleries, and savannah scrubs. The fruits of this plant have good nutritional value. They have demonstrated beneficial health effects and are used in the treatment of cough, bronchitis, and dysentery [22,24]. The extracts of this plant have also shown antibacterial, antifungal, and antiplasmodial effects [25].
A. citratum, belonging to the Zingiberaceae family, is a perennial herb with an underground rhizome [26]. This plant originates from Central and West Africa, where it is used as an aphrodisiac and in the treatment of bacterial infections, malaria, and cancers [26]. Its fruit is an ovoid capsule of 3 cm in diameter extended by the long persistent tube of the calyx, with many seeds of about 3 mm in diameter, harmonious, and contained in a white pulp. The seeds are also used as a food seasoning in Cameroon.
Despite the ethnopharmacological interest in these three plant species, research efforts to shed light on the potential insecticidal properties of their EOs are limited, and mainly focused on the use of X. ethiopica EO against stored product insect pests [27,28,29,30,31,32]. In this framework, herein we evaluated the EOs extracted from M. myristica, X. aethiopica, and A. citratum against a highly polyphagous moth pest, i.e., the cotton leaf worm, Spodoptera littoralis (Boisd.) [33], and two insects of medical and veterinary importance, i.e., the common housefly, Musca domestica L., and the filariasis and arbovirus mosquito vector, Culex quinquefasciatus Say, for which effective and sustainable control tools are still needed [34,35]. The EOs were analyzed through GC-MS analysis, and the toxicity of the main constituents of each EO was evaluated on the three insect targets to evaluate the role of major compounds in determining the insecticidal activity of the whole EOs.

2. Results

2.1. Essential Oil Yield and Chemical Composition

The hydrodistillation of the seeds has given yields of 3.84% for M. myristica, 4.89% for X. aethiopica, and 0.85% for A. citratum. The chemical compositions of the three EOs are reported in Table 1. We identified 35 compounds for M. myristica, 55 compounds for X. aethiopica, and 23 compounds for A. citratum, representing 92.9, 99.6, and 99.9% of the total composition, respectively. The main volatile compounds present in M. myristica were p-cymene (32.8%), α-phellandrene (32.3%), α-pinene (7.6%), limonene (4.4%), and myrcene (4.3%), while in the X. aethiopica EO we found sabinene (26.1%), β-pinene (17.4%), germacrene D (9.7%), α-pinene (9.6%), β-phellandrene (6.2%), and terpinene-4-ol (6.1%). The major compound in the A. citratum EO was geraniol (85.6%) followed by a minor percentage of β-pinene (5.4%).

2.2. Insecticidal Activity

The effects of M. myristica, X. aethiopica, and A. citratum EOs and their major compounds on M. domestica adult mortality are presented in Table 2. All our tested EOs were toxic to the insect species included in this study. However, significant differences were observed between the EOs. EOs from M. myristica and X. aethiopica showed the highest efficacy, with an LD50(90) of 29.1(137.6) and 30.7(164.2) µg adult−1 on females, respectively, and 22.1(127.6) and 31.5(178.5) µg adult−1, respectively, on males (Table 2).
The efficacy of M. myristica EO against houseflies was roughly equivalent to that of the major compound p-cymene, with the LD50 estimated as 28.4 µg adult−1 for females and 32.6 µg adult−1 for males. The other major compounds showed better efficacy compared to EOs, with special reference to the LD50 values estimated on males, which were more sensitive; nevertheless, LD90 values were approximately on the same level as those estimated for the EOs.
The tested EOs showed promising efficacy also against S. littoralis larvae (Table 3). Again, the highest efficacy was provided by the M. myristica EO with LD50(90) estimated as 29.3(123.5) µg larva−1. However, given the overlapping confidence intervals (CI95), it is impossible to determine with certainty whether the efficacy was significantly better. Among individual major compounds, a significantly better efficacy was shown by geraniol, which achieved a significantly lower LD50 (=25.3 µg larva−1), as well as LD90 (=83.2 µg larva−1), if compared to other tested substances (Table 3).
Last, the efficacy of the three EOs against C. quinquefasciatus larvae was very promising (Table 4). Higher efficacy was observed for M. myristica and X. aethiopica EOs, with LC50(90) estimated as 35.3(66.1) and 47.0(78.4) µg mL−1, respectively. Concerning tests carried out with major constituents, the highest efficacy was observed for p-cymene and α-phellandrene, with LC50 estimated as 26.8 and 36.8 µg mL−1, respectively (Table 4).

3. Discussion

3.1. Essential Oil Chemical Composition

The three EOs were analyzed using GC–MS, and the relative content of each component was determined by comparing the ratio of the peak area of each detected compound with the total area of all detected compounds. It resulted in the identification and quantification of both the major and minor compounds that are responsible for the insecticidal activity, acting synergistically. Regarding M. myristica harvested in the locality of Dschang in west Cameroon, Massodi et al. [21] found that the most abundant compounds in the EO were α-phellandrene (52.2%), followed by α-pinene (6.3%), myrcene (4.4%), limonene (3.7%), and α-thujene (2.9%). Similarly, the most represented class reported in this latter study was that of monoterpene hydrocarbons, representing 69.5% of the total composition. Meffo Dongmo et al. [26] identified 20 compounds in M. myristica EO from Bafoussam locality (west Cameroon) with the predominant compound as in the case of Massodi et al. [21] being α-phellandrene (61.5%) followed by germacradienol (7.9%) and δ-cadinene (4.2%). The analysis of this EO from the forest of Lobaye in Central African Republic by Koudou et al. [36] showed that α-phellandrene (34.4%) and p-cymene (22.2%) were the most abundant among 30 identified compounds. While Owokotomo and Ekundayo [37] have demonstrated that the EO of M. myristica seed harvested in Iwaro-Oka, Nigeria, was rich in germacrene-D-4-ol (25.48%), tricyclo [5.2.1(1,5)] dec-2-ene (13.35%), δ-cadinene (11.09%), and linalool (15.10%) on 22 identified compounds.
The chemical composition of X. aethiopica from Cameroon (Kribi-Southwest) and Chad (Gobe) reported by Bakarnga-Via et al. [38] demonstrated that this EO was mainly constituted by monoterpene hydrocarbons, i.e. 72.4 and 64.8%, respectively, a percentage close to that we found in our study (69.8%); nevertheless, the EOs qualitative profile was different. In the latter study, the main compounds were β-pinene (24.6.9–28.2%), terpinen-4-ol (10.0–15.1%), sabinene (4.8–14.5%), β-phellandrene (5.8–10.4%), and γ-terpinene (4.9–5.7%) [38]. Another study of this oil from the Ivory Coast revealed that the most represented compounds were β-pinene (20.5%), α-pinene (17.8 %), 1.8-cineole (7.4%), and α-phellandrene (5.6%) [39]. Keita et al. [23] reported that the dried fruit powder of this plant was richer in compounds (42 identified compounds) than the intact one (33 compounds), with a great difference in the percentages of the compounds.
The results obtained by Meffo Dongmo et al. [26] about the composition of A. citratum corroborate with what we found to the extent that the major compound present in both studies was geraniol (96.8%).
The differences in chemical composition and percentage of compounds of an EO from a different location can be justified by the fact that many factors such as genetics as well as environmental ones (maturity of fruits, geographical conditions, and climate and seasonal changes) can influence the yield and quantitative–qualitative composition of EOs [40,41].

