Effectiveness of eight essential oils against two key stored-product beetles, Prostephanus truncatus (Horn) and Trogoderma granarium Everts

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Highlights

  • C. acaulis EO (500 ppm) killed > 97% of P. truncatus adults within 3 days on maize.

  • M. longifolia EO (500 ppm) killed all T. granarium adults within 2 days on wheat.

  • D. ambrosioides EO (500 ppm) killed > 95% of T. granarium adults within 4 days on wheat.

  • M. longifolia and D. ambrosioides EOs (1000 ppm) killed > 93% of T. granarium larvae on wheat after 16 h.

  • These EOs may be considered for developing green grain protectants against stored-product pests.

Abstract

The use of chemical pesticides to preserve food commodities is a global issue of concern due to their negative effect on the environment and public health. In recent years, the European Union is trying to reduce their use, favoring alternative or complementary approaches based on natural products. In this scenario, plant-borne essential oils (EOs) represent valid options for Integrated Pest Management (IPM) programs. In the present study, the insecticidal effect of eight EOs obtained from plants from different parts of the world, namely Mentha longifolia, Dysphania ambrosioides, Carlina acaulis, Trachyspermum ammi, Pimpinella anisum, Origanum syriacum, Cannabis sativa and Hazomalania voyronii, were evaluated against two stored-product insect species of economic importance, Prostephanus truncatus and Trogoderma granarium. Simulating a small-scale stored-product conservation environment, an AG-4 airbrush was used to spray maize and wheat with 500 and 1000 ppm of EOs, then T. granarium and P. truncatus were exposed to the stored products and mortality was evaluated over selected time intervals (4, 8, and 16 h, and 1, 2, 3, 4, 5, 6, and 7 days). The EO of C. acaulis exhibited high efficacy against P. truncatus adults at both tested concentrations by killing > 97% of the individuals exposed to treated maize within 3 days at 500 ppm. The EO of D. ambrosioides eliminated all T. granarium adults exposed to 1000 ppm-treated wheat 2 days post-exposure. At this exposure interval, 91.1% of the exposed T. granarium adults died on wheat treated with 1000 ppm of C. acaulis EO. The EO of M. longifolia at both tested concentrations was the most effective against T. granarium larvae, leading to 97.8% mortality at 500 ppm after 3 days of exposure, and 100% mortality at 1000 pm 2 days post-exposure. At 1000 ppm, the EOs of D. ambrosioides and P. anisum led to 95.6 and 90% mortality, respectively, to larvae exposed to treated wheat for 7 days. Overall, our research shed light on the potential of selected EOs, with special reference to M. longifolia, D. ambrosioides, C. acaulis and P. anisum, which could be considered further to develop effective and alternative grain protectants to manage P. truncatus and T. granarium infestations.

Introduction

The widespread overuse of synthetic pesticides to manage arthropod pests, including those attacking food commodities, represents a major issue of concern because of environmental and health issues (Desneux et al., 2007). In this scenario, the European Union encourages a substantial reduction in the use of chemical pesticides, boosting the employment of more eco-friendly approaches under the Integrated Pest Management (IPM) criteria (Hillocks, 2012; Lucchi and Benelli, 2018).

Prostephanus truncatus (Horn) (Coleoptera: Bostrychidae) is an important pest of economic importance in stored maize and dried roots of cassava (Hodges et al., 1985; Schäfer et al., 2000; Hill, 2003; Gnonlonfin et al., 2008; Gueye et al., 2008; Giliomee, 2011; Muatinte et al., 2014), and is subjected to quarantine restrictions measures per country (Tyler and Hodges, 2002; Myers and Hagstrum, 2012). This species was accidently introduced from Central America to Africa four decades ago, and expanded quickly in several regions of Africa, Asia and Americas (Dunstan and Magazini, 1981; Hodges, 2002; EPPO, 2020a). Prostephanus truncatus can survive on numerous non-maize grains and flours, indicating that these commodities could significantly contribute to its expansion as “vehicle” grains (Athanassiou et al., 2017). Furthermore, P. truncatus is tolerant to synthetic and natural insecticides, such as organophosphates (OPs) and diatomaceous earths (DEs), respectively (Golob, 2002; Athanassiou et al., 2007; Kavallieratos et al., 2018).

