Toxicity and deleterious effects of Artemisia annua essential oil extracts on mulberry pyralid (Glyphodes pyloalis)

doi:10.1016/j.pestbp.2020.104702

Pesticide Biochemistry and Physiology

Volume 170, November 2020, 104702

https://doi.org/10.1016/j.pestbp.2020.104702 Get rights and content

Highlights

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Wormwood essential oil could be a candidate natural compound for pest control.
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This EO affected most of physiological systems which is a proof for this potential.
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Thus wormwood EO could be the next botanical to be formulated and incorporated.

Abstract

Botanical extracts are an important source of bio-pesticides and are generally considered safe to the environment. Artemisia annua L, a medicinal plant, well known for its antimalarial potential, was evaluated as a source of a type of essential oil collected during vegetative growth stage against Glyphodes pyloalis Walker. The main chemical components of the essential oil at vegetative stage of Artemisia annua was analyzed by GC- MS and contained 1,8-cineole (18.68%), Camphor (11.4%), α-Pinene (9.3%) and 3-Carene (6.3%). The LC₅₀ of this plant oil was estimated to be 0.652% W/V and 2.585 μL/L air incorporated orally and fumigation, respectively. The digestive enzymes such as α-amylases, Proteases, Lipases and α- and β-glucosidases were considereably inhibited in treated larvae compared with controls. Similarly, the amount of protein, glucose, and triglyceride were decreased in the treated larvae by methods used. The lower hemocyte numbers, nodule formation and activity of phenoloxidases after injection of Beauveria bassiana and latex beads showed its EO effect on immunity. The anatomy of the larval midgut after treatment showed degeneration in digestive cells. Emerging adult's ovaries showed significant changes in the ovarian sheath and lack of yolk spheres. The present investigation in accordance with our previous studies may ultimately lead to a formulation in controlling this notorious pest especially in mulberry orchards where the use of conventional chemicals is restricted.

Graphical abstract

Introduction

The lesser mulberry pyralid (Glyphodes pyloalis Walker) (Lepidoptera: Pyralidae) is a prominent pest of mulberry trees. The larva rolls the leaves then starts feeding from within, resulting in skeletonizing the plant (Aruga 1994). There are two problems associated with this pest, firstly the mulberry (Morus sp.) is also the host plant of common silkworm, Bombyx mori L. thereby causeing the loss of leaves and secondly, this pest is associated with transmission of silkworm viral diseases (Watanabe et al. 1988).

There are always concerns about side effects of conventional insecticides to humans, pest resistance, and pest resurgence following elimination of natural enemies (Chowdhury et al. 2012). While natural control agents could be considered as beneficial alternatives, gradually replacing conventional practices (Sousa et al. 2017; Pavela and Sedlák, 2018).

Among natural pest control factors, plants have a very prestigious status attributed to their secondary metabolites (Benelli et al. 2018). The products of plants including oils and extracts affect various sites of activity on target insects, consequently resistance to them seems less likely (Isman 2000).

The sweet wormwood, Artemisia annua L. (Asteraceae), locally known as Caspian wormwood and/or Gandwash is a plant that grows wild in north provinces of Iran (Shekari et al. 2008). This plant possesses several medicinal properties well established in the literature (Bhakuni et al. 2001). A. annua has shown to have considerable toxicity which cause, various physiological disorders in nutrition, reproduction, immune system, and intermediary metabolism. (Shekari et al. 2008; Hasheminia et al. 2011; Zibaee 2011; Mojarab-Mahboubkar et al. 2015). We used essential oil from vegetative growth stage of sweet wormwood using two methods; i.e. oral and fumigation, on toxicity, enzymatic and non-enzymatic compounds, immune system, and on the histology of digestive and female reproductive system in Glyphodes pyloalis. This is the first comprehensive study aiming to find and introduce a reasonable formulation for controlling G. pyloalis.

Section snippets

Rearing

Various stages of lesser mulberry pyralid were collected from mulberry trees in and around Rasht city (37.2682° N, 49.5891° E), Guilan province, Iran. The larvae fed daily with tender leaves of mulberry (Shin Ichinoise) in transparent plastic jars 10 × 20 × 5 cm maintained in an incubator (25 ± 1 °C, 75 ± 5% Relative humidity and 16:8 Light: Darkness). The emerged adults were kept in 18 × 7 × 5 cm rectangular jars. Tender mulberry leaves were placed in the jars for egg laying and honey solution

Chemical composition of Artemisia annua essential oil

The chemicals present in A. annua EO showed about 28 chemical constituents including 1,8-cineole (18.68%), Camphor (11.4%), α-pinene (9.3%), 3-Carene (6.3%), Pinocarvone (7.5%). Pentadecane (5.7%) as the main components (Table 1).

Bioassay

Results of A. annua EO bioassays in two incorporated methods (i.e. oral and fumigant) 24 h after treatments showed toxicity. The LC₅₀ values were estimsted to be 0.652% W/V and 2.585 μL/L air for oral and fumigant assays respectively. By increasing concentration, the

Discussion

Essential oils are the products of plants which are considered as the secondary metabolites, naturally needed for both growth and protection. Their major characteristics lie in their types of chemical constituents. This feature is very specific and shows great variations even in the same species growing in two different geographical conditions. The oils are produced and maintained in various parts of the plant (Regnault-Roger et al. 2012).

