Next Article in Journal
Update on COVID-19 Therapy in Pediatric Age
Next Article in Special Issue
Synergistic and Antibiofilm Effects of the Essential Oil from Croton conduplicatus (Euphorbiaceae) against Methicillin-Resistant Staphylococcus aureus
Previous Article in Journal
3-(1,2,3-Triazol-4-yl)-β-Carbolines and 3-(1H-Tetrazol-5-yl)-β-Carbolines: Synthesis and Evaluation as Anticancer Agents
Previous Article in Special Issue
Hydrosols of Veronica Species—Natural Source of Free Volatile Compounds with Potential Pharmacological Interest
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

The Essential Oil from the Resurrection Plant Myrothamnus moschatus Is Effective against Arthropods of Agricultural and Medical Interest

1
Crop Research Institute, Drnovska 507, 161 06 Prague, Czech Republic
2
Department of Plant Protection, Czech University of Life Sciences Prague, Kamycka 129, 165 00 Praha 6, Czech Republic
3
Chemistry Interdisciplinary Project (ChIP), School of Pharmacy, University of Camerino, 62032 Camerino, Italy
4
Centre National d’Application de Recherches Pharmaceutiques, Antananarivo 101, Madagascar
5
Department of Agriculture, Food and Environment, University of Pisa, via del Borghetto 80, 56124 Pisa, Italy
*
Author to whom correspondence should be addressed.
Pharmaceuticals 2022, 15(12), 1511; https://doi.org/10.3390/ph15121511
Submission received: 12 November 2022 / Revised: 29 November 2022 / Accepted: 1 December 2022 / Published: 3 December 2022

Abstract

:
This work aimed to evaluate the chemical composition, insecticidal and acaricidal potential of the essential oil (EO) obtained from the resurrection plant Myrothamnus moschatus (Baill.) Baill. (Myrothamnaceae) from Madagascar. The EO bioactivity was evaluated against selected arthropod pests and vectors of agricultural and public health relevance. The most abundant volatile compounds were trans-pinocarveol (37.7 ± 4.2%) and pinocarvone (20.8 ± 3.1%), similar to the EO of the chemotype collected from the same region. Lethal concentrations (LC50) or doses (LD50) from acute toxicity tests were estimated for Musca domestica (L.) adults at 22.7 µg adult−1, for Spodoptera littoralis (Boisduval) larvae at 35.6 µg larva−1, for Culex quinquefasciatus (Say) at 43.6 µg mL−1, for adults of Metopolophium dirhodum (Walker) at 2.4 mL L−1, and for adults of Tetranychus urticae (Koch) at 1.2 mL L−1. The good insecticidal and acaricidal activities determined in this work may open a new perspective on the use of this plant as a source of botanical insecticide ingredients. The exploitation of this species could also be important for the African economy, helping local farmers cultivating this plant.

1. Introduction

In the last century, the world population has risen dramatically, and it is estimated that by 2050 food production will have to increase by 70% [1]. To guarantee a wide crop’s effectiveness, pesticides play a fundamental role. They can reduce the development of several plant diseases and ensure the recovery of 30–40% of crop losses worldwide [2,3]. However, conventional chemical pesticides can be toxic to other beneficial organisms and non-target plants, as well as to air, water, and soil, resulting in environmental pollution and a threat to human health [2]. Moreover, long-lasting uses of pesticides can often lead to resistance phenomena in the targeted arthropod populations [4].
For the above reason, there has been a growing global interest in eco-friendly pesticides, including those produced by plants [5,6,7]. Among botanical products, essential oils (EOs) could play a fundamental role in the agrochemical industries, and they have been widely studied against many arthropod pests [8,9,10,11]. EOs showed different modes of action, such as antifeedant, repellent, or deterrent activities, and they can be useful as larvicide, ovicide, and adulticidal agents. Their main constituents could act at different stages of insect and mite development [12]. Moreover, EOs are often made up of several active substances with multiple modes of action that avoid the development of resistance phenomena in targeted pests [13].
Myrothamnus moschatus (Baill.) Baill. is a small dioecious shrub, endemic in Madagascar and belonging to the Myrothamnaceae family [14]. It belongs to a group of plants containing more than 1300 species that are called ‘resurrection plants’, owing to their remarkable peculiarity of being able to desiccate in a drought state and restart the photosynthetic activity once the stressed condition ends (Figure 1). Therefore, they can remain quiescent for long periods of time, ‘resurrecting’ at the first substantial fall of rain [15]. Myrothamnus moschatus has been used for many purposes, from medicinal to recreational. For instance, Malagasy people used to smoke the dried leaves to treat asthma and for their psychoactive action reminiscent of that of marijuana [16,17]. The plant is also used as an anti-emetic and to treat coughs [18], while in the central highlands, the leaves are burned during magical rituals to expel the devil [19].
In the past, ‘resurrection’ plants were mainly studied for their ability to remain quiescent under stressed conditions [20,21,22]. However, recently, interest in these plants has shifted towards the potential of their products, such as extracts and EOs. They contain many compounds that demonstrate a wide range of properties in experimental models [23,24,25]. The biological activities of the EO of M. moschatus were investigated for the first time in 2012 by Nicoletti et al. [18]. To date, this EO has shown a strong inhibition potential toward cancerous cells, as well as antifungal, anticonvulsant, and antioxidant activities [18,26]. However, there are still relatively few studies on M. moschatus EO, and, to the best of our knowledge, there are no data available on the insecticidal potential of this plant.
Therefore, the aim of this work was to assess, for the first time, the effectiveness of this plant EO against some noxious arthropod pests and vectors of agricultural and public health relevance, i.e., the rose grain aphid, Metopolophium dirhodum (Walker) (Hemiptera: Aphididae), the cotton leafworm, Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae), and the two-spotted mite, Tetranychus urticae (Koch) (Acari: Tetranychidae), as well as representative insect species of urban importance. i.e., the mosquito vector Culex quinquefasciatus (Say) (Diptera: Culicidae) and the common house fly, Musca domestica (L.) (Diptera: Muscidae).

