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Article

Anti-Termitic Activity of Three Plant Extracts, Chlorpyrifos, and a Bioagent Compound (Protecto) against Termite Microcerotermes eugnathus Silvestri (Blattodea: Termitidae) in Egypt

by
Mohamed Z. M. Salem
1,*,
Mona F. Ali
2,
Maisa M. A. Mansour
2,
Hayssam M. Ali
3,4,
Esraa M. Abdel Moneim
5 and
Ahmed Abdel-Megeed
6
1
Forestry and Wood Technology Department, Faculty of Agriculture (EL-Shatby), Alexandria University, Alexandria 21545, Egypt
2
Conservation Department, Faculty of Archaeology, Cairo University, Giza 12613, Egypt
3
Botany and Microbiology Department, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
4
Timber Trees Research Department, Sabahia Horticulture Research Station, Horticulture Research Institute, Agriculture Research Center, Alexandria 21526, Egypt
5
Conservation Department, Ministry of Antiquities, Giza 12578, Egypt
6
Department of Plant Protection, Faculty of Agriculture (Saba Basha), Alexandria University, Alexandria 21531, Egypt
*
Author to whom correspondence should be addressed.
Insects 2020, 11(11), 756; https://doi.org/10.3390/insects11110756
Submission received: 4 September 2020 / Revised: 31 October 2020 / Accepted: 2 November 2020 / Published: 4 November 2020
(This article belongs to the Special Issue Pest Management of Termites)
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Abstract

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Simple Summary

The termite Microcerotermes eugnathus Silvestri (Blattodea, Termitidae) showed structural damage in Bir al-Shaghala cemeteries located in the oasis of Dakhla, Egypt. The mud tubes of this termite spread inside and over the mural painted floors of the tombs. Extracts from Lavandula latifolia, Origanum vulgare, and Syzygium aromaticum were tested for their anti-termitic activity and compared with the bio-insecticide, Bacillus thuringiensis var. kurstaki (Protecto 9.4% WP) and Dursban (Chlorpyrifos 48%). The bioassay experimental showed that the extracts have low activity against M. eugnathus compared to Protecto and Dursban, but the extract from O. vulgare showed promising natural termiticides.

Abstract

A trend towards environmentally friendly chemicals for use in termite management has been occurring globally. This study examined three naturally occurring plant extracts from Lavandula latifolia (Spike lavender), Origanum vulgare (Marjorum), and Syzygium aromaticum (Clove) against the termite Microcerotermes eugnathus. Plant extract results were compared to two commercially used termite pesticides, the bio-insecticide, Bacillus thuringiensis var. kurstaki (Protecto 9.4% WP) and Dursban (Chlorpyrifos 48%). Gas chromatography–mass spectrometry (GC-MS) analysis was used to identify the main compounds in the three plant extracts. The main compounds in Lavandula Latifolia were linalool (21.49%), lavandulol (12.77%), β-terpinyl acetate (10.49%), and camphor (9.30%). Origanum vulgare extract contained thymol (14.64%), m-cymene (10.63%), linalool (6.75%), and terpinen-4-ol (6.92%) as main compounds. Syzygium aromaticum contained eugenol (99.16%) as the most abundant identified compound. The extract of O. vulgare caused the highest termite death rate, with an LC50 of 770.67 mg/L. Exposure to lavender extract showed a high death rate with an LC50 of 1086.39 mg/L. Clove extract did not show significant insecticidal activity with an LC50 > 2000 mg/L. Significant termiticide effects were found, with LC50 values of 84.09 and 269.98 mg/L for soldiers and workers under the application of Dursban and Protecto, respectively. The LC50 values reported for nymphs were <120, <164.5, and 627.87 mg/L after exposure to Dursban, Protecto, and O. vulgare extract, respectively. The results of the study show that some of the extracts have low toxicity compared to the bioagent and Dursban, and may show promise as natural termiticides, particularly as extracts from O. vulgare.