Trogoderma granarium Everts (Coleoptera: Dermestidae) is an important insect species acting as a major pest of economic importance, which falls under strict phytosanitary concerns (Banks, 1977; Lowe et al., 2000; Hill, 2003; Myers and Hagstrum, 2012; EPPO, 2013). This species has been categorized among the most hazardous invasive alien species of the world (Lowe et al., 2000). Trogoderma granarium is originated from India (Rahman et al., 1945), but it has been spread to many regions of Africa, Asia and Europe (Athanassiou et al., 2015; EPPO, 2020b). The potential expansion of T. granarium is highly determined by the fact that it feeds on numerous commodities, such as stored cereals or related amylaceous products and non-grain commodities (Lindgren et al., 1955; Lindgren and Vincent, 1959; Bhattacharya and Pant, 1968; Viljoen, 1990; Degri and Zainab, 2013; Athanassiou et al., 2016; Kavallieratos et al., 2019). Furthermore, T. granarium larvae may fall under facultative diapause for several years (Burges, 1962; Hill, 2003; Myers and Hagstrum, 2012) and are tolerant to insecticidal treatments (Bell et al., 1984; Bell and Wilson, 1995; Edde et al., 2012; Athanassiou et al., 2015).

During the last decades, botanicals have been evaluated for the control of a large spectrum of insects on different stored commodities (Weaver and Subramanyam, 2000; Athanassiou et al., 2014). A rather wide number of research items focused on the estimation of the contact effect of plant extracts or essential oils (EOs) against the target insect species, by topical application to the dorsal surface of the insect thorax or by applying them on filter paper, as well as the evaluation of the botanical repellent efficacy (Tapondjou et al., 2002; Tripathi and Kumar, 2007; Abdel Sattar et al., 2010; Nenaah and Ibrahim, 2011; Zia et al., 2013; Nenaah, 2014; Alamir et al., 2015; Nouri Ganbalani and Borzoui, 2017; Janaki et al., 2018). In this framework, several medicinal and aromatic plants have been evaluated as grain protectants; most of them have been used as powders directly mixed with grains, against P. truncatus, T. granarium and other serious insect pests of stored products (Obeng Ofori et al., 1997; Obeng Ofori and Reichmuth, 1999; Tapondjou et al., 2002; Nukenine et al., 2010; Nenaah and Ibrahim, 2011). However, there are very limited data available on the utilization of EOs as grain protectants for the control of P. truncatus (Schmidt and Streloke, 1994; Nukenine et al., 2010), while such data are yet to be reported for T. granarium.

Indeed, the toxicity of major components of few EOs, such as eugenol from the holy basil, Ocimum suave (Wild.) (Lamiales: Lamiacae), β-asarone from the EO of the sweetflag, Acorus calamus (L.) (Arales: Araceae), 1,8-cineole, from the EO of O. kenyense (Ayobangira) (Lamiales: Lamiacae), camphor, from the EO of the camphor basil, O. kilimandscharicum (Wild.) (Lamiales: Lamiacae), have been assessed as grain protectants against stored-product insects, including P. truncatus (Schmidt and Streloke, 1994; Obeng Ofori et al., 1997, Obeng Ofori et al., 1998; Obeng Ofori and Reichmuth, 1997, 1999), while few data are available about T. granarium (Abdel Sattar et al., 2010; Tayoub et al., 2012).