2. Results and Discussion

The chemical variability of the M. moschatus EO observed in this study comprises 34 compounds, representing 98.2% of the total oil composition. The results obtained by GC-MS analysis are shown in Table 1. Most of the constituents are oxygenated monoterpenes (75.3%), while monoterpene hydrocarbons (12.6%) and sesquiterpene hydrocarbons (10.2%) are minor chemical classes. The most abundant volatile compounds were trans-pinocarveol (37.7 ± 4.2%) and pinocarvone (20.8 ± 3.1%), followed by β-selinene (10.2 ± 1.3%), α-pinene (8.8 ± 1.2%), and perillyl acetate (4.9 ± 0.9 %). Myrtenal (1.8 ± 0.3%), p-cymene (1.8 ± 0.4%), myrtenol (1.5 ± 0.3), trans-p-mentha-1(7),8-dien-2-ol (2.2 ± 0.4%), and cis-p-mentha-1(7),8-dien-2-ol (1.4 ± 0.3%) were detected in minor percentages.
Myrothamnus moschatus EO has been studied for its chemical variability among species of different geographical origins. It was demonstrated that the occurrence of different chemotypes depends on the plant variability, but also on the interaction with the environment and genetic selection [27]. The chemical composition of this EO is very similar to those obtained by M. moschatus plants harvested in the same region in previous studies [18,19]. Even if these latter were collected in different seasons, it was demonstrated that the environmental conditions do not influence the EO chemical composition of this species [18]. Conversely, Randrianarivo et al., [28] analyzed the EOs of M. moschatus plants growing in different areas of Madagascar. They showed many differences, depending on the plant variability, but also on the environmental parameters and genetic selection. As a confirmation, the chemotype of this work was widely different from those of plants collected in other regions. EOs of the plants harvested in the central-northern part of the island were mainly composed of oxygenated sesquiterpenes. Conversely, southern populations were mainly constituted of oxygenated monoterpenes. In particular, the chemotype of the Ifandana populations was quite comparable to that of our study [28].
Comparing our results with those reported for the other species of the genus Myrothamnus, i.e., M. flabellifolia Welw., we observed a similar profile, with trans-pinocarveol, pinocarvone, limonene, trans-p-mentha-1(7),8-dien-2-ol, cis-p-mentha-1(7),8-dien-2-ol, α-pinene, and β-selinene as the main EO component of this species [29,30]. It is worth noting that the monoterpenoid perillyl acetate, an uncommon EO constituent, was detected only in the M. moschatus species. This compound has been demonstrated to prevent carcinoma of the breast in rats [31]. The other major compounds, trans-pinocarveol and its oxidation product, pinocarvone, have been correlated to the ethnobotanical use of the plant [19]. The former seems effective against coughs, being included in pharmaceutical preparations to treat respiratory tract diseases [30], while the latter appears effective against colds [32]. These molecules are also released when the plant is smoked by Malagasy people during magic rituals [30].
To the best of our knowledge, no data are available in the literature on the insecticidal and acaricidal properties of this EO and their components. Therefore, this work represents the first investigation of its effectiveness against arthropod vectors and pests, with the aim of widening the possible application of this plant in Madagascar. The EO analyzed here showed relatively good insecticidal activity, and this EO and its main components, whenever available as chemical reagents, can be considered promising active ingredients of new botanical insecticides and acaricides. EO lethal concentrations (LC50) or doses (LD50) from acute toxicity tests (Table 2) were estimated for M. domestica adults at 22.7 µg adult−1, for S. littoralis larvae at 35.6 µg larva−1, for Cx. quinquefasciatus at 43.6 µg mL−1, for adults of M. dirhodum at 2.4 mL L−1, and for adults of T. urticae at 1.2 mL L−1. Testing a positive control is an important requirement for validating green insecticide research [33,34,35]. Table 3 reports the acute toxicity results achieved testing a positive control, i.e., a commercial botanical insecticide based on Pongamia pinnata L. (Pierre) oil, commercially known as Rock Effect (Agro CS a.s., Česká Skalice, Czech Republic) on the same arthropod targets. Lethal concentrations (LC50) or doses (LD50) from acute toxicity tests (Table 2) were estimated for M. domestica adults at >500 µg adult−1, for S. littoralis larvae at 18.2 µg larva−1, for Cx. quinquefasciatus at 275.4 µg mL−1, for adults of M. dirhodum at 12.5 mL L−1 and for adults of T. urticae at 5.8 mL L−1. Comparing M. moschatus EO (Table 2) against the positive control (Table 3) highlighted differences in efficacy depending on the target species. The LC50 of M. moschatus EO in particular was lower when tested on M. domestica adults, Cx. quinquefasciatus larvae, M. dirhodum larvae, and T. urticae adults, suggesting greater efficacy than the positive control. These promising results support the development of increasingly effective botanical insecticides for the management of key insect and mite pests.
It should be noted that aphids are generally sensitive to preparations based on EOs. Several botanical insecticides are currently produced commercially against a range of pests, including aphids [36]; for example, a US company, EcoSMART Technologies, produces a ‘Garden Insect Killer’ against sucking pests containing mint and rosemary EO, which is contained in an applied spray liquid in a total dose of 10 mL L−1. For example, for EO from Rosmarinus officinalis L., the lethal concentration for Lipaphis pseudo-brassicae Davis was estimated at 7.4 mL L−1 and for Macrosiphum rosae (L.) at 57.5 mL L−1 [8]. Our estimated lethal concentrations for M. dirhodum and T. urticae were significantly lower, indicating a promising perspective for the commercial use of M. moschatus EO. Similarly, in our work, the lethal concentration estimated for Cx. quinquefasciatus larvae was lower than 100 µg mL−1, which is generally considered to be the limit of prospective EOs usable mosquito larval management [37]. Of note, our knowledge about the modes of action of the EO’s two major constituents, trans-pinocarveol and pinocarvone, is limited. Earlier research showed that these compounds were toxic to various insect species [38,39,40,41,42,43]. For example, Seo et al. [38] demonstrated that trans-pinocarveol, used through a fumigant treatment, exhibited a strong fumigant toxicity at all concentrations (0.312, 0.625, 1.25, 2.5, 5, and 10 mg L−1) against the Japanese termite, Reticulitermes speratus Kolbe (Isoptera: Rhinotermitidae), killing all the exposed individuals; trans-pinocarveol at 1 mg mL−1 on R. speratus adults had an acetylcholinesterase (AChE) inhibition rate of between 15 and 20% [38]. trans-Pinocarveol was found among the main components of several EOs, such as that of Salvia tomentosa Mill., Eucalyptus kruseana Muel, Croton tetradenius (Baill), and Artemisia anethoides (Mattf.) [39,40,41,42,43]. Salvia tomentosa EO tested on stored product beetles i.e., Acanthoscelides obtectus (Say) (Coleoptera: Bruchidae), and Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae), E. kruseana EO tested on Rhyzopertha dominica F. (Coleoptera: Bostrichidae), C. tetradenius EO tested on Acromyrmex balzani (Emery) (Hymenoptera: Formicidae), and A. anethoides EO tested on T. castaneum and Lasioderma serricorne (Fabricius) (Coleoptera: Anobiidae) achieved good efficacy (S. tomentosa EO against T. castaneum: LC50 = 111.67 µL L−1 air, LC95 = 174.66 µL L−1 air; S. tomentosa EO against A. obtectus: LC50 = 22.47 µL L−1 air, LC95 = 41.73 µL L−1 air; R. dominica EO against E. kruseana: LC50 = 22.98 µL L−1 air, LC90 = 65.32 µL L−1 air; C. tetradenius EO against A. balzani showed LC50 values ranging from 1.47 to 2.40 μL L−1, while trans-pinocarveol obtained by C. tetradenius showed an LC50 ranging between 1.40 and 1.75 μL L−1; A. anethoides possessed contact and fumigant toxicities against T. castaneum adults (LD50 = 28.80 μg adult−1 and LC50 = 13.05 mg L−1 air, respectively) and against L. serricorne (LD50 = 24.03 μg adult−1 and LD50 = 8.04 mg L−1 air, respectively), making them potentially suitable for pest management by reducing the use of synthetic insecticides.
The insecticidal action of trans-pinocarveol and pinocarvone could be linked to their chemical structure. α,β-Unsaturated compounds are reported to be alkylating agents with mutagenic properties [43]. trans-Pinocarveol is an α, β-unsaturated alcohol, while pinocarvone belongs to the chemical class of α,β-unsaturated ketones, which are well-known alkylating compounds with marked toxicity, as are myrtenal, verbenone, and carvone. The α,β-unsaturation is responsible for improved polarizability of the ketone moiety, which leads to enhanced London dispersion-type intermolecular attractive forces [44]. These structure-related properties could be the basis of the insecticidal/acaricidal mode of action. Additional studies on these two compounds should be performed.
Further efforts to evaluate possible non-target effects of this EO on useful arthropods [45,46] as well as to improve the field stability and effectiveness of the tested botanical product through its formulation in micro- or nanoemulsions are still needed [45,47,48,49,50].