3.2. Insecticidal Activity

Botanical-based pesticides represent a concrete and eco-friendly opportunity for small farmers worldwide, being able to exert their action through multiple mechanisms, therefore limiting resistance development. In this scenario, Africa can play a key role in botanical pesticide discovery, development, and commercialization [42,43]. After a careful analysis of the literature, it has been noted that our knowledge on the insecticidal activity of the A. citratum, M. myristica, and X. ethiopica EOs is patchy. Indeed, the available studies on EOs, only tested the X. ethiopica EO against several stored product insect pests [27,28,29,30,31,32,44]. Only a study has been done on M. myristica EO, still on stored product beetles [45], while the insecticidal activity of A. citratum EO has never been investigated. Further research has been conducted on extracts from the three plants. For example, M. myristica ethanolic extracts have been tested against dermestid beetles attacking stored fish [46], while M. myristica and A. citratum extracts exerted toxic effects on bruchid beetle species developing on stored pulses [44], and acted as antifeedants against S. littoralis larvae [47].
Our results pointed out that M. myristica and X. aethiopica EOs were effective against M. domestica adults (♀ LD50 29.1; ♂ LD50 22.1 µg adult−1). Bioactivity rates of both EOs are significant, even if still lower if compared to other promising plant EOs, such as the Carlina acaulis L. one, recently tested against houseflies [48]. On the other hand, EOs from these plants are much more available [49,50] and at the same time are characterized by a high extraction yield, which ranges between 4–5%.
The insecticidal effectiveness of EOs depends on many factors, such as the content of major constituents and their synergistic or antagonistic relationships, post-application conditions, and/or the modes of action of the major compounds [51,52]. Also in our case, it was found that the effectiveness of EOs was in line with the effectiveness of most substances.
Against houseflies, the EO from M. myristica and its major compound p-cymene showed comparable effectiveness, while other major compounds performed better in terms of LD50 while LD90 values were close to those calculated for EOs. In addition, on S. littoralis larvae, the M. myristica EO was the most effective one, with the major constituent geraniol, showing higher toxicity if compared to the other tested molecules. Last, the EOs from M. myristica and X. aethiopica, as well as the major constituents p-cymene and α-phellandrene, were the most toxic against C. quinquefasciatus larvae. Although the relatively good insecticidal effectiveness of the EOs tested by us on the three insect species was found, it will be important to study other options to make the effectiveness of EOs more efficient, so that the lowest possible amount of active substance is applied in practice. An increase in biological effectiveness can be achieved, for example, by using suitable formulation methods, which include encapsulation or nanoemulsion [8,53,54]. These methods can both extend the persistence time and significantly increase the insecticidal efficacy of EOs themselves. However, it will be equally important to study the effect of sublethal doses or concentrations on target and non-target organisms [55]. It was found that even a sublethal concentration or a short period of exposure to EOs can subsequently significantly reduce the vitality of insects [53,56,57]. Thanks to this phenomenon, not only the high mortality of treated larvae or adults can occur, but also the fertility of the next generation can be significantly reduced, and this can lead to a significant reduction in the number of pests or vectors.
Although EOs are generally considered environmentally safe [6,58,59,60,61], our further research will be directed to testing the effect of EOs on selected characteristics of non-target organisms, with the aim of confirming the environmental safety of botanical insecticide applications based on our selected EOs. It will also be important to study the possibility of increasing the content of EOs in plants, on the one hand by using suitable elicitation methods and on the other hand by developing more profitable cultivation technologies, and technique of extractions [62,63,64] that will lead to a higher yield of EOs, like the case of other aromatic plants.
Overall, there is still a long way ahead of us, which will lead from the basic screening we performed to the development and production of botanical insecticides based on EOs from M. myristica and X. aethiopica. However, this does not change the fact that we have managed to select EOs that may potentially lead to the development and production of effective botanical insecticides for African smallholders [43].

4. Materials and Methods

4.1. Plant Material and Essential Oil Extraction

The plant material was bought in a local market of Yaounde (3°52′00″ N, 11°31′00″ E, 726 m a.s.l.), Cameroon, in December 2019. The seeds from the three aromatic plants were dried away from the sun at room temperature. Plant specimens were identified by one of us (N. Tsabang). The dried seeds (500 g for M. myristica, 584 g for X. aethiopica, and 550 g for A. citratum) were ground to reduce them into smaller pieces, then inserted in a 10 L Pyrex flask, which was filled with 6 L of distilled water. EOs were obtained by hydrodistillation using a Clevenger-type apparatus for 4 h. The calculation of the oil yields was based on a dry weight (w/w) matter.

4.2. GC-MS Analysis

The M. myristica, X. aethiopica, and A. citratum EOs were prepared by a 1:100 dilution with hexane and analyzed with an Agilent 6890N–5973N GC–MS system operating in the EI mode at 70 eV, using a HP-5MS (5% phenylmethylpolysiloxane, length 30 m, internal diameter 0.25 mm, film thickness 0.1 µm; J & W Scientific, Folsom, CA, USA) capillary column. The total duration of the run was around 66 min with the following temperature program: 60 °C for 5 min, afterward up to 220 °C at 4 °C min−1, then up to 280 °C at 11 °C min−1 and maintained for 15 min. The carrier gas used in this analysis was helium at a flow rate of 1 mL min−1. The injection volume was 2 μL and the split ratio 1:50. The range of acquisition was 29–400 m z−1. The combination of linear retention indices (RIs) and mass spectra (MS) with those appearing in libraries such as Adams (2007), FFNSC2 (2012), and NIST17 (2017) was the method used for the peak identification unless no analytical standard (purchased from Merck, Milan, Italy) was available. The analytical standards of the major EO components, namely geraniol, sabinene, α-pinene, p-cymene, α-phellandrene, and β-pinene, were purchased from Merck (Milan, Italy). Relative peak area percentage for each identified compound was extracted from the total area in the chromatogram without using correction factors.

4.3. Insects

Insects used for the tests were obtained from established laboratory colonies, reared under controlled conditions for >20 generations. Uniform larvae of S. littoralis (third instar, mean larval weight 12 ± 3 mg), C. quinquefasciatus larvae (third instar), and adults of M. domestica (males and females, 3–5 days old) were selected for the experiments. The rearing methods of the three species mentioned above were recently described by Benelli et al. [65]). All the species were maintained at 25 ± 1 °C, 70 ± 3% R.H., and 16:8 h (L:D). All below described experiments were carried out under the same conditions.