1. Introduction

Termites, although important in ecosystems, are economically important structural pests to wood and cellulosic material in service [1,2,3,4,5,6]. Bir al-Shaghala cemeteries, located to the west of the city of Mut, 3 km from Dakhla Oasis, Egypt, are the site of heavy infestation by the termite Microcerotermes eugnathus Silvestri (Blattodea, Termitidae) [7,8,9,10]. These termites forage and feed on the cellulosic material used in the construction of the mud brick from which the tombs are built. Termites infest the walls and tomb foundations, building noticeable foraging tubes (Figure 1).
In Egypt, this termite was reported along the northwestern coast [9] and in the Western Desert where the oasis of Dakhla is located [7]. Termite mud tubes spread inside and over the mural painted floors of the tombs, causing structural damage that often needs repair. The damage observed in some of the monastery buildings, as well as in a church located in a nearby village of Saint Catherine, was associated with M. eugnathus [8].
Treatments used to control this termite include bioagents, chemical pesticides, and natural products. Natural products investigated for termite management include plant extracts. In many parts of the world, chemical pesticides are considered poor for the environment and new research is examining the use of naturally occurring, less environmentally toxic, compounds [11,12,13].
Bioagents such as Bacillus thuringiensis var. kurstaki and Stenotrophomonas maltophilia Palleroni & Bradbury have potential application as biological control agents of termites [14,15,16]. The entomopathogenic bacteria B. thuringiensis is an example of this [17,18]. Chitinase produced by S. maltophilia has shown potential application as a biocontrol agent and could degrade chitin in the termites, Coptotermes heimi (Wasmann) (Blattodea: Rhinotermitidae) and Heterotermes indicola (Wasmann) (Blattodea: Rhinotermitidae) [15].
Dursban (Chlorpyrifos 48%) is an organophosphate pesticide that acts on the insect nervous system by inhibiting acetylcholinesterase (AChE) [19,20,21]. Dursban is still used in the Egyptian agriculture ecosystem, with some conditions [22]. Starting from May 2019, the California Department of Pesticide Regulation said, “the registration that allows Dursban to be sold in California will be canceled”, but this process could take up to two years [23]. In 2016, Denmark, Finland, Germany, Latvia, Sweden, Ireland, Lithuania, Slovenia and the United Kingdom banned, or never authorized, the use of Dursban products, and the Swiss government decided to withdraw permissions for 12 Dursban and Dursban-methyl products according to Tagblatt [24]. As toxic Dursban has been withdrawn for use in many countries, less toxic alternatives are being examined.
Natural products are being studied as potential termiticides. The termite C. intermedius Silvestri (Blattodea: Rhinotermitidae) died within 30, 40, and 110 min when exposed to 70% ethanol, aqueous, and acetone extracts from seeds of Parkia biglobosa (Jacq) Benth, respectively, at the concentration of 4 gm/L [25]. Seed oils from Khaya senegalensis (Desr.) A. Juss., K. ivorensis A. Chev. and Swietenia mahagoni (L.) Jacq. showed potential insecticidal efficacy towards the dry wood termite Kalotermes flavicollis (Fabricius, 1793) (Blattodea: Kalotermitidae) [26]. Water extracts from Larix leptolepis (Lamb.) Carr. Wood, with its large quantities of flavonoids, showed strong feeding deterrent activity against the subterranean termite Coptotermes formosanus Shiraki (Insecta: Blattodea: Rhinotermitidae) [27]. Jatropha curcas L. oil showed maximum wood protection against Microcerotermes beesoni Snyder (Termitidae: Amitermitinae) at a concentration of 20% [28].
Some heartwoods show resistance to termite attack, which is attributed to the presence of toxic compounds within the heartwood [29,30]. For example, heartwood extractives from Tectona grandis L.f., Dalbergia sissoo Roxb., Cedrus deodara (Roxb.) G.Don and Pinus roxburghii Sarg. rapidly lowered numbers of protozoans in the hindgut of Reticulitermes flavipes (Kollar) (Insecta: Blattodea: Rhinotermitidae) and H. indicola workers, which were closely correlated with the mortality of worker [30]. Wood samples from southern pine and poplar impregnated with the extractives from Morus alba L. heartwood resulted in 100% mortality in R. flavipes after feeding [31]. Methanolic and ethyl acetate extracts were found to be to be effective against the termite Microcerotermes beesoni Snyder (Termitidae: Amitermitinae) [32]. Heartwood extract from of D. sissoo showed termite mortality at 10 mg/mL against H. indicola and R. flavipes with LC50s at 5.54 and 3.89 mg/mL, respectively [33]. H. indicola mortality reached more than 75% after feeding on Populus deltoides W.Bartram ex Marshall wood treated with extract from M. alba [34].