3. Material and Methods

3.1. Plant Material and Essential Oil Preparation

Aerial parts of M. moschatus were collected in September 2019 at Ifandàna, Madagascar (S 22°00′39″, E 46°23′03″). Identification of plant was performed by one of us (R.R.) at the Parc Botanique et Zoologique de Tsimbazaza, Antananarivo. The voucher specimen (code RR-0002) was deposited at the Herbarium of the Parc Botanique et Zoologique de Tsimbazaza and the Centre National d’Application des Recherches Pharmaceutiques. The EO, of transparent color, was obtained in 0.02% (w/w f.w.) from freshly collected aerial parts of M. moschatus after 3 h of steam distillation. It was stored at +4 °C until use.
Furthermore, a botanical insecticide approved for organic farming in the Czech Republic was tested as positive control on the various arthropod species mentioned above. The insecticide’s commercial name was Rock Effect (Agro CS a.s., Česká Skalice, Czech Republic) and it is a commercial formulation of P. pinnata oil. The oil content is declared as 868.5 g·L−1. It is generally used as a 1 to 3% aqueous solution.

3.2. Gas Chromatography–Mass Spectrometry (GC–MS) Analysis

The chemical composition of the M. moschatus EO was determined using an Agilent 6890 N gas chromatograph equipped with a single quadrupole 5973 N mass spectrometer and an auto-sampler 7863 (Agilent, Wilmington, DE). The separation of the compounds was achieved with an HP-5 MS capillary column (30 m, 0.25 μm i.d., 0.1 μm f.t.; 5% phenylmethylpolysiloxane), provided by Agilent (Folsom, CA, USA). The conditions of the analysis and the identification method for each compound were the same as that reported by Pavela et al. [51].