From an extensive literature examination, the EO of horsemint, Mentha longifolia (L.) Huds. (Lamiales: Lamiaceae), wormseed, Dysphania ambrosioides (L.) Mosyakin and Clemants (Caryophyllales: Chenopodioideae), stemless carline thistle, Carlina acaulis L. (Asterales: Compositae), ajowain, Trachyspermum ammi (L.) Sprague ex Turrill (Apiales: Apiaceae), anise, Pimpinella anisum L. (Apiales: Apiaceae), Syrian oregano, Origanum syriacum L. (Lamiales: Lamiaceae), industrial hemp, Cannabis sativa L. (Rosales: Cannabaceae), and hazomalany, Hazomalania voyronii (Jum.) Capuron (Laurales: Hernandiaceae), have never been examined before as grain protectants for the control of P. truncatus and T. granarium. Only an evaluation of the contact toxicity of dry ground leaves directly mixed with maize, and the contact/fumigant toxicity of the D. ambrosioides EO, has been attempted against P. truncatus (Tapondjou et al., 2002) and T. granarium (Nenaah and Ibrahim, 2011).

Thus, the aim of this study is to mimic a small-scale stored-product conservation environment, where maize and wheat were treated with different concentrations of the eight above-mentioned plant EOs, namely M. longifolia, D. ambrosioides, C. acaulis, T. ammi, P. anisum, O. syriacum, C. sativa and H. voyronii, and then exposed to P. truncatus adults and T. granarium adults and larvae evaluating the beetle mortality rates over selected time intervals (4, 8 and 16 h, and 1, 2, 3, 4, 5, 6 and 7 days).

Section snippets

Plant materials

A list of plant species, part used and origin of the species employed for EOs distillation is given in Table 1. Aerial parts of M. longifolia were collected in Molina Aterno, L'Aquila, Italy (N 42°09′0.36′′; E 13°43′34.90″, 450 m a.s.l.) in September 2017 (Table 1). A voucher specimen was collected and stored in the Herbarium of Géoarchitecture, UFR Sciences & Techniques, Université de Bretagne Occidentale, Brest, France, using the code BREKC11. Flowering aerial parts of D. ambrosioides were

EO compositions

The GC-MS semi-quantitative analysis of the eight EOs, in terms of relative peak area percentages, are presented in Table 2. The M. longifolia EO was dominated by piperitenone oxide (61.1%), with lower content of myrcene (10.8%), limonene (5.3%) and 1,8-cineole (5.3%). The D. ambrosioides EO was characterized by ascaridole (61.4%), being the sum of the cis- and trans-isomers (35.4 and 26.0%, respectively), followed by p-cymene (29.2%). The C. acaulis EO was dominated by the polyacetylene

Discussion

Botanicals include a wide array of promising compounds to be exploited for developing novel, effective and environmentally sustainable pesticides (Isman, 2015; Stevenson et al., 2017; Pavela et al., 2019a) and repellents (Lupi et al., 2013; Benelli and Pavela, 2018). In particular, plant-based insecticides are often characterized by multiple modes of action that makes the resistance development unlikely (Pavela and Benelli, 2016; Jankowska et al., 2017). In this framework, our findings indicate

Author contributions section

N.G.K., F.M. and G.B. conceived and designed the study. L.C., R.P. and F.M. performed the isolation and chemical analysis of EOs. N.G.K., M.C.B., N.N., A.S., E.S.K., E.P.N. performed the toxicity tests. N.G.K., M.C.B., N.N., A.S., E.S.K., E.P.N., D.C.K., L.C., R.P., K.C., M.R.M., L.A.T., R.R., F.M. and G.B. interpreted the data. N.G.K. and M.C.B. performed statistical analyses. N.G.K., M.C.B., N.N., F.M. and G.B. drafted of the manuscript. All authors revised the manuscript. All authors have

Funding

This study was funded by the 34.0401 project (Special Account for Research Funds of the Agricultural University of Athens) and by the University of Camerino (Fondo di Ateneo per la Ricerca, FAR).

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.

Acknowledgments

The authors thank Mr. Claudio Cianfaglione for his kind support during plant collection.

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