Many plants contain bioactive compounds such as phenols, terpenoids (monoterpenes, sesquiterpenes, diterpenes, sesterpenes, and triterpenes), aldehydes, ketones, and other compounds that have a strong effect against microorganisms and termites [35,36,37,38,39,40,41]. For example, extracts from Cymbopogon citratus (DC.) Stapf, Eucalyptus globulus Labill., Syzygium aromaticum (L.) Merr. and L. M. Perry, Origanum vulgare L., Rosmarinus officinalis L., Cinnamomum verum J.Presl, and Thymus vulgaris L. showed strong termiticidal activity against Odontotermes assamensis Holmgren (Blattodea: Termitidae) [42]. Insecticidal activity from Cananga odorata (Lam.) Hook.f. and Thomson flower extract of 2 mg/filter paper showed cumulative mortalities of 18% and 94%, after 2 and 7 days of exposure, respectively, against the termite Reticulitermes speratus (Kolbe) (Rhinotermitidae: Blattodea) [43]. K. flavicollis pseudergates fed Casuarina sp. wood wafers, previously treated separately with Taxodium distichum (L.) Rich., E. citriodora Hook. and Cupressus sempervirens L. extracts, showed reduced numbers and vigour in spirochaete and flagellate populations [44]. At a dose of 6 μL/Petri-plate, Tagetes erecta L. leaf extract, caused 100% mortality in Odontotermes obesus (Rambur) (Blattodea: Termitidae) after 24 h of exposure [45]. Therefore, in the present study, three plant extracts were used as natural products to control the termite Microcerotermes eugnathus.
Lavender (Lavandula latifolia Medik.) belongs to the family Lamiaceae and is native to the Mediterranean. It is also cultivated in different regions of the world. The bioactivity of L. angustifolia Mill. and L. latifolia extracts from Spain were found to be associated with the presence of linalool, camphor, p-cymene, and limonene [46]. Linalool and linalyl acetate have been shown to be the main compounds in the extract of fresh and dry flowers from lavender [47]. Other constituents of lavender include α-pinene, thujene, β-pinene, sabinene, myrcene, p-cymene, limonene, camphene, camphor, 1,8-cineole, (Z)- and (E) ocimene, terpinene, terpinene-4-ol, lavandulol, lavandulylacetate, β-caryophyllene, and (Z)- and (E) farnesene [48].
Several Origanum (Marjoram–Lamiaceae family) species are characterized by the presence of two main chemotypes, thymol and carvacrol, while others have γ-terpinene, p-cymene, cis-sabinene hydrate, terpinen-4-ol, α-terpineol, α-terpinene, γ-terpinene, sabinene, and linalool as their main compounds [39,49,50,51,52]. O. vulgare L. ssp. vulgare extract showed the presence of caryophyllene, spathulenol, germacrene-D, and α-terpineol and had antimicrobial properties [53]. Terpinen-4-ol, γ-terpinene, α-terpineol, thymol, carvacrol, cis-sabinene-hydrate, linalool, p-cimene, 1,8-cineole were identified as the main compounds in the extract of O. vulgare L. [54]. O. vulgare extract and its major compounds carvacrol, p-cymene, and γ-terpinene showed potent larvicidal activity against the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae: Heliothinae) [55].
Clove (Syzygium aromaticum (L.) Merr. and L.M.Perry, Myrtaceae family) bud extract has shown the presence of eugenol, eugenol acetate and β-caryophyllene as main compounds with percentages of 88.61, 8.89 and 1.89%, respectively. It exhibited strong contact toxicity against Cacopsylla chinensis (Yang and Li) (Hemiptera: Psyllidae) with LD50 values of 0.730 µg/adult and 1.795 µg/nymph, respectively [56]. S. aromaticum extract gave LC50 values of 13.871 and 15.551 μL against larvae and adult Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae) 48 h after fumigation [57]. Other studies have indicated that the clove extract caused 100% mortality 48 h after treatment with the concentrations of 17.9 and 35 μL/g, and with LC50 values of 9.45 and 10.15 μL/g, against Acanthoscelides obtectus (Say) (Coleoptera: Chrysomelidae: Bruchinae) and Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae), respectively [58].
This research aimed to (1) determine the chemical composition of three plant extracts (lavender, marjoram and clove) with potential anti-termitic activities; (2) evaluate the anti-termitic activity of the three plant extracts against Microcerotermes eugnathus compared with two commercial pesticides used in termite control; the bioagent “Bacillus thuringiensis var. kurstaki” (Protecto 9.4% WP) and the chemical compound Dursban (chlorpyrifos 48%). In addition, the chemical composition of the three extracts were analyzed with using GC-MS apparatus.