4.4. Insecticidal Activity

Contact toxicity of M. myristica, X. aethiopica, and A. citratum EOs was evaluated by applying them, as well as their major constituents (i.e., geraniol, sabinene, α-pinene, p-cymene, α-phellandrene, and β-pinene), topically on the pronotum of M. domestica males and females, as well as on S. littoralis larvae. The EOs or major compounds were dissolved in acetone to obtain a concentration series. Subsequently, 1 µL was applied on each insect using a micro-electric applicator (HandyStep Electronic, Brand, Turnov, Czech Republic) to treat the CO2-anesthetized M. domestica or S. littoralis. The tested doses were 20, 30, 50, 80, 100, 120, 140, 160, 180, 200, and 250 µg adult−1 or 20, 40, 60, 80, 100, 120, 150, 180, 210, and 250 µg larva−1, respectively. Certified acetone (Sigma-Aldrich, Darmstadt, Germany) was used as the negative control treatment in the experiments. After the application, moth larvae and housefly adults were moved to rearing containers sized 15 cm × 12 cm × 8 cm with perforated lids (at 25 ± 1 °C, 70 ± 3% R.H. and 16:8 h (L:D)), containing their usual food.
In the assays focusing on C. quinquefasciatus larvae, M. myristica, X. aethiopica, and A. citratum EOs and their major constituents (i.e., geraniol, sabinene, α-pinene, p-cymene, α-phellandrene, and β-pinene) were diluted in dimethyl sulfoxide (DMSO) and then tested following WHO (1996) with minor modifications by Pavela and Sedlak [52] and Pavela et al. [48]; the tested concentrations were 20, 30, 40, 50, 70, 80, 100, 120, and 140 µg mL−1. Distilled water with the same amount of DMSO as that used for dissolving the EOs was used as negative control.
To calculate the lethal doses/concentrations for M. myristica, X. aethiopica, and A. citratum EOs and their main compounds on each insect target, we used a minimal series of at least five different doses/concentrations that resulted in mortality rates in the range of 10–90%. The experiment was replicated four times in total (20 insects per replication). Insect mortality was assessed 24 h after treatment. In insecticidal experiments, mortality was corrected, where needed, through the Abbott’s formula [66], LC50 and LC90 and the associated 95% confidence limits were estimated by probit analysis [67].

5. Conclusions

In this work, three EOs extracted from the Cameroonian plants M. myristica, X. aethiopica, and A. citratum were analyzed, and their insecticidal activity was evaluated. Their efficacy against M. domestica, S. littoralis, and C. quinquefasciatus proved to be strongly influenced by the synergistic and antagonistic interactions of the major constituents. In particular, M. myristica and X. aethiopica and their major components p-cymene and α-phellandrene resulted the most active against both houseflies and C. quinquefasciatus, while S. littoralis larvae showed sensitivity to M. myristica EO. Due to their activity and wide distribution in the African continent, these EOs have a great potential to develop insecticide products on a large scale. Future steps in this direction will be the encapsulation of the EOs in nanoformulations and the evaluation of the effect of sublethal doses or concentrations on target and non-target organisms.

Author Contributions

Conceptualization, F.M., R.P. (Roman Pavela), R.P. (Riccardo Petrelli) and G.B.; methodology, J.G.N.W., C.B., M.F., F.M., R.P. (Roman Pavela), N.T. and G.B.; software, F.M., R.P. (Roman Pavela), R.P. (Riccardo Petrelli) and G.B.; validation, F.M., R.P. (Roman Pavela), R.P. (Riccardo Petrelli), G.B., R.R. and G.B.; formal analysis, J.G.N.W., C.B., M.F., F.M., R.P. (Roman Pavela) and N.T.; investigation, J.G.N.W., C.B., M.F., F.M., R.P. (Roman Pavela), N.T., R.P. (Riccardo Petrelli), R.R., N.D. and G.B.; resources, F.M., R.P. (Roman Pavela), R.P. (Riccardo Petrelli), G.B., N.D. and G.B.; data curation, J.G.N.W., C.B., M.F., F.M., R.P. (Roman Pavela), N.T., R.P. (Riccardo Petrelli), R.R., N.D. and G.B.; writing—original draft preparation, C.B., M.F., F.M., R.P. (Roman Pavela), R.P. (Riccardo Petrelli) and G.B.; writing—review and editing, J.G.N.W., C.B., M.F., R.P., N.T., R.P., R.R. and N.D.; visualization, J.G.N.W., C.B., M.F., F.M., R.P. (Roman Pavela), N.T., R.P. (Riccardo Petrelli), R.R., N.D. and G.B.; supervision, F.M., R.P. (Roman Pavela), R.P. (Riccardo Petrelli), N.D. and G.B.; project administration, F.M., R.P. (Roman Pavela) and R.P. (Riccardo Petrelli); funding acquisition, F.M., R.P. (Roman Pavela) and R.P. (Riccardo Petrelli). All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Ministry of Agriculture of the Czech Republic (Project MZE-RO0418) and by the Italian Ministry of Health (PRIN 2017CBNCYT_005).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding authors.