3.3. Insecticidal and Acaricidal Experiments

3.3.1. Target Organisms

Metopolophium dirhodum aphids, S. littoralis moths, T. urticae mites, Cx. quinquefasciatus, and M. domestica were tested. These species have been reared under controlled laboratory conditions for more than 20 generations. The following uniform individuals were selected for the experiments: M. dirhodum adults (1–2 days old), S. littoralis larvae (3rd instar, larval weight 10.2 ± 3.1 mg), Cx. quinquefasciatus larvae (early 3rd instar), M. domestica adults (female, 2–5 days old), and T. urticae adults (2–3 days old).
Arthropod mass-rearing in brief: M. dirhodum was reared on wheat plants in pots with a diameter of 10 cm; S. littoralis was reared on a semi-synthetic diet developed in the CRI laboratory that was based on soybean meal, agar, and vitamins; adults were fed honey solution and allowed to mate and lay eggs on prepared filter paper; T. urticae was reared on beans (Phaseolus vulgaris L.) planted in 10 cm diameter pots filled with a common garden substrate, and placed in a growth chamber [51]; larvae of Cx. quinquefasciatus were fed dried dog biscuits, adults were allowed to mate, and the females were given blood so that they could complete the development of the eggs, which they then laid in prepared containers of water; larvae of M. domestica were reared on a semi-synthetic diet developed at CRI consisting of a mixture of milk, agar, and sawdust; adults were fed powdered milk and sugar solution, eggs were laid on cotton wool dipped in sweet milk.
All arthropod species were maintained at 25 ± 1 °C, 70 ± 3% R.H., and 16:8 h (L:D). All experiments described below were performed under the same conditions.

3.3.2. Insecticidal and Acaricidal Activity

The EO was dissolved in acetone to obtain a series of concentrations that, when applied at 1 µL, gave the following doses: for houseflies 10, 20, 30, 50, 80, and 100 µg adult−1; for moth larvae 20, 30, 40, 50, 60, and 80 µg larva−1. Before application, the arthropods were immobilized using CO2. As a negative control, acetone alone (Sigma-Aldrich, Czech Republic) was used in the experiments. After application, the adults and larvae were transferred to rearing containers with dimensions of 15 × 12 × 8 cm with a perforated lid, and the usual food. Twenty individuals were used for each repetition, and the experiment was repeated 4 times.
In tests targeting larvae of Cx. quinquefasciatus, EO was mixed in dimethyl sulfoxide (DMSO, Sigma-Aldrich, Czech Republic) and tested according to WHO (1996) with minor modifications by Pavela and Sedlák [52]. Each time, 1 mL of DMSO, containing a defined amount of EO, was mixed in 99 mL of water, and a concentration series containing 20, 40, 60, 80, and 100 mg mL−1 of EO was prepared. DMSO alone was used as a negative control. For each replicate, 20 larvae were used, and the experiment was repeated 4 times.
In tests targeting M. dirhodum and T. urticae, EO was mixed in Tween 80 (Sigma-Aldrich, Czech Republic) in a 1:1 (v:v) ratio. Subsequently, a concentration series was prepared (1.5, 2.0, and 3.0, 4.0, and 5.0 mL L−1, or 0.5, 1.0, 1.5, 2.0, and 3.0 mL L−1 for M. dirhodum and T. urticae, respectively) by thoroughly mixing the modified EO in water. Adults of M. dirhodum were transferred to wheat leaves using a fine brush (20 adults per plant in a 9 cm diameter pot); T. urticae adults were also transferred with a fine brush to bean leaves (20 adults per plant in a 9 cm diameter pot). The plants were sprayed using an electric applicator (5 mL of solution per plant). The experiment was replicated 5 times. For all tested species, the positive control was the commercial pesticide Rock Effect, a.i. P. pinnata oil.
Arthropod mortality was assessed 24 h after treatment. Mortality was corrected using Abbott’s formula [53] (Abbott 1925); LD50(90) and LC50(90) were estimated by probit analysis [54].

4. Conclusions

The findings of our work may open a new perspective on the use of M. moschatus in Madagascar as a source of botanical insecticide and acaricide ingredients. One of the advantages of this plant species is its ease of cultivation and growth in arid and semi-arid areas, offering the possibility to extract its EO in both dry and wet seasons. Thus, following the example of pyrethrum [55], M. moschatus may represent a new non-food cash crop to produce pesticidal products by Malagasy smallholder farmers. A future challenge born from this work is to prepare an artificial blend made up of the main EO constituents, such as trans-pinocarveol and pinocarvone, and to test it in insecticidal and acaricidal assays. However, difficulty in supplying these compounds may limit this applied research. Therefore, new synthetic or extractive approaches for these compounds should be pursued to have high disposability of these chemicals for agrochemical purposes.

Author Contributions

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

Funding

Financial support for this work was provided by the Ministry of Agriculture of the Czech Republic (Project MZE-RO0418).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

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 they have no conflicts of interest.