2. Materials and Methods

2.1. Termite Infestation in the Cemeteries of Bir al-Shaghala at the Oases of Dakhla

Termite infestation in the cemeteries of Bir al-Shaghala located at the oases of Dakhla, Egypt was noted by the presence of Microcerotermes eugnathus foraging tubes. Termite tunnels could be observed on the floors and tomb substructure, causing cracks and separation of mortar. This termite species produces winged alates during the months of April and January, the remnants of which (wings) could often be observed around the tombs [59]. Figure 1A,B shows the cemetery termite damage.

2.2. Plant Extracts

Three plant extracts from Spike Lavender (Lavandula latifolia Medik., Lamiaceae) dry flower, Marjoram (Origanum vulgare L., Lamiaceae) dry leaves and Clove (Syzygium aromaticum (L.) Merrill and Perry, Mytaceae) dry buds were selected for their potential effect on termites. The extraction process was carried out at the National Research Center in Cairo, Egypt. Plant material was shade air-dried in the laboratory at room temperature for one week, then ground into a fine powder in an electrical blender. About 100 g of the fine powdered material was put into a 2-L flask containing 1000 mL of distilled water (DW) and extracted by the hydrodistillation method using a Clevenger-type apparatus for 3 h [60].

2.3. Gas Chromatography–Mass Spectrometry (GC-MS) Analysis of Extracts

The chemical composition of extracts from L. latifolia, O. vulgare, and S. aromaticum were determined using a Trace GC-TSQ Evo 9000 mass spectrometer (Thermo Scientific, Austin, TX, USA) with a TG–5MS direct capillary column (30 m × 0.25 mm × 0.25 µm film thickness). Extracts were diluted in n-hexane solvent in the ratio of 3:1 (3 n-heaxane: 1 extract sample) before being injected to the GC-MS. The column oven temperature was initially held at 50 °C and then increased by 5 °C/min to 250 °C and held for 2 min, then increased to a final temperature of 310 °C by 25 °C/min and held for 2 min. The injector and MS transfer line temperatures were kept at 270 and 260 °C, respectively; helium was used as a carrier gas at a constant flow rate of 1 mL/min. The solvent delay was 3 min, and diluted samples of 2 µL were injected automatically using an Autosampler AS1310 coupled with GC in the splitless mode. EI mass spectra were collected at 70 eV ionization voltages over the m/z range of 50–650 in full scan mode. The ion source temperature was set at 250 °C. The components were identified by comparison of their retention times and mass spectra with those in the WILEY 09 and NIST 11 mass spectral databases [61]. The match factor (MF) between the mass spectrum obtained for each compound and the library mass spectra for each compound was measured and reported; it was accepted if its value was more than or equal to 650 [36,38,39,40,62,63].

2.4. Preparation of the Plant Extracts, Protecto and Dursban

Extract concentrations for laboratory testing were prepared by mixing with 0.01% of Tween 80 and diluting with distilled water to obtain the following concentrations: 125, 250, 500, 1000, and 2000 mg/L. The bioagent “Bacillus thuringiensis var. kurstaki” (Protecto 9.4% WP) was diluted in distilled water to obtain the following concentrations: 164.5, 258.5, 376, 756, and 1410 mg/L. Dursban (Chlorpyrifos 48%) was diluted in distilled water and prepared in concentrations of 120, 240, 360, 480, and 960 mg/L.

2.5. Collecting and Rearing the Termites

Microcerotermes eugnathus castes were collected from soil around cemeteries and kept in a container with a portion of termite nesting material. Briefly, from the experimental location, termites were placed inside a special box (4-L in capacity) for preservation and the box was covered with wool textile to maintain the temperature, because the temperatures in the interior oases are as high as 50 °C. During the transfer to the laboratory in Cairo, the death of the termites occurs due to the different environmental conditions, so it was necessary to warm the termites. Termites’ death was also observed during transportation to the laboratory or even in the laboratory during the preparation for the laboratory experiment. Therefore, 10% glucose sugar solution [64,65] was placed where sterile cotton was absorbed into the sugar solution and suspended in a flask above the cardboard feeding medium as a source of nourishment for termites, to give moisture and nutrition. The termites were incubated at 48 ± 3 °C in order to provide a medium close to that of the oasis.