Acknowledgments

Roman Pavela would like to thank the Ministry of Agriculture of the Czech Republic for financial support of the botanical pesticide and basic substances research.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. De La Torre, J.E.; Gassara, F.; Kouassi, A.P.; Brar, S.K.; Belkacemi, K. Spice use in food: Properties and benefits. Crit. Rev. Food Sci. Nutr. 2017, 57, 1078–1088. [Google Scholar] [CrossRef]
  2. Scott, I.M.; Jensen, H.R.; Philogène, B.J.R.; Arnason, J.T. A review of Piper spp. (Piperaceae) phytochemistry, insecticidal activity and mode of action. Phytochem. Rev. 2008, 7, 65–75. [Google Scholar] [CrossRef]
  3. Ashouri, S.; Shayesteh, N. Insecticidal activities of two powdered spices, black pepper and red pepper on adults of Rhyzopertha dominica (F.) and Sitophilus granaries (L.). Munis Entomol. Zool. J. 2010, 5, 600–607. [Google Scholar]
  4. Devi, K.C.; Devi, S.S. Insecticidal and oviposition deterrent properties of some spices against coleopteran beetle, Sitophilus oryzae. J. Food Sci. Technol. 2013, 50, 600–604. [Google Scholar] [CrossRef]
  5. Benelli, G.; Pavela, R.; Petrelli, R.; Cappellacci, L.; Bartolucci, F.; Canale, A.; Maggi, F. Origanum syriacum subsp. syriacum: From an ingredient of Lebanese ‘manoushe’ to a source of effective and eco-friendly botanical insecticides. Ind. Crops Prod. 2019, 134, 26–32. [Google Scholar] [CrossRef]
  6. Pavela, R.; Benelli, G. Essential Oils as Ecofriendly Biopesticides? Challenges and Constraints. Trends Plant Sci. 2016, 21, 1000–1007. [Google Scholar] [CrossRef]
  7. da Silva, I.M.; Zanuncio, J.C.; Brügger, B.P.; Soares, M.A.; Zanuncio, A.J.V.; Wilcken, C.F.; de Souza Tavares, W.; Serrão, J.E.; Sediyama, C.S. Selectivity of the botanical compounds to the pollinators Apis mellifera and Trigona hyalinata (Hymenoptera: Apidae). Sci. Rep. 2020, 10, 4820. [Google Scholar] [CrossRef]
  8. Sánchez-Gómez, S.; Pagán, R.; Pavela, R.; Mazzara, E.; Spinozzi, E.; Marinelli, O.; Zeppa, L.; Morshedloo, M.R.; Maggi, F.; Canale, A.; et al. Lethal and sublethal effects of essential oil-loaded zein nanocapsules on a zoonotic disease vector mosquito, and their non-target impact. Ind. Crops Prod. 2022, 176, 114413. [Google Scholar] [CrossRef]
  9. Ribeiro, A.V.; de Sá Farias, E.; Santos, A.A.; Filomeno, C.A.; dos Santos, I.B.; Barbosa, L.C.A.; Picanço, M.C. Selection of an essential oil from Corymbia and Eucalyptus plants against Ascia monuste and its selectivity to two non-target organisms. Crop Prot. 2018, 110, 207–213. [Google Scholar] [CrossRef]
  10. Kavallieratos, N.G.; Boukouvala, M.C.; Ntalaka, C.T.; Skourti, A.; Nika, E.P.; Maggi, F.; Spinozzi, E.; Mazzara, E.; Petrelli, R.; Lupidi, G.; et al. Efficacy of 12 commercial essential oils as wheat protectants against stored-product beetles, and their acetylcholinesterase inhibitory activity. Entomol. Gen. 2021, 41, 385–414. [Google Scholar] [CrossRef]
  11. Benelli, G.; Pavela, R. Repellence of essential oils and selected compounds against ticks—A systematic review. Acta Trop. 2018, 179, 47–54. [Google Scholar] [CrossRef]
  12. Benelli, G.; Pavela, R. Beyond mosquitoes—Essential oil toxicity and repellency against bloodsucking insects. Ind. Crops Prod. 2018, 117, 382–392. [Google Scholar] [CrossRef]
  13. Benelli, G.; Maggi, F.; Canale, A.; Mehlhorn, H. Lyme disease is on the rise–How about tick repellents? A global view. Entomol. Gen. 2019, 39, 61–72. [Google Scholar] [CrossRef]
  14. Marsin, A.M.; Muhamad, I.I.; Anis, S.N.S.; Lazim, N.A.M.; Ching, L.W.; Dolhaji, N.H. Essential oils as insect repellent agents in food packaging: A review. Eur. Food Res. Technol. 2020, 246, 1519–1532. [Google Scholar] [CrossRef]
  15. Galland, C.; Glesner, V.; Verheggen, F. Laboratory and field evaluation of a combination of attractants and repellents to control Drosophila suzukii. Entomol. Gen. 2020, 40, 263–272. [Google Scholar] [CrossRef]
  16. Dunan, L.; Malanga, T.; Bearez, P.; Benhamou, S.; Monticelli, L.S.; Desneux, N.; Michel, T.; Lavoir, A.V. Biopesticide evaluation from lab to greenhouse scale of essential oils used against Macrosiphum euphorbiae. Agriculture 2021, 11, 867. [Google Scholar] [CrossRef]
  17. Shah, F.M.; Razaq, M.; Ali, Q.; Ali, A.; Shad, S.A.; Aslam, M.; Hardy, I.C.W. Action threshold development in cabbage pest management using synthetic and botanical insecticides. Entomol. Gen. 2020, 40, 157–172. [Google Scholar] [CrossRef]
  18. Verheggen, F.; Barrès, B.; Bonafos, R.; Al, E. Producing sugar beets without neonicotinoids: An evaluation of alternatives for the management of viruses-transmitting aphids. Entomol. Gen. 2022, 42, 491–498. [Google Scholar] [CrossRef]
  19. Eddleston, M.; Eyer, P.; Worek, F.; Mohamed, F.; Senarathna, L.; Von Meyer, L.; Juszczak, E.; Hittarage, A.; Azhar, S.; Dissanayake, W.; et al. Differences between organophosphorus insecticides in human self-poisoning: A prospective cohort study. Lancet 2005, 366, 1452–1459. [Google Scholar] [CrossRef]
  20. Agiriga, A.; Siwela, M. Monodora myristica (Gaertn.) Dunal: A plant with multiple food, health and medicinal applications: A review. Am. J. Food Technol. 2017, 12, 271–284. [Google Scholar] [CrossRef]
  21. Massodi, M.L.E.; Mime, L.C.; Fogang, H.P.D.; Djikeng, F.T.; Karuna, M.S.L.; Womeni, H.M. Chemical composition and antioxidant activity of Syzygium aromaticum and Monodora myristica essential oils from Cameroon. J. Food Stab. 2018, 1–13. [Google Scholar]
  22. Asekun, O.T.; Adeniyi, B.A. Antimicrobial and cytotoxic activities of the fruit essential oil of Xylopia aethiopica from Nigeria. Fitoterapia 2004, 75, 368–370. [Google Scholar] [CrossRef]
  23. Keita, B.; Sidibé, L.; Figueredo, G.; Chalchat, J.-C. Chemical composition of the essential oil of Xylopia aethiopica (Dunal) A. ch. from Mali. J. Essent. Oil Res. 2003, 15, 267–269. [Google Scholar] [CrossRef]
  24. Ijeh, I.I.; Omodamiro, O.D.; Nwanna, I.J. Antimicrobial effects of aqueous and ethanolic fractions of two spices, Ocimum gratissimum and Xylopia aethiopica. Afr. J. Biotechnol. 2005, 4, 953–956. [Google Scholar]
  25. Adaramoye, O.A.; Okiti, O.O.; Farombi, E.O. Dried fruit extract from Xylopia aethiopica (Annonaceae) protects Wistar albino rats from adverse effects of whole body radiation. Exp. Toxicol. Pathol. 2011, 63, 635–643. [Google Scholar] [CrossRef] [PubMed]