The terpinoides are considered as the main constituents

Conclusion

Our results show that A. annua essential oil obtained from the vegetative growth stage has the potential of being a candidate natural compound for future pest control, in particular. Particularly the places where the use of conventional pesticides are restricted or even prohibited. These areas include the mulberry orchards of which the leaves are used for silk worm rearing in rural areas by regional farmers. The use of mulberry plantations for urban green spaces area on the sides of streets or

Acknowledgements

The authors wish to thank Iran National Science Foundation (INSF) for research grant 98004512.

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Plant secondary metabolites are currently known to interfere with basic metabolic, behavioral and physiological processes of insects. In the current study, the biological and physiological effects of trans-anethole were investigated against Hyphantria cunea Drury. The bioassay data demonstrated the high toxicity of trans-anethole against the fourth-instar larvae with the LC₃₀, LC₅₀ and LC₉₀ values of 0.72, 1.41 and 7.20 μL/mL, respectively. Also the concentrations of LC₃₀ and LC₅₀ showed 53 and 87% feeding deterrency against the larvae. The biochemical experiments revealed that oral exposure of trans-anethole decreased the activities of digestive enzymes, acetylcholinesterase and the contents of energy reserves while, it induced the activities of detoxifying and antioxidant enzymes compared to control. In fact, trans-anethole induced the inhibition of digestion and AChE activities accompanied by imbalance in metabolic and oxidative processes so it may be recommended as a potent biopesticide in control of H. cunea populations.
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Our data demonstrated activity of ESTs decreased in the treated larvae by A. annua EO and its constituents. Inhibition of ESTs in the current research is consistent with previous investigations indicating similar decrease in enzymatic activity of ESTs in insects after treatment with A. annua and its components (Mojarab-Mahboubkar et al., 2015; Oftadeh et al., 2020, 2021). On the other hand, high induction of ESTs was also noted in the larvae of G. pyloalis after treatment with A. annua (Khosravi et al., 2011).
The fall webworm, Hyphantria cunea (Drury), is a harmful polyphagous global defoliator. The major chemical components of Artemisia annua essential oil (EO) was found to contain (±)-camphor (16.42%), 1,8-cineole (6.22%), α-pinene (6%), caryophyllene (5.19%), and α-selinene (5.17%). The highest toxicity was recorded for EO of A. annua (LD₅₀ = 305.05 μg/larva), followed by (±)-camphor (LD₅₀ = 465.03 μg/larva) and 1,8-cineole (LD₅₀ = 573.49 μg/larva). The binary mixtures of compounds expressed a weaker activity compared to individuals. The (±)-camphor was found to be antagonistic to 1,8-cineole. The biochemical compounds of treated larvae were also determined. The activity level of alanin and aspartate aminotransferase decreased sharply while acid and alkaline phosphatase increased. Activity of lactate dehydrogenase was significantly higher than the control group at 24 h, but decreased significantly after 48 h in all treatments. The activity of esterases were decreased in the treated larvae. The glutathione S-transferase significantly increased in all time intervals. Overall the current results suggest that the sweet wormwood (A. annua) EO and its components could be a safe and environmentally friendly approach in possible control of fall webworm (H. cunea).

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Toxicity and deleterious effects of Artemisia annua essential oil extracts on mulberry pyralid (Glyphodes pyloalis)

Highlights

Abstract

Graphical abstract

Introduction

Section snippets

Rearing

Chemical composition of Artemisia annua essential oil

Bioassay

Discussion

Conclusion

Acknowledgements

Ind. Crop. Prod.

Pestic. Biochem. Physiol.

Anal. Biochem.

J. Insect Physiol.

J. Pestic. Biochem. Physiol.

Crop Prot.

J. King Saud Univ. Sci.

Cell. Signal.

Ind. Crop. Prod.

J. Asia Pac. Entomol.

Chemosphere.

Pestic. Biochem. Physiol.

J. Insect Physiol.

J. Inverteber. Pathol.

Ind. Crop. Prod.

The role of glutathione transferases in the development of insecticide resistance

Principles of Sericulture

Bioinsecticides induce change in biochemical and immunological parameters of Spodoptera littoralis larvae

Annu. Rev. Chem. Biomol. Eng.

Inhibition of Phenoloxidase activity delays development in Bactrocera dorsalis (Diptera: Tephritidae)

Fla. Entomol.

Artemisia spp. essential oils against the disease-carrying blowfly Calliphora vomitoria

Parasit. Vectors

α-Amylases

Methods Enzymol.

Secondary metabolites of Artemisia annua and their biological activity

Curr. Sci.

Lethal and sublethal effects of essential oils from Artemisia khorassanica and Vitex pseudo-negundoAgainst Plodia interpunctella (Lepidoptera: Pyralidae)

J. Env. Entomol.

The Insects: Structure and Function

Feeding inhibitory effectof some plant extracts on jute hairy caterpillar (Spilosoma obliqua)

Indian. J. Agric. Res.

Costs of resistance: genetic correlations and potential trade-offs in an insect immune system

J. Evol. Biol.

Phytochemistry, toxicity and feeding inhibitory activity of Melissa officinalis L. essential oil against a cosmopolitan insect pest; Tribolium castaneum Herbst

Toxin Rev.