2.6. Testing Anti-Termitic Activity (No-Choice Bioassay Method)

A no-choice bioassay method [66,67] was employed to measure the anti-termitic activity of the three plant extracts, Protecto, and Dursban. 1125 pieces of cardboard similar to the laboratory rearing material were prepared and divided into three groups and each group contained 375 pieces and divided to five subgroups (75 pieces). In the first group, each subgroup (75 pieces) was dipped in each of the concentrations of plant extracts, in the second group (375 pieces); each subgroup (75 pieces) was dipped in each of the concentrations of Protecto, and the third group (375 pieces) each subgroup (75 pieces) was dipped in in each of the concentrations of Dursban. Treated cardboard samples were placed in glass flasks (2-L capacity), 15 pieces were used for each concentration, where termites were added and the flasks were sealed using a piece of gauze to allow ventilation. Each flask contained 10 workers and five soldiers (Total 15). With the same manner, the experiment was carried out with nymphs, where each flask contained five nymphs.
Untreated control replicates (five replicates) contained 10 workers, five soldiers and five nymphs, who were supplied with pieces of untreated cardboard paper only. Each concentration tested was replicated five times. All the treatments were kept in darkness at 48 ± 3 °C. After seven days, the test was halted, the number of surviving termites was counted, and percent mortality was calculated. The lethal concentration (LC50) expressed as mg/L was calculated from log-concentration mortality regression lines [38].

2.7. Statistical Analysis

Probit analysis was used to estimate the lethal concentrations LC50 from mortality data, and the slope was obtained according to Finney [68].

3. Results and Discussion

3.1. Chemical Composition of Three Plant Extracts

Table 1 shows the results of the Gas chromatography–mass spectrometry (GC-MS) analysis of L. latifolia extract. The main constituents, were linalool (21.49%), lavandulol (12.77%), β-terpinyl acetate (10.49%), camphor (9.30%), linalyl acetate (7.87%), (−)-β-fenchol (5.12%), isobornyl acetate (5.00%), α-pinene (3.81%), terpineol (3.64%), and L-α-terpineol (2.62%).
Table 2 shows the results of the GC-MS analysis of extract from O. vulgare dry leaves. The main components were thymol (14.64%), m-cymene (10.63%), terpinen-4-ol (6.92%), linalool (6.75%), estragole (5.42%), γ-terpinene (5.39%), anethole (5.00%), eucalyptol (3.61%), borneol (3.29%), β-caryophyllene (3.29%), α-terpinene (2.89%), carvacrol (2.58%), camphor (2.36%) and carvacryl methyl ether (2.34%).
Table 3 shows results of the GC-MS analysis of S. aromaticum extract. The main component was eugenol (99.16%).

3.2. Anti-Termitic Activity Comparison of Plant Extracts, Protecto and Dursban against Microcerotermes Eugnathus

The effects of the tested plant extracts showed that marjoram extract had the highest toxicity against Microcerotermes eugnathus. After a seven-day exposure to this extract, the LC50 was 770.67 mg/L against soldiers and workers and 627.87 mg/L against nymphs. Lavender extract had less of toxic effect against M. eugnathus than marjoram, with an LC50 of 1086.39 mg/L for the group of soldiers and workers and 1140.74 mg/L for nymphs. Clove extract showed the lowest insecticidal activity against M. eugnathus for both nymphs and soldier/workers, with an LC50 > 2000 mg/L (Table 4). Marjoram extract was most effective as an insecticide against M. eugnathus. Table 4 shows that the LC50 values for Dursban for individuals and nymphs were 84.09 and <120 mg/L, respectively. LC50 values for individuals and nymphs were <164.5 and 269.98 mg/L for Protecto, respectively.
Our results show that Dursban caused the highest termite mortality of 80%, while Protecto ranked second at 75% mortality. For the plant extracts, marjoram caused the highest mortality at 70% (Table 5).