  26. Sylvie, C.M.D.; Jean-De-Dieu, T.; Guy, S.S.N.; Pierre, T.; Jules-Roger, K. Chemical composition and antimicrobial activity of essential oils from Aframomum citratum, Aframomum daniellii, Piper capense and Monodora myristica. J. Med. Plants Res. 2019, 13, 173–187. [Google Scholar] [CrossRef]
  27. Okonkwo, E.U.; Okoye, W.I. The efficacy of four seed powders and the essential oils as protectants of cowpea and maize grains against infestation by Callosobruchus maculatus (Fabricus) (Coleoptera: Bruchidae) and Sitophilus zeamais (Motschulsky) (Coleoptera: Curculionidae) in Nigeria. Int. J. Pest Manag. 1996, 42, 143–146. [Google Scholar] [CrossRef]
  28. Kouninki, H.; Haubruge, E.; Noudjou, F.E.; Lognay, G.; Malaisse, F.; Ngassoum, M.B.; Goudoum, A.; Mapongmetsem, P.M.; Ngamo, L.S.; Hance, T. Potential use of essential oils from Cameroon applied as fumigant or contact insecticides against Sitophilus zeamais Motsch. (Coleoptera: Curculionidae). Commun. Agric. Appl. Biol. Sci. 2005, 70, 787–792. [Google Scholar]
  29. Kouninki, H.; Hance, T.; Noudjou, F.A.; Lognay, G.; Malaisse, F.; Ngassoum, M.B.; Mapongmetsem, P.M.; Ngamo, L.S.T.; Haubruge, E. Toxicity of some terpenoids of essential oils of Xylopia aethiopica from Cameroon against Sitophilus zeamais Motschulsky. J. Appl. Entomol. 2007, 131, 269–274. [Google Scholar] [CrossRef]
  30. Babarinde, S.A.; Adeyemo, Y.A. Toxic and repellent properties of Xylopia aethiopica (Dunal) A. Richard on Tribolium castaneum Herbst infesting stored millets, Pennisetum glaucum (L.) R. Br. Arch. Phytopathol. Plant Prot. 2010, 43, 810–816. [Google Scholar] [CrossRef]
  31. Habiba, K.; Thierry, H.; Jules, D.; Félicité, N.; Georges, L.; François, M.; Benoit, N.M.; Marie, M.P.; Leonard, N.T.; Eric, H. Persistent effect of a preparation of essential oil from Xylopia aethiopica against Callosobruchus maculates (Coleoptera, Bruchidae). Afr. J. Agric. Res. 2010, 5, 1881–1888. [Google Scholar]
  32. Nguemtchouin, M.M.G.; Ngassoum, M.B.; Ngamo, L.S.T.; Gaudu, X.; Cretin, M. Insecticidal formulation based on Xylopia aethiopica essential oil and kaolinite clay for maize protection. Crop Prot. 2010, 29, 985–991. [Google Scholar] [CrossRef]
  33. Salama, H.S.; Dimetry, N.Z.; Salem, S.A. On the host preference and biology of the cotton leaf worm Spodoptera littoralis Bois. Z. Für Angew. Entomol. 1971, 67, 261–266. [Google Scholar] [CrossRef]
  34. Wilke, A.B.B.; Beier, J.C.; Benelli, G. Filariasis vector control down-played due to the belief the drugs will be enough–not true! Entomol. Gen. 2020, 40, 15–24. [Google Scholar] [CrossRef]
  35. Neupane, S.; Nayduch, D. Effects of habitat and sampling time on bacterial community composition and diversity in the gut of the female house fly, Musca domestica Linnaeus (Diptera: Muscidae). Med. Vet. Entomol. 2022, 1–9. [Google Scholar] [CrossRef]
  36. Koudou, J.; Ossibi, A.W.E.; Aklikokou, K.; Abenna, A.A.; Gbeassor, M.; Bessiere, J.M. Chemical composition and hypotensive effects of essential oil of Monodora myristica Gaertn. J. Biol. Sci 2007, 7, 937–942. [Google Scholar] [CrossRef]
  37. Owokotomo, I.A.; Ekundayo, O. Comparative study of the essential oils of Monodora myristica from Nigeria. Eur. Chem. Bull. 2012, 1, 263–265. [Google Scholar] [CrossRef]
  38. Bakarnga-Via, I.; Hzounda, J.B.; Fokou, P.V.T.; Tchokouaha, L.R.Y.; Gary-Bobo, M.; Gallud, A.; Garcia, M.; Walbadet, L.; Secka, Y.; Dongmo, P.M.J.; et al. Composition and cytotoxic activity of essential oils from Xylopia aethiopica (Dunal) A. Rich, Xylopia parviflora (A. Rich) Benth.) and Monodora myristica (Gaertn) growing in Chad and Cameroon. BMC Complement. Altern. Med. 2014, 14, 125. [Google Scholar] [CrossRef]
  39. Konan, N.; Kouame, B.A.; Mamyrbekova-Bekro, J.A.; Nemlin, J.; Yves-Alain, B. Chemical composition and antioxidant activities of essential oils of Xylopia aethiopica (dunal) a. rich. Eur. J. Sci. Res. 2009, 37, 311–318. [Google Scholar]
  40. Yasser, S. Variation in Chemical Composition of Essential Oil of Ferulago angulata Collected from West Parts of Iran. Pharmaceut. Sci. 2016, 22, 16–21. [Google Scholar] [CrossRef]
  41. da Silva, R.O.M.; Castro, J.W.G.; Junior, O.d.M.D.; de Araújo, A.C.J.; Leandro, M.K.D.N.S.; Costa, R.J.O.; Pinto, L.L.; Leandro, L.M.G.; da Silva, L.E.; Do Amaral, W.; et al. Photoinduced antibacterial activity of the essential oils from Eugenia brasiliensis lam and Piper mosenii C. DC. by blue led light. Antibiotics 2019, 8, 242. [Google Scholar] [CrossRef]
  42. Sola, P.; Mvumi, B.M.; Ogendo, J.O.; Mponda, O.; Kamanula, J.F.; Nyirenda, S.P.; Belmain, S.R.; Stevenson, P.C. Botanical pesticide production, trade and regulatory mechanisms in sub-Saharan Africa: Making a case for plant-based pesticidal products. Food Secur. 2014, 6, 369–384. [Google Scholar] [CrossRef]
  43. Stevenson, P.C.; Isman, M.B.; Belmain, S.R. Pesticidal plants in Africa: A global vision of new biological control products from local uses. Ind. Crops Prod. 2017, 110, 2–9. [Google Scholar] [CrossRef]
  44. Ito, E.E.; Ighere, E.J. Bio-insecticidal potency of five plant extracts against Cowpea Weevil, Callosobruchus maculatus (F.), on Stored Cowpea, Vigna unguiculata (L). Jordan J. Biol. Sci. 2017, 10, 317–322. [Google Scholar]
  45. Owolabi, M.S.; Oladimeji, M.O.; Lajide, L.; Singh, G.; Marimuthu, P.; Isidorov, V.A. Bioactivity of three plant derived essential oils against the maize weevils Sitophilus zeamais (Motschulsky) and Cowpea Weevils Callosobruchus maculatus (Fabricius). Electron. J. Environ. Agric. Food Chem. 2009, 8, 828–835. [Google Scholar]
  46. Nwosu, L.C.; Obi, O.A.; Azoro, V.A.; Dialoke, S.A.; Onah, E.; Zakka, U.; Azeez, O.M.; Eluwa, A.N.; Uloma, A.; Ukpai, K.U.; et al. The efficacy of the plant extracts of Afrostyrax kamerunensis, Monodora myristica, Moringa oleifera and Azadirachta indica against the infestation of the leather beetle, Dermestes maculatus De Geer in smoked African mud catfish, Clarias gariepinus Burchell. Jordan J. Biol. Sci. 2018, 11, 511–515. [Google Scholar]
  47. Ntonifor, N.N.; Mueller-Harvey, I.; Van Emden, H.F.; Brown, R.H. Antifeedant activities of crude seed extracts of tropical African spices against Spodoptera littoralis (Lepidoptera: Noctuidae). Int. J. Trop. Insect Sci. 2006, 26, 78–85. [Google Scholar] [CrossRef]
  48. Pavela, R.; Maggi, F.; Petrelli, R.; Cappellacci, L.; Buccioni, M.; Palmieri, A.; Canale, A.; Benelli, G. Outstanding insecticidal activity and sublethal effects of Carlina acaulis root essential oil on the housefly, Musca domestica, with insights on its toxicity on human cells. Food Chem. Toxicol. 2020, 136, 111037. [Google Scholar] [CrossRef]
