The volatile oils from the oleo-gum-resins of Ferula assa-foetida and Ferula gummosa: A comprehensive investigation of their insecticidal activity and eco-toxicological effects

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Highlights

  • The volatile oils from the oleo-gum-resins of Ferula assa-foetida and F. gummosa were studied.

  • Their efficacy against arthropod vectors, and agricultural and stored-product pests was evaluated.

  • The eco-toxicological effects on non-target organisms were measured.

  • The cytotoxicity on non-target vertebrate cells and on tumor cells was determined.

Abstract

Since time immemorial, the oleo-gum-resins of Ferula assa-foetida and F. gummosa are used in the traditional medical systems as well as in foodstuffs, perfumery and cosmetics. In the present study, we explored the insecticidal efficacy of the essential oils obtained from these oleo-gum-resins to widen their fields of industrial applications. The two essential oils were mainly composed of sulfides [sec-butyl (Z)-propenyl disulfide, sec-butyl (E)-propenyl disulfide, sec-butyl (Z)-propenyl trisulfide and sec-butyl (E)-propenyl trisulfide)] and monoterpenes (α-pinene, β-pinene and β-phellandrene), respectively, as determined by GC-MS analysis. The two essential oils were assayed for toxicity on a panel of insects, represented by species of public health relevance (Culex quinquefasciatus and Musca domestica), agricultural (Spodoptera littoralis) and stored-product pests (Prostephanus truncatus and Trogoderma granarium). The ecotoxicological effects of the essential oils were assessed on the aquatic microcrustacean Daphnia magna and the earthworm Eisenia fetida, as well as on human cells. Overall, the two essential oils were effective against important insect pests and vectors. On the other hand, they resulted cytotoxic to fibroblasts and non-target aquatic microcrustaceans. Thus, further insights are needed to determine the full spectrum of their eco-toxicological effects.

Introduction

The genus Ferula L., one of the largest genera of the Apiaceae family, encompasses about 170 species distributed in central Asia, Mediterranean countries and northern Africa (Pimenov and Leonov, 1993). Several Ferula species possess a pronounced odour due to the production of sulphur-containing essential oils or oleo-gum-resins in their different parts that make them valuable industrial crops exploitable in different fields such as food and beverages, perfumery, varnishes, soaps and detergents, cosmetics, pharmaceutics, textile and jewellery (Jalali et al., 2011; Radulović et al., 2015; Malekzadeh et al., 2018). They are also widely used in the traditional medicine.

Ferula assa-foetida L. and F. gummosa Boiss. are two perennial and monocarpic plants living up to 6–8 years, up to 3 m tall, with dissected leaves, showy yellow compound umbels and schizocarp fruits, growing wild in Iran and popularly referred to as ‘Anghouzeh’ and ‘Baridje’, respectively (Mozaffarian, 2012; Najafabadi et al., 2017). F. assa-foetida, also known as asafetida, is an endemic plant of Iran where is found in rocky hillside of Khorasan, Yazd Esfahan and some parts of Hormozgan provinces. On the other hand, F. gummosa, also known as galbanum, is distributed in the highlands of Iran, Afghanistan and Central Asia (Mozaffarian, 2012). Both species produce a sort of milky latex or translucent oleo-gum-resin, turning to yellowish-brown as it is exposed to air. This exudate is made up of three fractions: (i) volatile oil (10–17%, w/w dw), (ii) gum (25%) and (iii) resin (40–64%) (Saeidy et al., 2018). These products, which exude spontaneously from the duct channels occurring in the plant taproots, but can also be obtained by incision, are endowed with a very strong odour (sulphurous and balsamic, respectively), a bitter taste, and are frequently used as spices and perfumes (Rajanikanth et al., 1984; Ghannadi and Amree, 2011; Peter, 2012; Kavoosi and Rowshan, 2013; Amalraj and Gopi, 2017). Notably, the oleo-gum-resin of F. assa-foetida, when cooked, releases a garlic-like smell particularly appreciated in the Indian cousin (Gholami and Faravani, 2014). The secrete of F. assa-foetida roots is also reported in the Belfrit list of botanicals to be employed in food supplements (Cousyn et al., 2013).

Because of the strong odour, in some parts of Iran the local farmers use these oleo-gum-resins as a repellent agent against pests; further uses include the preparation of a remedy against insect and snake bites (Peyrovi et al., 2011; Gholami and Faravani, 2014). In the Iranian traditional medicine, their oleo-gum-resins have been used for centuries to treat various ailments such as asthma, bronchitis, cough, influenza, diabetes, intestinal parasites, gastrointestinal disorders, spasms, infections, haemorrhoids, kidney and bladder stones, cancer, epilepsy and frequently as a laxative, carminative, sedative, analgesic, aphrodisiac, tonic, neuroprotective, nerve stimulating and memory enhancer agent (Fazel Nabavi et al., 2010; Mozaffarian, 2012; Adhami et al., 2014; Moghadam et al., 2014; Bagheri et al., 2017,Bagheri et al., 2017; Vijayasteltar et al., 2017; Boghrati and Iranshahi, 2019; Mohammadhosseini et al., 2019). The volatile oil obtained from the oleo-gum-resin of F. assa-foetida is rich in sulphurous compounds such as sec-butyl (Z)-propenyl disulphide and sec-butyl (E)-propenyl disulphide (Kavoosi and Rowshan, 2013), while the one from F. gummosa is rich in monoterpenes such as α- and β-pinene and is one of the top essential oils used for specialty industrial materials (Ghannadi and Amree, 2011; Lubbe and Verpoorte, 2011).