4. Discussion

Many plant compounds can incur high mortality in termites. This is related to their mechanism of action on the insect nervous system [69]. Plant compounds may also have neurotoxic (hyperactivity, seizures, and tremors) modes of action [70,71,72]. The data presented in this work clearly show big differences in chemical components among plant samples depending on their origin, even in the same species.
Earlier studies showed that linalool, eucalyptol, camphor, α-pinene, α-terpineol, and α-bisabolene were the most abundant components in L. latifolia extract grown in the southeast of Spain [47]. Another study found linalool, 1,8-cineole, and camphor were dominant in extracts from seven natural populations of L. latifolia from the eastern Iberian Peninsula [73] and from wild Spanish populations [74]. The chemical composition of lab-distilled extract from L. latifolia and commercial spike lavender extract characterized 1.8-cineole, linalool, and camphor as major constituents [75]. Compounds from fresh stems and dry stemless flowers of lavender cultivars in Turkey showed linalool, linalyl acetate, camphor, sabinene, cimene, and terpeneol-4-ol as the main compounds [76]. Others reported α-fenchone, myrtenyl acetate, α-pinene, camphor and 1,8-cineole in the flowers of L. stoechas L. ssp. stoechas [77]. Fenchone and camphor (68.2% and 11.2%, respectively) were found in extract of L. stoechas from Tunisia [78].
Linalool, borneol and terpinene-4-ol, 1,8-cineole, camphor, and linalyl acetate were reported in lavandin (Lavandula x intermedia Emeric ex Loisel.) extract from Macedonia [79]. In another study from Iran, extract of dried lavender consisted predominately of 1,8-cineole, linalool, borneol, camphor, and linalyl acetate [80]. Linalool, camphor, 1,8-cineole, lavandulol, p-cymen-8-ol and bornyl acetate with values of 32.3%, 12.4%, 11.7%, 8.7%, 7.7%, and 4.2%, respectively, were the main compounds in L. latifolia extract from the Northern Tunisia [81]. Chemotypes of L. latifolia extracts from Spain, characterized by 1,8-cineole with high amounts (36.3–33.65%) [75,82], while L. latifolia from Iran showed the presence of linalool (31.9–30.6%) as the main compound [47]. In other species of Lavandula, 1,8-cineole, 2-β-pinene, α-thujone, camphor and cis-α-bisabolene were the main compounds isolated from L. angustifolia extract [83].
Previous work identified α-terpinene, γ-terpinene, cis-sabinene-hydrate, linalool, terpinen-4-ol, terpineol, thymol, and carvacrol as the main compounds in O. vulgare extract with percentages of 5.58, 12.32, 3.35, 3.47, 21.43, 3.17, 9.45, and 11.67%, respectively [54]. Other work found that O. vulgare extract contained p-cymene, linalool, thymol, caryophyllene, and carvacrol. These authors showed insecticidal activity against Schistocerca gregaria (Forskål) (Orthoptera: Acrididae) [84]. In the present study, thymol was found at 14.64% in O. vulgare extract. Other studies reported this same compound at 9.45% [54], 44.55% [85], 26.75% [86], and 58.31% [87]. After 5 h exposure, Coleus amboinicus Lour. extract caused 100% mortality to the termite Odontotermes obesus at a dose of 2.5 × 10−2 mg/cm3. This study found that thymol was the main compound, with 94.3% [88]. Extracts from Pittosporum undulatum Vent., Lippia sidoides Cham. and Lippia gracilis Schauer showed 100% mortality to the termite Heterotermes sulcatus Mathews (Blattodea: Rhinotermitidae) after 14 days of exposure, where the activity was related to the major compounds, limonene (80.8%), carvacrol (45.6%) and thymol (78.55%), that were identified in each extract, respectively [69].
Terpineol (22.85%), α–terpinene (20.60%), caryophyllene (6.75%) and thymol (4.53%) were the main compounds isolated from O. vulgare extract [89]. O. vulgare extract with its main compounds of thymol (40.35%), p-cymene (17.32%), γ-terpinene (15.66%), and carvacrol (12.15%), observed 72% and 88% mortality at 48 and 72 h, respectively, against Sitophilus oryzae (L.) (Coleoptera: Curculionidae) [90]. O. vulgare extract showed toxicity in higher doses against Plutella xylustella L. (Lepidoptera: Pyralidae) [91]. After application, O. vulgare extract at 40% exhibited 100% repellency against Cimex lectularius Linnaeus (Hemiptera: Cimicidae) [89].
Oxygenated monoterpenes such as thymol, eucalyptol, linalool and carvacrol found in the extracts from the present study are reported to be more toxic against termite workers [92]. For example, thymol and carvacrol from Origanum were shown to have insecticidal activity against larvae of Culex pipiens L. (Diptera: Culicidae) [93]. The extract of Lippia sidoides contained 44.55% thymol and showed high insecticidal activity against the termite Nasutitermes corniger (Blattodea: Termitidae) with 48 h exposure at a dose of 0.27 μg/mg [85].
In this study, clove extract showed the lowest activity against Microcerotermes eugnathus with an LC50 value of >2000 mg/L. Eugenol has been shown to be an effective fumigant and feeding deterrent against the termite C. formosanus [94]. Carvacrol has been shown to produce potent, acute toxicity to insects, nematodes, and mites [95]. It causes positive allosteric modulators in insects to bind to γ-aminobutyric acid, causing inhibitory symptoms in the nervous system [3]. Carvacrol caused 100% mortality of Odontotermes assamensis Holmgren (Blattodea: Termitidae) at 2.5 mg/g after 8 days [42]. At 1.5 mg/g and after 48 h, it exhibited anti-termitic activity against Reticulitermes messperatus Kolbe (Blattodea: Rhinotermitidae) nymphs [96,97]. S. aromaticum extract at 0.5 mL/L after 10 min of exposure showed 100% mortality against Coptotermes formosanus Shiraki (Insecta: Blattodea: Rhinotermitidae) [98]. Clove bud extract caused 100% mortality at 0.5 μL/L of air by fumigation method against R. speratus [99].
Our present results show a higher resistance of M. eugnathus against termiticides than those of other termites. In addition, our results suggest that O. vulgare extract caused moderate activity against the termite M. eugnathus compared to commercial termiticides tested. Further research may show that O. vulgare extract or its derivatives could potentially be used to control and manage some termite infestations and lessen or limit the amount of more toxic pesticides currently in use.