  49. Bello, M.O.; Adekunle, A.S.; Oyekunle, J.A.O.; Yusuf, T.A. Evaluation of the fixed oil of two commonly consumed spices, Monodora myristica and Myristica fragrans, as adjunct in food formulations. Sci. Res. Essays 2014, 9, 607–610. [Google Scholar] [CrossRef] [Green Version]
  50. Sokamte Tegang, A.; Beumo, T.M.N.; Dongmo, P.M.J.; Ngoune, L.T. Essential oil of Xylopia aethiopica from Cameroon: Chemical composition, antiradical and in vitro antifungal activity against some mycotoxigenic fungi. J. King Saud. Univ.-Sci. 2018, 30, 466–471. [Google Scholar] [CrossRef]
  51. Pavela, R.; Maggi, F.; Iannarelli, R.; Benelli, G. Plant extracts for developing mosquito larvicides: From laboratory to the field, with insights on the modes of action. Acta Trop. 2019, 193, 236–271. [Google Scholar] [CrossRef]
  52. Pavela, R.; Sedlák, P. Post-application temperature as a factor influencing the insecticidal activity of essential oil from Thymus vulgaris. Ind. Crops Prod. 2018, 113, 46–49. [Google Scholar] [CrossRef]
  53. Pavela, R.; Pavoni, L.; Bonacucina, G.; Cespi, M.; Cappellacci, L.; Petrelli, R.; Spinozzi, E.; Aguzzi, C.; Zeppa, L.; Ubaldi, M.; et al. Encapsulation of Carlina acaulis essential oil and carlina oxide to develop long-lasting mosquito larvicides: Microemulsions versus nanoemulsions. J. Pest Sci. 2021, 94, 899–915. [Google Scholar] [CrossRef]
  54. Suresh, U.; Murugan, K.; Panneerselvam, C.; Aziz, A.T.; Cianfaglione, K.; Wang, L.; Maggi, F. Encapsulation of sea fennel (Crithmum maritimum) essential oil in nanoemulsion and SiO2 nanoparticles for treatment of the crop pest Spodoptera litura and the dengue vector Aedes aegypti. Ind. Crops Prod. 2020, 158, 113033. [Google Scholar] [CrossRef]
  55. Desneux, N.; Decourtye, A.; Delpuech, J.M. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 2007, 52, 81–106. [Google Scholar] [CrossRef]
  56. Stepanycheva, E.; Petrova, M.; Chermenskaya, T.; Pavela, R. Fumigant effect of essential oils on mortality and fertility of thrips Frankliniella occidentalis Perg. Environ. Sci. Pollut. Res. 2019, 26, 30885–30892. [Google Scholar] [CrossRef]
  57. Pavela, R. Sublethal effects of some essential oils on the cotton leafworm Spodoptera littoralis (Boisduval). J. Essent. Oil Bear. Plants 2012, 15, 144–156. [Google Scholar] [CrossRef]
  58. Chellappandian, M.; Thanigaivel, A.; Vasantha-Srinivasan, P.; Edwin, E.S.; Ponsankar, A.; Selin-Rani, S.; Kalaivani, K.; Senthil-Nathan, S.; Benelli, G. Toxicological effects of Sphaeranthus indicus Linn. (Asteraceae) leaf essential oil against human disease vectors, Culex quinquefasciatus Say and Aedes aegypti Linn., and impacts on a beneficial mosquito predator. Environ. Sci. Pollut. Res. 2018, 25, 10294–10306. [Google Scholar] [CrossRef]
  59. Thanigaivel, A.; Vasantha-Srinivasan, P.; Edwin, E.S.; Ponsankar, A.; Selin-Rani, S.; Chellappandian, M.; Kalaivani, K.; Senthil-Nathan, S.; Benelli, G. Development of an eco-friendly mosquitocidal agent from Alangium salvifolium against the dengue vector Aedes aegypti and its biosafety on the aquatic predator. Environ. Sci. Pollut. Res. 2018, 25, 10340–10352. [Google Scholar] [CrossRef]
  60. Benelli, G.; Ricciardi, R.; Romano, D.; Cosci, F.; Stefanini, C.; Lucchi, A. Wing-fanning frequency as a releaser boosting male mating success—High-speed video analysis of courtship behavior in Campoplex capitator, a parasitoid of Lobesia botrana. Insect Sci. 2019, 27, 1298–1310. [Google Scholar] [CrossRef]
  61. Pavela, R.; Morshedloo, M.R.; Mumivand, H.; Khorsand, G.J.; Karami, A.; Maggi, F.; Desneux, N.; Benelli, G. Phenolic monoterpene-rich essential oils from apiaceae and lamiaceae species: Insecticidal activity and safety evaluation on non-target earthworms. Entomol. Gen. 2020, 40, 421–435. [Google Scholar] [CrossRef]
  62. Pavela, R.; Žabka, M.; Vrchotová, N.; Tříska, J. Effect of foliar nutrition on the essential oil yield of Thyme (Thymus vulgaris L.). Ind. Crops Prod. 2018, 112, 762–765. [Google Scholar] [CrossRef]
  63. Benelli, G.; Pavela, R.; Iannarelli, R.; Petrelli, R.; Cappellacci, L.; Cianfaglione, K.; Afshar, F.H.; Nicoletti, M.; Canale, A.; Maggi, F. Synergized mixtures of Apiaceae essential oils and related plant-borne compounds: Larvicidal effectiveness on the filariasis vector Culex quinquefasciatus Say. Ind. Crops Prod. 2017, 96, 186–195. [Google Scholar] [CrossRef]
  64. Pavela, R.; Sajfrtová, M.; Sovová, H.; Bárnet, M. The insecticidal activity of Satureja hortensis L. extracts obtained by supercritical fluid extraction and traditional extraction techniques. Appl. Entomol. Zool. 2008, 43, 377–382. [Google Scholar] [CrossRef]
  65. Benelli, G.; Pavel, R.; Zorzetto, C.; Sanchez-Mateo, C.C.; Santini, G.; Canale, A.; Maggi, F. Insecticidal activity of the essential oil from Schizogyne sericea (Asteraceae) on four insect pests and two non-target species. Entomol. Gen. 2019, 39, 9–18. [Google Scholar] [CrossRef]
  66. Abbott, W.S. A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 1925, 18, 265–267. [Google Scholar] [CrossRef]
  67. Finney, D.J. Probit Analysis; Cambridge University Press: Cambridge, UK, 1971. [Google Scholar]
Table
Table 1. Chemical composition of the essential oils extracted from seeds of Monodora myristica, Aframomum citratum, and Xylopia aethiopica.
Table 1. Chemical composition of the essential oils extracted from seeds of Monodora myristica, Aframomum citratum, and Xylopia aethiopica.
Relative % in Essential Oil
Component aRI Calc. bRI Lit. cM. myristicadX. aethiopicaA. citratumMethod of Identification e
α-Thujene9209243.1 ± 0.61.9 ± 0.4tr fRI,MS
α-Pinene9259327.6 ± 1.29.6 ± 1.61.0 ± 0.2Std
Camphene938946 0.1 ± 0.0 Std
Thuja-2,4(10)-diene944953 tr RI,MS
Sabinene9669690.1 ± 0.026.1 ± 3.1 Std
β-Pinene9689740.3 ± 0.017.4 ± 1.95.4 ± 0.9Std
Myrcene9889884.3 ± 0.80.2 ± 0.00.1 ± 0.0Std
δ-2-carene99810010.9 ± 0.0 0.1 ± 0.0RI,MS
α-Phellandrene1002100232.3 ± 3.60.3 ± 0.0 Std
α-Terpinene101310140.1 ± 0.01.9 ± 0.4 Std
p-Cymene1021102032.8 ± 3.01.1 ± 0.20.1 ± 0.0Std
Limonene102410244.4 ± 0.9 0.3 ± 0.1Std
β-Phellandrene10241025 6.2 ± 1.2 Std
1,8-Cineole10261026 3.6 ± 0.70.7 ± 0.2Std
(Z)-β-Ocimene103610320.3 ± 0.01.2 ± 0.3trStd
(E)-β-Ocimene104610440.1 ± 0.00.1 ± 0.00.3 ± 0.0Std
α-Terpinene105410540.1 ± 0.03.2 ± 0.6trStd
cis-Sabinene hydrate10621065 1.3 ± 0.3 RI,MS
cis-Linalool oxide10691067 trRI,MS
Terpinolene10841086tr0.6 ± 0.2 Std