The essential oils from the oleo-gum-resins of these two species have been the subject of several biological investigations attesting mainly their antibacterial, antifungal, anti-biofilm, anti-quorum sensing, antioxidant, relaxant, repellent and cytotoxic properties (Sahebkar and Iranshahi, 2010; Peyrovi et al., 2011; Kavoosi and Rowshan, 2013; Bagheri et al., 2014; Mahboubi, 2016; Amalraj and Gopi, 2017; Zomorodian et al., 2018; Boghrati and Iranshahi, 2019).

In the last decades, the cultivation of these two species for production of oleo-gum-resins has increased in Iran. This increase should be counterbalanced by an appropriate diversification of their uses on an industrial level. On this basis, in the present study we decided to explore the insecticidal potential of the essential oils obtained from F. gummosa and F. assa-foetida oleo-gum-resins, to widen their fields of application and offer new opportunities of economic income to farmers. To our knowledge, only a few studies have been carried out on this topic so far. Indeed, the essential oil from oleo-gum-resin of F. assa-foetida and F. gummosa have been tested for their repellent activity against Ectomyelois ceratoniae (Zeller) (Lepidoptera: Pyralidae) under field conditions (Peyrovi et al., 2011). Besides, their toxicity was evaluated against some stored-product insect pests, such as Ephestia kuehniella Zeller (Lepidoptera: Pyralidae), and the stored-product beetles Sitophilus oryzae (L.), S. granarius (L.) (Coleoptera: Curculionidae) and Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae) (Ghasemi et al., 2014; Mahmoudvand et al., 2012).

Therefore, in the present work these two essential oils, obtained from the oleo-gum-resins by hydrodistillation and analysed by gas chromatography coupled with mass spectrometry (GC-MS), were assayed for toxicity on a panel of insects, represented by species of public health relevance (Culex quinquefasciatus Say (Diptera: Culicidae) and Musca domestica L. (Diptera: Muscidae)), as well as agricultural (Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae)) and stored-product pests (Prostephanus truncatus (Horn) (Coleoptera: Bostrychidae) and Trogoderma granarium Everts (Coleoptera: Dermestidae)). In order to shed light on the possible mode of action, the inhibitory effects of the two essential oils on the acetylcholinesterase (AChE) enzyme were determined. Furthermore, the ecotoxicological effects of sub-lethal doses of these two essential oils were measured on the aquatic microcrustacean Daphnia magna Straus (Cladocera: Daphniidae) and on the earthworm Eisenia fetida Savigny (Haplotaxida: Lumbricidae), which are very sensitive to synthetic pesticides and pollutants. To complete the work, the two essential oils were also compared for cytotoxicity on human cells and antimicrobial activities by using the MTT and agar disk diffusion methods, respectively.

Section snippets

Plant material

The oleo-gum-resins of F. gummosa and F. assa-foetida were collected from the four years old plants growing in Kohsorkh, Kashmar province, Iran (N 35°29′, E 58°27′, 1812 m a.s.l. and N 35°36′, E 58°32′, 1842 m a.s.l., respectively) in August 2018. The botanical identification was made by Yosef Asghari and voucher specimens were deposited in the Herbarium of Agricultural and Natural Resources Research and Education Center, Kohgiluyeh and Boyer-Ahmad, Iran, with the numbers 4548 and 4545,

Essential oil analyses

The classical method of hydrodistillation applied to the oleo-gum-resins from F. assa-foetida and F. gummosa yielded 8.9 and 11.6% (w/w) of essential oil, respectively. These values are in line with those reported in literature (Jalali et al., 2012; Divya et al., 2014; Saeidy et al., 2018; Hassanabadi et al., 2019) and support the use of these essential oils on an industrial level. The colour of the oil was pale-yellow (F. assa-foetida) and transparent (F. gummosa).

The chemical composition of

Essential oil analysis

In the present analysis we confirmed that the two sulfides sec-butyl (Z)-propenyl disulfide (45.5%) and sec-butyl (E)-propenyl disulfide (30.4%) were the main constituents of the volatile oil distilled from the oleo-gum-resin of F. assa-foetida. Noteworthy, we reported for the first time in this species the two trisulfides sec-butyl (Z)-propenyl trisulfide (12.3%) and sec-butyl (E)-propenyl trisulfide (4.5%) (Fig. 1). Previously, they were detected in the essential oil from F. alliacea Boiss.

Conclusions

The oleo-gum-resins of F. assa-foetida and F. gummosa represent natural sources of spices and medicines of economic importance in Iran. The present work shed light into the potential uses of their liquid part, represented by essential oils, as green pesticides effective against agricultural and stored-product insect pests as well as on insect vectors and microbial fungal pathogens. Overall, the one from F. assa-foetida seemed to be more active. However, the relatively high toxicity on human

CRediT authorship contribution statement

Roman Pavela: Methodology, Resources, Data curation, Writing - review & editing. Mohammad Reza Morshedloo: Conceptualization, Writing - review & editing, Visualization. Giulio Lupidi: Methodology, Writing - review & editing. Giorgia Carolla: Methodology, Writing - review & editing. Luciano Barboni: Methodology, Writing - review & editing. Luana Quassinti: Methodology, Writing - review & editing. Massimo Bramucci: Methodology, Writing - review & editing. Luca A. Vitali: Methodology, Writing -

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper: Herein we confirm that none of the following points subsist for our work. (1) All third-party financial support for the work in the submitted manuscript. (2) All financial relationships with any entities that could be viewed as relevant to the general area of the submitted manuscript. (3) All sources of revenue with relevance

Acknowledgments

Two anonymous reviewers kindly improved an earlier version of our manuscript. Dr. Roman Pavela would like to thank the Ministry of Agriculture of the Czech Republic for its financial support concerning botanical pesticide and basic substances research (Project No. RO0418). This study was partially funded by the 34.0401 project (Special Account for Research Funds of the Agricultural University of Athens).

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