5. Conclusions

Chemical pesticides had the greatest impact on the mortality of the termite M. eugnathus. However, due to the highly toxic nature of Dursban and the fact that it has been withdrawn for use in some countries, the search for less toxic and natural termiticides from plants is of interest. Extract from the plant Origanum vulgare showed some promise as a plant-based toxicant for this termite.

Author Contributions

M.F.A., M.M.A.M., M.Z.M.S. and E.M.A.M. designed the experiments and conducted the laboratory analyses, M.F.A., M.M.A.M., M.Z.M.S., E.M.A.M. and H.M.A. wrote parts of the manuscript and interpreted the results; A.A.-M. revised the amended the scientific materials; all coauthors contributed to writing and revising the article. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Researchers Supporting Project number (RSP-2020/123) King Saud University, Riyadh, Saudi Arabia.

Acknowledgments

Researchers Supporting Project number (RSP-2020/123) King Saud University, Riyadh, Saudi Arabia.

Conflicts of Interest

The authors declare no conflict of interest.

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Insects 11 00756 g001 550
Figure 1. Bir Al-Shaghala Cemetery views and damage caused by termite attack. (A) damage occurred in the binding materials of mudbricks; (B) damage to the surface walls and shelter tubes of termites over the mudbricks.
Figure 1. Bir Al-Shaghala Cemetery views and damage caused by termite attack. (A) damage occurred in the binding materials of mudbricks; (B) damage to the surface walls and shelter tubes of termites over the mudbricks.
Insects 11 00756 g001
Table
Table 1. Gas chromatography–mass spectrometry (GC-MS) results for the extract of Lavandula latifolia.
Table 1. Gas chromatography–mass spectrometry (GC-MS) results for the extract of Lavandula latifolia.
Retention Time (min)Percentage in the Oil (%)Compound NameMatch Factor (MF)
4.743.81α-Pinene938
6.9510.49β-Terpinyl acetate913
8.9521.49Linalool944
10.489.30Camphor946
11.562.62L-α-Terpineol938
11.703.64α-Terpineol940
11.855.12(−)-β-Fenchol935
13.2912.77Lavandulol938
13.723.32Linalyl anthranilate914
14.355.00Isobornyl acetate953
16.237.87Linalyl acetate929
Table
Table 2. GC-MS results for the extract of Origanum vulgare.
Table 2. GC-MS results for the extract of Origanum vulgare.
Retention Time (min)Percentage in the Oil (%)Compound NameMatch Factor (MF)
6.612.89α-Terpinene939
6.8510.63m-Cymene939
7.043.61Eucalyptol939
7.755.39γ-Terpinene939
8.926.75Linalool930
9.982.36Camphor955
10.643.29Borneol937
11.006.92Terpinen-4-ol (4-Terpinenol)943
11.585.42Estragole (4-Allylanisole)956
12.772.34Carvacryl methyl ether873
13.955.00Anethole955
14.3114.64Thymol929
14.552.58Carvacrol930
17.443.29β-Caryophyllene954
Table
Table 3. GC-MS results for the extract of Syzygium aromaticum.
Table 3. GC-MS results for the extract of Syzygium aromaticum.
Retention Time (min) Percentage in the Oil (%)Compound NameMatch Factor (MF)
5.9299.16Eugenol852
Table