References

  1. Poveda, J. Insect frass in the development of sustainable agriculture. A review. Agron. Sustain. Dev. 2021, 41, 5. [Google Scholar] [CrossRef]
  2. Tudi, M.; Daniel Ruan, H.; Wang, L.; Lyu, J.; Sadler, R.; Connell, D.; Chu, C.; Phung, D.T. Agriculture Development, Pesticide Application and Its Impact on the Environment. Int. J. Environ. Res. Public Health 2021, 18, 1112. [Google Scholar] [CrossRef]
  3. Zhao, J.; Liang, D.; Li, W.; Yan, X.; Qiao, J.; Caiyin, Q. Research Progress on the Synthetic Biology of Botanical Biopesticides. Bioengineering 2022, 9, 207. [Google Scholar] [CrossRef] [PubMed]
  4. Benelli, G.; Pavela, R.; Petrelli, R.; Nzekoue, F.K.; Cappellacci, L.; Lupidi, G.; Quassinti, L.; Bramucci, M.; Sut, S.; Dall’Acqua, S.; et al. Carlina oxide from Carlina acaulis root essential oil acts as a potent mosquito larvicide. Ind. Crops Prod. 2019, 137, 356–366. [Google Scholar] [CrossRef]
  5. Tataridas, A.; Kanatas, P.; Chatzigeorgiou, A.; Zannopoulos, S.; Travlos, I. Sustainable crop and weed management in the era of the EU Green Deal: A survival guide. Agronomy 2022, 12, 589. [Google Scholar] [CrossRef]
  6. Tian, T.; Sun, B.; Li, H.; Li, Y.; Gao, T.; Li, Y.; Zeng, Q.; Wang, Q. Commercialization and Regulatory Requirements of Biopesticides in China. In Agriculturally Important Microorganisms; Singh, H.B., Sarma, B.K., Keswani, C., Eds.; Springer: Singapore, 2016; Volume 1, pp. 237–254. [Google Scholar] [CrossRef]
  7. Zoubiri, S.; Baaliouamer, A. Potentiality of plants as source of insecticide principles. J. Saudi Chem. Soc. 2014, 18, 925–938. [Google Scholar] [CrossRef]
  8. Ikbal, C.; Pavela, R. Essential oils as active ingredients of botanical insecticides against aphids. J. Pest Sci. 2019, 92, 971–986. [Google Scholar] [CrossRef]
  9. 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]
  10. Benelli, G.; Pavela, R.; Maggi, F.; Wandjou, J.G.N.; Koné-Bamba, D.; Sagratini, G.; Vittori, S.; Caprioli, G. Insecticidal activity of the essential oil and polar extracts from Ocimum gratissimum grown in Ivory Coast: Efficacy on insect pests and vectors and impact on non-target species. Ind. Crops Prod. 2019, 132, 377–385. [Google Scholar] [CrossRef]
  11. Giordani, C.; Spinozzi, E.; Baldassarri, C.; Ferrati, M.; Cappellacci, L.; Nieto, D.S.; Pavela, R.; Ricciardi, R.; Benelli, G.; Petrelli, R.; et al. Insecticidal Activity of Four Essential Oils Extracted from Chilean Patagonian Plants as Potential Organic Pesticides. Plants 2022, 11, 2012. [Google Scholar] [CrossRef]
  12. Sarma, R.; Adhikari, K.; Mahanta, S.; Khanikor, B. Combinations of plant essential oil based terpene compounds as larvicidal and adulticidal agent against Aedes aegypti (Diptera: Culicidae). Sci. Rep. 2019, 9, 9471. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Lavoir, A.V.; Michel, T.; Poëssel, J.L.; Siegwart, M. Challenges in Developing Botanical Biopesticides for Pest Control. In Extended Biocontrol; Fauvergue, X., Rusch, A., Barret, M., Bardin, M., Jacquin-Joly, M., Malausa, T., Lannou, C., Eds.; Springer: Dordrecht, The Netherlands, 2022; Volume 3, pp. 161–170. [Google Scholar] [CrossRef]
  14. Millogo-Rasolodimby, J. Myrothamnaceae, Famille 94. In Flore de Madagascar et des Comores; Publications du Museum National d’Historie Naturelle: Paris, France, 1991; pp. 81–85. [Google Scholar]
  15. Scott, P. Resurrection plants and the secrets of eternal leaves. Ann. Bot. 2000, 85, 159–166. [Google Scholar] [CrossRef] [Green Version]
  16. Boiteau, P. Sur deux plantes autochtones de Madagascar utilisées à la manière du Chanvre comme stupéfiant. Comptes Rendus Acad. Sci. 1967, 264, 41–42. [Google Scholar]
  17. Razafindrambao, R. Contribution à l’inventaire des Plantes Médicinales des Hauts Plateaux de Madagascar. In Contribution à L’Inventaire des Plantes Médicinales de Madagascar; Debray, M., Jacquemin, H., Razafindrambao, R., Eds.; ORSTOM: Paris, France, 1971; pp. 49–150. [Google Scholar]
  18. Nicoletti, M.; Maggi, F.; Papa, F.; Vittori, S.; Quassinti, L.; Bramucci, M.; Lupidi, G.; Petrelli, D.; Vitali, L.A.; Ralaibia, E.; et al. In vitro biological activities of the essential oil from the ‘resurrection plant’ Myrothamnus moschatus (Baillon) Niedenzu endemic to Madagascar. Nat. Prod. Res. 2012, 26, 2291–2300. [Google Scholar] [CrossRef] [PubMed]
  19. Rasoanaivo, P.; Ralaibia, E.; Maggi, F.; Papa, F.; Vittori, S.; Nicoletti, M. Phytochemical investigation of the essential oil from the ‘resurrection plant’ Myrothamnus moschatus (Baillon) Niedenzu endemic to Madagascar. J. Essent. Oil Res. 2012, 24, 299–304. [Google Scholar] [CrossRef]