trans-Sabinene hydrate10931098 0.8 ± 0.2 RI,MS
Linalool110010951.9 ± 0.40.1 ± 0.02.4 ± 0.5Std
cis-p-Menth-2-en-1-ol111711180.2 ± 0.00.3 ± 0.0 RI,MS
α-Campholenal11221122tr0.1 ± 0.0 RI,MS
allo-Ocimene11281128 0.1 ± 0.0 RI,MS
trans-Pinocarveol11311135 0.4 ± 0.1trStd
trans-p-Menth-2-en-1-ol113511360.1 ± 0.00.2 ± 0.0 RI,MS
trans-Verbenol11401140 0.1 ± 0.0 RI,MS
Pinocarvone11561160 0.2 ± 0.0 RI,MS
Borneol115911650.1 ± 0.0tr Std
p-Mentha-1,5-dien-8-ol11641166 tr RI,MS
cis-Pinocamphone11671172 tr RI,MS
Terpinen-4-ol11721174 6.1 ± 1.1trStd
p-Cymen-8-ol118311790.1 ± 0.0 RI,MS
Cryptone11811183 0.1 ± 0.0 RI,MS
α-Terpineol118611860.5 ± 0.11.0 ± 0.20.3 ± 0.0RI,MS
Myrtenal11891195 0.2 ± 0.0trStd
Myrtenol11911194 0.4 ± 0.1 Std
trans-Piperitol120312070.1 ± 0.0 RI,MS
Verbenone12041204 0.1 ± 0.0 RI,MS
Cuminaldehyde12361238 tr RI,MS
Neral12391235 0.5 ± 0.2RI,MS
Carvotanacetone124312440.1 ± 0.0 RI,MS
Geraniol12641249 85.6 ± 2.8Std
Geranial12721264 1.9 ± 0.4Std
Carvacrol130312980.6 ± 0.2 Std
δ-Elemene13311335 1.8 ± 0.4 RI,MS
α-Cubebene13431345 0.1 ± 0.0 RI,MS
α-Ylangene13621373 0.2 ± 0.0 RI,MS
α-Copaene136713740.1 ± 0.00.4 ± 0.1 RI,MS
β-Cubebene13821387 0.1 ± 0.0 RI,MS
β-Elemene13851389 0.2 ± 0.0 Std
Geranyl acetate13851379 0.8 ± 0.2RI,MS
Cyperene13871398 0.1 ± 0.0RI,MS
(E)-Caryophyllene14081417 trStd
cis-α-Bergamotene140814110.1 ± 0.0 RI,MS
β-Ylangene14081419 0.2 ± 0.0 RI,MS
α-Santalene141214160.5 ± 0.1 RI,MS
β-Copaene14191430 0.1 ± 0.0 RI,MS
γ-Elemene14261434 0.3 ± 0.0 RI,MS
trans-α-Bergamotene14301432tr RI,MS
6,9-Guaiadiene14341442 0.1 ± 0.0 RI,MS
α-Humulene14421452tr0.1 ± 0.0 Std
Germacrene D14711484 9.7 ± 1.6 RI,MS
Bicyclogermacrene14861500 0.5 ± 0.2 RI,MS
α-Muurolene149215000.1 ± 0.0tr RI,MS
δ-Amorphene14981511 0.1 ± 0.0 RI,MS
γ-Cadinene150415130.3 ± 0.00.1 ± 0.0 RI,MS
δ-Cadinene151615221.2 ± 0.30.3 ± 0.1 RI,MS
α-Cadinene15281537tr RI,MS
Germacrene B15441559 0.3 ± 0.1 RI,MS
epi-α-Cadinol163116380.1 ± 0.0 RI,MS
epi-α-Muurolol164516400.1 ± 0.0 RI,MS
Manool oxide19911987 0.1 ± 0.0 RI,MS
Total identified (%) 92.999.699.9
Number of identified compounds 355523
Grouped compounds (%)
Monoterpene hydrocarbons 86.569.87.4
Oxygenated monoterpenes 3.815.091.5
Sesquiterpene hydrocarbons 2.414.60.2
Oxygenated sesquiterpenes 0.2--
Others tr0.20.9
a Order of components according to their elution from a HP-5MS column. b RI calc.: calculated linear retention index using a mix of n-alkanes (C8–C30). c RI lit.: retention index reported from the literature. d Peak area percentage as the mean of three injections (different solution preparations) ± standard deviation. e Method of identification: Std, comparison of RI and MS with that of analytical standard; RI, coherence of the linear retention index with those reported in literature; MS, mass fragmentation overlapping with those stored in commercial libraries. f tr: trace.
Table
Table 2. Insecticidal activity of Monodora myristica, Aframomum citratum, and Xylopia aethiopica seed essential oils and their major constituents on Musca domestica adults.
Table 2. Insecticidal activity of Monodora myristica, Aframomum citratum, and Xylopia aethiopica seed essential oils and their major constituents on Musca domestica adults.
Musca domestica—FemaleMusca domestica—Male
LD50 (µg adult−1)CI95LC90 (µg adult−1)CI95χ2dfp-valueLD50 (µg adult−1)CI95LC90 (µg adult−1)CI95χ2dfp-Value
Essential oils
Monodora myristica29.118.5–42.8137.6128.5–152.74.76340.32122.115.7–26.9127.6111.2–136.72.46540.144
Aframomum citratum48.943.5–65.7373.5301.8–421.72,57450.25380.569.7–91.5160.2155.7–189.52.21540.286
Xylopia aethiopica30.722.5–40.8164.2135.7–178.91.68230.64161.555.7–65.7178.5156.7–192.95.12540.562
Major compounds
Geraniol151.5111.5–182.7288.7232.5–302.83.45530.45223.517.6–29.3126.1111.5–148.91.51830.687
Sabinene109.785.7–122.5213.8195.7–252.73.45230.65210.48.2–15.9117.598.6–135.92.45230.128
α-Pinene69.751.5–78.8254.7212.2–278.92.75130.4288.67.2–15.9100.287.5–120.94.25630.318
p-Cymene28.416.5–31.9131.7118.5–145.75.12340.25132.628.9–51.6145.6126.9–158.72.24630.257
α-Phellandrene43.535.5–48.9187.9175.7–201.53.45640.42546.739.7–56.2178.9156.8–193.31.15230.562
β-Pinene56.142.8–65.3316.5289.7–324.72.24540.15639.733.5–42.8189.7165.9–195.52.85240.349
Table
Table 3. Insecticidal activity of Monodora myristica, Aframomum citratum, and Xylopia aethiopica essential oils and their major constituents on Spodoptera littoralis third instar larvae.
Table 3. Insecticidal activity of Monodora myristica, Aframomum citratum, and Xylopia aethiopica essential oils and their major constituents on Spodoptera littoralis third instar larvae.
LC50 (µg larva−1)CI95LC90 (µg larva−1)CI95χ2dfp-Value
Essential oils
Monodora myristica29.321.5–37.1123.5102.5–148.71.66330.645
Aframomum citratum31.123.6–39.7130.2118.7–142.61.07630.782
Xylopia aethiopica60.352.8–71.5155.6128.7–165.51.72130.632
Major compounds
Geraniol25.219.7–28.683.272.9–105.61.47830.687
Sabinene45.138.9–52.3240.4201.8–259.71.37830.711
α-Pinene123.5111.5–138.7198.7179.6–222.12.52830.477
p-Cymene52.344.1–60.5112.298.7–125.92.14730.542
α-Phellandrene54.643.7–66.1143.7132.6–169.51.64230.649
β-Pinene84.572.8–101.8226.5212.5–257.83.45830.117
Table
Table 4. Insecticidal activity of Monodora myristica, Aframomum citratum, and Xylopia aethiopica essential oils and their major constituents on Culex quinquefasciatus third instar larvae.
Table 4. Insecticidal activity of Monodora myristica, Aframomum citratum, and Xylopia aethiopica essential oils and their major constituents on Culex quinquefasciatus third instar larvae.
LC50 (µg mL−1)CI95LC90 (µg mL−1)CI95χ2dfp-Value
Essential oils
Monodora myristica35.325.1–42.366.155.8–72,43.23630.356
Aframomum citratum82.775.1–90.3160.1149.8–196.53.00330.391
Xylopia aethiopica47.038.7–52.278.463.9–92.75.24530.079
Major compounds
Geraniol98.191.5–104.8153.3138.9–165.71.01130.798
Sabinene64.460.1–68.5102.393.5–116.70.31130.998
α-Pinene74.566.1–81.5144.7128.5–172.71.18330.686
p-Cymene26.821.5–37.956.542.7–75.93.52630.161
α-Phellandrene36.825.7–51.385.172.8–95.93.51230.318
β-Pinene66.161.3–70.5109.3100.2–123.10.08940.999
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Wandjou, J.G.N.; Baldassarri, C.; Ferrati, M.; Maggi, F.; Pavela, R.; Tsabang, N.; Petrelli, R.; Ricciardi, R.; Desneux, N.; Benelli, G. Essential Oils from Cameroonian Aromatic Plants as Effective Insecticides against Mosquitoes, Houseflies, and Moths. Plants 2022, 11, 2353. https://doi.org/10.3390/plants11182353