Table 4. The insecticidal activity of three plant extracts, Dursban, and Protecto against termite groups.
Table 4. The insecticidal activity of three plant extracts, Dursban, and Protecto against termite groups.
TreatmentTermite GroupsLC50LC90Slope ± SEχ2 Sig.
Conc
mg/L		95% CIConc
mg/L		95% CI
LowerUpperLowerUpper
Spike lavender oilNymphs1140.74521.932493.2117,591.548048.8138,448.221.09 ± 0.170.62
Soldiers and workers1086.39563.862093.1710,134.455259.9619,526.211.33 ± 0.140.88
Marjoram oilNymphs627.87292.671346.979474.854416.6020,326.201.091 ± 0.170.88
Soldiers and workers770.67420.411412.737006.473822.1712,843.681.42 ± 0.130.73
Clove oilNymphs>2000
Soldiers and workers>2000
DursbanNymphs<120
Soldiers and workers84.0945.260156.255568.587306.0121056.4641.55 ± 0.130.99
ProtectoNymphs<164.5
Soldiers and workers269.98108.85669.677163.842888.2217,768.940.91 ± 0.210.99
Table
Table 5. Effect of various compounds on the mortality of the termite Microcerotermes eugnathus (soldiers/workers and Nymphs) in a no-choice laboratory test.
Table 5. Effect of various compounds on the mortality of the termite Microcerotermes eugnathus (soldiers/workers and Nymphs) in a no-choice laboratory test.
DursbanProtectoPlant Extracts
Conc
(mg/L)		Mortality %Conc
(mg/L)		Mortality %Conc
(mg/L)		Mortality (%)
MarjoramLavenderClove
Control0Control0Control000
12048164.535125151015
24051258.545250201520
3606037651500201520
48065756501000304020
960801410752000705025
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Salem, M.Z.M.; Ali, M.F.; Mansour, M.M.A.; Ali, H.M.; Abdel Moneim, E.M.; Abdel-Megeed, A. Anti-Termitic Activity of Three Plant Extracts, Chlorpyrifos, and a Bioagent Compound (Protecto) against Termite Microcerotermes eugnathus Silvestri (Blattodea: Termitidae) in Egypt. Insects 2020, 11, 756. https://doi.org/10.3390/insects11110756

AMA Style

Salem MZM, Ali MF, Mansour MMA, Ali HM, Abdel Moneim EM, Abdel-Megeed A. Anti-Termitic Activity of Three Plant Extracts, Chlorpyrifos, and a Bioagent Compound (Protecto) against Termite Microcerotermes eugnathus Silvestri (Blattodea: Termitidae) in Egypt. Insects. 2020; 11(11):756. https://doi.org/10.3390/insects11110756

Chicago/Turabian Style

Salem, Mohamed Z. M., Mona F. Ali, Maisa M. A. Mansour, Hayssam M. Ali, Esraa M. Abdel Moneim, and Ahmed Abdel-Megeed. 2020. "Anti-Termitic Activity of Three Plant Extracts, Chlorpyrifos, and a Bioagent Compound (Protecto) against Termite Microcerotermes eugnathus Silvestri (Blattodea: Termitidae) in Egypt" Insects 11, no. 11: 756. https://doi.org/10.3390/insects11110756

APA Style

Salem, M. Z. M., Ali, M. F., Mansour, M. M. A., Ali, H. M., Abdel Moneim, E. M., & Abdel-Megeed, A. (2020). Anti-Termitic Activity of Three Plant Extracts, Chlorpyrifos, and a Bioagent Compound (Protecto) against Termite Microcerotermes eugnathus Silvestri (Blattodea: Termitidae) in Egypt. Insects, 11(11), 756. https://doi.org/10.3390/insects11110756

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