  20. Suarez Rodriguez, M.C.; Edsgärd, D.; Hussain, S.S.; Alquezar, D.; Rasmussen, M.; Gilbert, T.; Nielsen, B.H.; Bartels, D.; Mundy, J. Transcriptomes of the desiccation-tolerant resurrection plant Craterostigma plantagineum. Plant J. 2010, 63, 212–228. [Google Scholar] [CrossRef] [PubMed]
  21. Yobi, A.; Wone, B.W.; Xu, W.; Alexander, D.C.; Guo, L.; Ryals, J.A.; Oliver, M.J.; Cushman, J.C. Comparative metabolic profiling between desiccation-sensitive and desiccation-tolerant species of Selaginella reveals insights into the resurrection trait. Plant J. 2012, 72, 983–999. [Google Scholar] [CrossRef]
  22. Yobi, A.; Wone, B.W.; Xu, W.; Alexander, D.C.; Guo, L.; Ryals, J.A.; Oliver, M.J.; Cushman, J.C. Metabolomic profiling in Selaginella lepidophylla at various hydration states provides new insights into the mechanistic basis of desiccation tolerance. Mol. Plant 2013, 6, 369–385. [Google Scholar] [CrossRef] [Green Version]
  23. Cheng, X.L.; Ma, S.C.; Yu, J.D.; Yang, S.Y.; Xiao, X.Y.; Hu, J.Y.; Lu, Y.; Shaw, P.C.; But, P.P.H.; Lin, R.C. Selaginellin A and B, two novel natural pigments isolated from Selaginella tamariscina. Chem. Pharm. Bull. 2008, 56, 982–984. [Google Scholar] [CrossRef]
  24. Gao, L.L.; Yin, S.L.; Li, Z.L.; Sha, Y.; Pei, Y.H.; Shi, G.; Jing, Y.; Hua, H. Three novel sterols isolated from Selaginella tamariscina with antiproliferative activity in leukemia cells. Planta Med. 2007, 73, 1112–1115. [Google Scholar] [CrossRef]
  25. Kamng’ona, A.; Moore, J.P.; Lindsey, G.; Brandt, W. Inhibition of HIV-1 and M-MLV reverse transcriptases by a major polyphenol (3,4,5 tri-O-galloylquinic acid) present in the leaves of the South African resurrection plant, Myrothamnus flabellifolia. J. Enzym. Inhib. Med. Chem. 2011, 26, 843–853. [Google Scholar] [CrossRef] [PubMed]
  26. Randrianarivo, E.; Maggi, F.; Nicoletti, M.; Rasoanaivo, P. Evaluation of the anticonvulsant activity of the essential oil of Myrothamnus moschatus in convulsion induced by pentylenetetrazole and picrotoxin. Asian Pac. J. Trop. Biomed. 2016, 6, 501–505. [Google Scholar] [CrossRef] [Green Version]
  27. Van den Dool, H.; Kratz, P.D. A generalization of the retention index system including linear temperature programmed gas-liquidpartition chromatography. J. Chromatogr. 1963, 2, 463–471. [Google Scholar] [CrossRef]
  28. Randrianarivo, E.; Rasoanaivo, P.; Nicoletti, M.; Razafimahefa, S.; Lefebvre, M.; Papa, F.; Vittori, S.; Maggi, F. Essential-Oil Polymorphism in the ‘Resurrection Plant’ Myrothamnus moschatus and Associated Ethnobotanical Knowledge. Chem. Biodivers. 2013, 10, 1987–1998. [Google Scholar] [CrossRef]
  29. Chagonda, L.S.; Makanda, C.; Chalcat, J.C. Essential oils of four wild and semi-wild plants from Zimbabwe: Colospermum mopane (Kirk ex Benth.) Kirk ex Leonard, Helichrysum splendidum (Thunb.) Less, Myrothamnus flabellifolia (Welw.) and Tagetes minuta L. J. Essent. Oil Res. 1999, 11, 573–578. [Google Scholar] [CrossRef]
  30. Viljoen, A.M.; Klepser, M.E.; Ernst, E.J.; Keele, D.; Roling, E.; Van Vuuren, S.; Demirci, B.; BaSer, K.H.C.; van Wyk, B.-E.; Jäger, A.K. The composition and antimicrobial activity of the essential oil of the resurrection plant Myrothamnus flabellifolius. S. Afr. J. Bot. 2002, 68, 100–105. [Google Scholar] [CrossRef] [Green Version]
  31. Haag, J.D.; Gould, M.N. Mammary carcinoma regression induced by perillyl alcohol, a hydroxylated analog of limonene. Cancer Chemother. Pharmacol. 1994, 34, 477–483. [Google Scholar] [CrossRef]
  32. Kerrola, K.; Galambosi, B.; Kallio, H. Volatile components and odor intensity of four phenotypes of Hyssop (Hyssopus officinalis L.). J. Agric. Food Chem. 1994, 42, 776–781. [Google Scholar] [CrossRef]
  33. Isman, M.B.; Grieneisen, M.L. Botanical insecticide research: Many publications, limited useful data. Trends Plant Sci. 2014, 19, 140–145. [Google Scholar] [CrossRef]
  34. Ribeiro, L.P.; Akhtar, Y.; Vendramim, J.D.; Isman, M.B. Comparative bioactivity of selected seed extracts from Brazilian Annona species and an acetogenin-based commercial bioinsecticide against Trichoplusia ni and Myzus persicae. Crop Prot. 2014, 62, 100–106. [Google Scholar] [CrossRef]
  35. de Souza Tavares, W.; Akhtar, Y.; Gonçalves, G.L.P.; Zanuncio, J.C.; Isman, M.B. Turmeric powder and its derivatives from Curcuma longa rhizomes: Insecticidal effects on cabbage looper and the role of synergists. Sci. Rep. 2016, 6, 34093. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Isman, M.B. Botanical Insecticides in the Twenty-First Century—Fulfilling Their Promise? Annu. Rev. Entomol. 2020, 65, 233–249. [Google Scholar] [CrossRef] [Green Version]