AMA Style

Wandjou JGN, Baldassarri C, Ferrati M, Maggi F, Pavela R, Tsabang N, Petrelli R, Ricciardi R, Desneux N, Benelli G. Essential Oils from Cameroonian Aromatic Plants as Effective Insecticides against Mosquitoes, Houseflies, and Moths. Plants. 2022; 11(18):2353. https://doi.org/10.3390/plants11182353

Chicago/Turabian Style

Wandjou, Joice G. Nkuimi, Cecilia Baldassarri, Marta Ferrati, Filippo Maggi, Roman Pavela, Nole Tsabang, Riccardo Petrelli, Renato Ricciardi, Nicolas Desneux, and Giovanni Benelli. 2022. "Essential Oils from Cameroonian Aromatic Plants as Effective Insecticides against Mosquitoes, Houseflies, and Moths" Plants 11, no. 18: 2353. https://doi.org/10.3390/plants11182353

APA Style

Wandjou, J. G. N., Baldassarri, C., Ferrati, M., Maggi, F., Pavela, R., Tsabang, N., Petrelli, R., Ricciardi, R., Desneux, N., & Benelli, G. (2022). Essential Oils from Cameroonian Aromatic Plants as Effective Insecticides against Mosquitoes, Houseflies, and Moths. Plants, 11(18), 2353. https://doi.org/10.3390/plants11182353

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