  37. Pavela, R. Essential oils for the development of eco-friendly mosquito larvicides: A review. Ind. Crops Prod. 2015, 76, 174–187. [Google Scholar] [CrossRef]
  38. Seo, S.M.; Kim, J.; Kang, J.; Koh, S.H.; Ahn, Y.J.; Kang, K.S.; Park, I.K. Fumigant toxicity and acetylcholinesterase inhibitory activity of 4 Asteraceae plant essential oils and their constituents against Japanese termite (Reticulitermes speratus Kolbe). Pestic. Biochem. Physiol. 2014, 113, 55–61. [Google Scholar] [CrossRef] [PubMed]
  39. Ulukanli, Z.; Karabörklü, S.; Cenet, M.; Sagdic, O.; Ozturk, I.; Balcilar, M. Essential oil composition, insecticidal and antibacterial activities of Salvia tomentosa Miller. Med. Chem. Res. 2013, 22, 832–840. [Google Scholar] [CrossRef]
  40. Aref, S.P.; Valizadegan, O. Eucalyptus krueseana Muel essential oil: Chemical composition and insecticidal effects against the lesser grain borer, Rhyzopertha dominica F. (Coleoptera: Bostrichidae). Biharean Biol. 2015, 9, 93–97. [Google Scholar]
  41. de Andrade Brito, F.; Bacci, L.; da Silva Santana, A.; da Silva, J.E.; de Castro Nizio, D.A.; de Lima Nogueira, P.C.; de Fátima Arrigoni-Blank, M.; Melo, C.R.; de Melo, J.O.; Blank, A.F. Toxicity and behavioral alterations caused by essential oils of Croton tetradenius and their major compounds on Acromyrmex balzani. Crop Prot. 2020, 137, 105259. [Google Scholar] [CrossRef]
  42. Liang, J.Y.; Wang, W.T.; Zheng, Y.F.; Zhang, D.; Wang, J.L.; Guo, S.S.; Zhang, W.-J.; Du, S.; Zhang, J. Bioactivities and chemical constituents of essential oil extracted from Artemisia anethoides against two stored product insects. J. Oleo Sci. 2017, 66, 71–76. [Google Scholar] [CrossRef] [Green Version]
  43. Eder, E.; Henschler, D.; Neudecker, T. Mutagenic properties of allylic and α, β-unsaturated compounds: Consideration of alkylating mechanisms. Xenobiotica 1982, 12, 831–848. [Google Scholar] [CrossRef]
  44. Herrera, J.M.; Zunino, M.P.; Dambolena, J.S.; Pizzolitto, R.P.; Gañan, N.A.; Lucini, E.I.; Zygadlo, J.A. Terpene ketones as natural insecticides against Sitophilus zeamais. Ind. Crops Prod. 2015, 70, 435–442. [Google Scholar] [CrossRef]
  45. 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]
  46. Giunti, G.; Benelli, G.; Palmeri, V.; Laudani, F.; Ricupero, M.; Ricciardi, R.; Maggi, F.; Lucchi, A.; Guedes, R.N.C.; Desneux, N.; et al. Non-target effects of essential oil-based biopesticides for crop protection: Impact on natural enemies, pollinators, and soil invertebrates. Biol. Control. 2022, 176, 105071. [Google Scholar] [CrossRef]
  47. Athanassiou, C.G.; Kavallieratos, N.G.; Benelli, G.; Losic, D.; Rani, U.P.; Desneux, N. Nanoparticles for pest control: Current status and future perspectives. J. Pest Sci. 2018, 91, 1–15. [Google Scholar] [CrossRef]
  48. Pavela, R.; Pavoni, L.; Desneux, N.; Canale, A.; Maggi, F.; Benelli, G.; Bonacucina, G.; Cespi, M.; Cappellacci, L.; Petrelli, R.; 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]
  49. Ibrahim, S.S. Essential Oil Nanoformulations as a Novel Method for Insect Pest Control in Horticulture. In Horticultural Crops; Baimaey, H.K., Hamamouch, N., Kolombia, A., Eds.; IntechOpen: London, UK, 2019; pp. 195–209. [Google Scholar]
  50. Khoshraftar, Z.; Safekordi, A.A.; Shamel, A.; Zaefizadeh, M. Evaluation of insecticidal activity of nanoformulation of Melia azedarach (leaf) extract as a safe environmental insecticide. Int. J. Environ. Sci. Technol. 2020, 17, 1159–1170. [Google Scholar] [CrossRef]
  51. Pavela, R.; Murugan, K.; Canale, A.; Benelli, G. Saponaria officinalis-synthesized silver nanocrystals as effective biopesticides and oviposition inhibitors against Tetranychus urticae Koch. Ind. Crops Prod. 2017, 97, 338–344. [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. 2013, 113, 46–49. [Google Scholar] [CrossRef]
  53. Abbott, W.S. A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 1925, 18, 265–267. [Google Scholar] [CrossRef]
  54. Finney, D.J. Probit Analysis; Cambridge University Press: London, UK, 1971. [Google Scholar]
  55. 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]
Figure 1. Myrtothamnus moschatus during the rainy season.
Figure 1. Myrtothamnus moschatus during the rainy season.
Pharmaceuticals 15 01511 g001
Table 1. Chemical composition of the Myrothamnus moschatus essential oil.
Table 1. Chemical composition of the Myrothamnus moschatus essential oil.
No.Component aRI bRI Lit. c% dID Method e
1α-pinene9269328.8 ± 1.2Std
2camphene9399460.4 ± 0.1Std
3thuja-2,4(10)-diene9449530.1 ± 0.0RI,MS
4benzaldehyde956952Tr fStd
5β-pinene9679740.6 ± 0.2Std
6p-cymene102010201.8 ± 0.4Std
7limonene102410240.8 ± 0.2Std
81,8-cineole102610260.7 ± 0.2Std
9γ-terpinene10551054TrStd
10p-cymenene108610890.1 ± 0.0RI,MS
116-camphenone109210950.1 ± 0.0RI,MS
12trans-p-mentha-2,8-dien-1-ol11181190.3 ± 0.0RI,MS
13α-campholenal112211220.5 ± 0.1RI,MS
14trans-pinocarveol1137113537.7 ± 4.2Std
15trans-pinocamphone115711580.1 ± 0.0RI,MS
16pinocarvone1159116020.8 ± 3.1RI,MS
17p-mentha-1,5-dien-8-ol11641166TrRI,MS
18cis-pinocamphone11681172TrRI,MS
19p-cymen-8-ol118411790.5 ± 0.2RI,MS
20trans-p-mentha-1(7),8-dien-2-ol118411872.2 ± 0.4RI,MS
21myrtenal118911941.8 ± 0.3Std
22myrtenol119111941.5 ± 0.3Std
23cis-piperitol119611950.3 ± 0.1RI,MS
24trans-carveol121512150.7 ± 0.1RI,MS
254-methylene121612160.5 ± 0.1RI,MS
26cis-p-mentha-1(7),8-dien-2-ol122412271.4 ± 0.3RI,MS
27carvone123912390.2 ± 0.0Std
28perilla aldehyde126812690.1 ± 0.0RI,MS
29bornyl acetate128012870.2 ± 0.1Std
30trans-pinocarvyl acetate129512980.1 ± 0.0RI,MS
31myrtenyl acetate132113240.5 ± 0.1RI,MS
32perillyl acetate143314364.9 ± 0.9RI,MS
33β-selinene1476148910.2 ± 1.3RI,MS
34α-selinene148114980.1 ± 0.0RI,MS
Total identified (%) 98.2
Chemical classes (%)
 Monoterpene hydrocarbons 12.6
 Oxygenated monoterpenes 75.3
 Sesquiterpene hydrocarbons 10.2
 Others Tr
a Components were eluted from an HP-5MS column (30 m l. × 0.25 mm i.d., 0.1 μm f.t.). b Linear retention index experimentally determined with respect to a mixture of C7-C30 n-alkanes (Sigma-Aldrich) according to the Van den Dool and Kratz formula [27]. c Retention index value taken from ADAMS or FFNSC3 libraries. d Peak area relative percentages are the mean of two independent injections ± SD. e Method of identification: Std, RT, RI, and MS overlapping with analytical standard (Sigma-Aldrich); RI, coherence of the calculated RI with those stored in ADAMS and FFNSC3 libraries. MS, matching of mass fragmentation with that of spectra contained in ADAMS, NIST17, FFNSC3, and WILEY275 libraries. f Traces, % < 0.1.
Table 2. Acute toxicity of the Myrothamnus moschatus essential oil on selected insect and mite species.
Table 2. Acute toxicity of the Myrothamnus moschatus essential oil on selected insect and mite species.
Arthropod Species and InstarUnitLD50CI95 aLC90CI95 bχ2 (d.f.) p-Value
Musca domestica adultµg adult−122.717.4–30.3109.675.7–175.81.545 (4)0.818 ns
Spodoptera littoralis larvaµg larva−135.630.1–41.379.266.1–101.30.933 (4)0.837 ns
Culex quinquefasciatus larvaµg mL−143.637.2–50.8111.490.5–149.50.750 (3)0.212 ns
Metopolophium dirhodum adultmL L−12.42.2–2.65.85.5–7.11.196 (3)0.753 ns
Tetranychus urticae adultmL L−11.20.9–1.73.32.3–8.72.703 (3)0.439 ns
a 95% confidence interval relative to LD50 values. b 95% confidence interval relative to LC50 values. ns = not significant (p > 0.05).
Table 3. Acute toxicity of the positive control, a commercial botanical insecticide based on Pongamia pinnata oil, on selected insect and mite species.
Table 3. Acute toxicity of the positive control, a commercial botanical insecticide based on Pongamia pinnata oil, on selected insect and mite species.
Arthropod Species and InstarUnitLD50CI95 aLC90CI95 bχ2 (d.f.) p-Value
Musca domestica adultµg adult−1˃500-----
Spodoptera littoralis larvaµg larva−118.215.6–19.828.626.8–32.52.451 (3)0.751 ns
Culex quinquefasciatus larvaµg mL−1275.4256.8–321.71285.71211.5–1354.43.512 (3)0.425 ns
Metopolophium dirhodum adultmL L−112.59.6–13.821.718.6–22.32.525 (3)0.598 ns
Tetranychus urticae adultmL L−15.85.1–6–810.19.2–12.71.851 (3)0.845 ns
a 95% confidence interval relative to LD50 values. b 95% confidence interval relative to LC50 values. ns = not significant (p > 0.05).
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Pavela, R.; Ferrati, M.; Spinozzi, E.; Maggi, F.; Petrelli, R.; Rakotosaona, R.; Ricciardi, R.; Benelli, G. The Essential Oil from the Resurrection Plant Myrothamnus moschatus Is Effective against Arthropods of Agricultural and Medical Interest. Pharmaceuticals 2022, 15, 1511. https://doi.org/10.3390/ph15121511

AMA Style

Pavela R, Ferrati M, Spinozzi E, Maggi F, Petrelli R, Rakotosaona R, Ricciardi R, Benelli G. The Essential Oil from the Resurrection Plant Myrothamnus moschatus Is Effective against Arthropods of Agricultural and Medical Interest. Pharmaceuticals. 2022; 15(12):1511. https://doi.org/10.3390/ph15121511

Chicago/Turabian Style

Pavela, Roman, Marta Ferrati, Eleonora Spinozzi, Filippo Maggi, Riccardo Petrelli, Rianasoambolanoro Rakotosaona, Renato Ricciardi, and Giovanni Benelli. 2022. "The Essential Oil from the Resurrection Plant Myrothamnus moschatus Is Effective against Arthropods of Agricultural and Medical Interest" Pharmaceuticals 15, no. 12: 1511. https://doi.org/10.3390/ph15121511

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop