Acaricidal, Insecticidal, and Nematicidal Efficiency of Essential

International Journal of Environmental Research and Public Health

Review Acaricidal, Insecticidal, and Nematicidal Efﬁciency of Essential Oils Isolated from the Satureja Genus

Asgar Ebadollahi 1,* , Jalal Jalali Sendi 2 , Masumeh Ziaee 3 and Patcharin Krutmuang 4,5,*

1 Department of Plant Sciences, Moghan College of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil 56199-36514, Iran 2 Department of Plant Protection, Faculty of Agricultural Sciences, University of Guilan, Rasht 41635-1314, Iran; [email protected] 3 Department of Plant Protection, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz 61357-43311, Iran; [email protected] 4 Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai 50200, Thailand 5 Innovative Agriculture Research Center, Faculty of Agriculture, Chiang Mai University, Chiang Mai 50200, Thailand * Correspondence: [email protected] (A.E.); [email protected] (P.K.)

Abstract: The overuse of synthetic pesticides in plant protection strategies has resulted in numerous side effects, including environmental contamination, food staff residues, and a threat to non-target organisms. Several studies have been performed to assess the pesticidal effects of plant-derived

essential oils and their components, as partially safe and effective agents, on economically important pests. The essential oils isolated from Satureja species are being used in medicinal, cosmetic, and

Citation: Ebadollahi, A.; Jalali Sendi, food industries. Their great potential in pest management is promising, which is related to high J.; Ziaee, M.; Krutmuang, P. amounts of terpenes presented in this genus. This review is focused on the acute and chronic Acaricidal, Insecticidal, and acaricidal, insecticidal, and nematicidal effects of Satureja essential oil and their main components. The Nematicidal Efﬁciency of Essential effects of eighteen Satureja species are documented, considering lethality, repellency, developmental Oils Isolated from the Satureja Genus. inhibitory, and adverse effects on the feeding, life cycle, oviposition, and egg hatching. Further, the Int. J. Environ. Res. Public Health 2021, biochemical impairment, including impairments in esterases, acetylcholinesterase, and cytochrome 18, 6050. https://doi.org/10.3390/ P450 monooxygenases functions, are also considered. Finally, encapsulation and emulsiﬁcation ijerph18116050 methods, based on controlled-release techniques, are suggested to overcome the low persistence and water solubility restrictions of these biopesticides. The present review offers Satureja essential Academic Editors: Surendra K. Dara oils and their major components as valuable alternatives to synthetic pesticides in the future of and Stefan T. Jaronski pest management.

Received: 14 April 2021 Accepted: 1 June 2021 Keywords: biopesticides; essential oil; multiple modes of action; Satureja; terpenes Published: 4 June 2021

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in 1. Introduction published maps and institutional affil- Although synthetic chemicals have been considered as the pest management strategy iations. so far, their overuse has led to several side effects. These include soil and groundwater pollution, toxic residues on the food stuffs, pest resistance, outbreak of secondary pests, and harmful effects on non-target organisms such as fish, bees, predators, and parasites [1–4]. The plant essential oils as low-risk agents are recommended alternatives to chem- Copyright: © 2021 by the authors. ical pesticides [5,6]. Essential oils are complex mixtures of aromatic and aliphatic com- Licensee MDPI, Basel, Switzerland. pounds, which mainly consist of hydrocarbon monoterpenes, monoterpenoids, hydro- This article is an open access article carbon sesquiterpenes, and sesquiterpenoids, and can be made by all plant parts, such distributed under the terms and as flowers, seeds, leaves, stems, and bark [7]. Essential oils are composed by plants as conditions of the Creative Commons secondary metabolites with anti-herbivore activity, resulted in critical defense strategies Attribution (CC BY) license (https:// against herbivorous pests along with other significant roles, such as allelopathic plant–plant creativecommons.org/licenses/by/ interactions and attraction of pollinators [8]. Hence, the possibilities of pest resistance 4.0/).

Int. J. Environ. Res. Public Health 2021, 18, 6050. https://doi.org/10.3390/ijerph18116050 https://www.mdpi.com/journal/ijerph Int. J. Environ. Res. Public Health 2021, 18, 6050 2 of 16

to plant-derived essential oils is very low [9]. Along with multiple modes of action and efficiency against a wide range of arthropod pests, essential oils also exhibit comparative lower toxicity on non-target organisms, such as mammals and beneficial insects compared to chemicals [10]. Additionally, with about 24–48 h half-lives, they are degraded quickly by natural degradation mechanisms and considered as biodegradable agents [9]. The pesticidal effects of essential oils isolated from several species of plant families, such as Lamiaceae, Asteraceae, Myrtaceae, Apiaceae, Cupressacae, and Rutaceae, against diverse groups of agricultural pests have been well-endorsed in recent years [11–13]. Along with the toxicity of plant essential oils to arthropod pests, there are promising findings against pathogenic nematodes [14,15]. The genus Satureja belongs to the Lamiaceae family, Nepetoidae subfamily, and the Mentheae tribe, that includes about 200 species of aromatic herbs and shrubs. They are broadly distributed in America, the Mediterranean area, Middle East, North Africa, and West Asia [16]. Several species from this genus, conventionally known as savory, especially summer savory (Satureja hortensis L.), are cultivated in various countries [17]. These aromatic plants possess a high content of essential oil (even about 4%) located in their leaves, stems, and flowers [18]. Numerous medicinal properties, including reduction of blood pressure, joint pains, rheumatic pains, stomachache, toothache, fever, diarrhea, dyspepsia, gastrointestinal bloating, influenza, colds, scabies and itching, eye strengthening, antioxidant, antidiabetic, and antimicrobial properties, of Satureja species, especially their extracted essential oils, are well-documented in the literature [16,19–21]. The present review aimed to update the current knowledge on the essential oils extracted from different Satureja species in controlling economically damaging insects, mites, ticks, and nematodes. Thus, vast amounts of individual research have been gathered from scientific databases, including Scopus, Web of Science, PubMed, and Google Scholar. Our main aim was to introduce a novel, safe, and efficient bio-rational agent(s), as alternatives to the detrimental chemicals. The search also considers the sub-lethal and biochemical changes after application of these compounds in order to obtain a thorough insight into their mode of action.

2. Pesticidal Effects of Essential Oils Extracted from Various Satureja Species The great potential of several species from the Satureja genus, including S. aintabensis Davis, S. bachtiarica Bung, S. cilicica Davis, S. cuneifolia Ten, S. hellenica Halásky, S. hortensis L., S. intermedia C. A. Mey, S. isophylla L., S. khuzestanica Jamzad, S. montana L., S. parnassica Heldr & Sart ex Boiss, S. parvifolia (Phil) Epling, S. rechingeri Jamzad, S. sahendica Bornm, S. spicigera Boiss, S. spinosa L., S. thymbra L., and S. wiedemanniana (Avé-Lall) Velen, has been reported in the insects, mites, ticks, and nematodes’ management. As shown in Table1, the efﬁciency of Satureja essential oils was assessed against a diverse group of insects from Coleoptera to Diptera, Hemiptera, Homoptera, Lepidoptera, Phthiraptera, and Thysanoptera orders, and similarly, on other arthropods, including mites and ticks, and plant pathogenic nematodes. The pesticidal effects of Satureja essential oils can be considered from two viewpoints, i.e., lethal and sub-lethal. For example, along with acute fumigant toxicity of S. thymbra essential oil against the adults of Acanthoscelides obtectus, Ephestia. kuehniella, and Leptinotarsa decemlineata, its repellent effect on Aedes albopictus was also reported [22–24]. In general, there are several sub-lethal bio-efﬁciencies of Satureja essential oils, including repellent and antifeedant activities and adverse effects on fecundity, fertility, and life cycle. Some of these studies have also considered the biochemical mode of action in pests such as general esterase, acetylcholinesterase, and cytochrome P450 monooxygenases [25–27]. The studies include different developmental stages of pests, from eggs to larvae, pupae, and adults. Among the large species of Satureja studied, the essential oils of S. hortensis, S. montana, and S. thymbra are considered as the most promising in pest management (Table1) . Another prospective is the possibility of using Satureja essential oil along with other pest control agents, such as entomopathogenic fungi. For example, Hosseinzadeh et al. [28] Int. J. Environ. Res. Public Health 2021, 18, 6050 3 of 16

indicated that the essential oil of S. sahendica had a signiﬁcant synergistic effect with entomopathogenic fungus Beauveria bassiana against the cowpea weevil, Callosobruchus maculatus (Fabricius).

Table 1. Reported acaricidal, insecticidal, and nematicidal effects of the essential oils isolated from different Satureja species.

Pests Satureja Species Bioassay and Target Pest Efﬁciency

Contact assay (on treated filter papers) against Significant toxicity with LC50 (lethal Insects S. aintabensis Davis the adult females of the turnip aphid (Lipaphis concentration to kill 50% of tested insects) of pseudobrassicae (Davis)). 1.7 mg/mL after 1 h [29]. Aqueous suspension of essential oil against the third- and fourth-instar larvae of the Asian The larval mortality of 100% at the S. bachtiarica Bung malaria mosquito (Anopheles stephensi) and concentration of 160 ppm after 24 h [30]. filariasis vector (Culex quinquefasciatus Say). Fumigant and repellency assays (by Significant fumigant toxicity impregnated filter papers in glass vials and (LC = 4.71 mg/L) and repellent action (100% Petri dishes, respectively) against the adults of 50 at the concentration of 1% v/v after 8 h) [31]. red flour beetle (Tribolium castaneum (Herbst)). Fumigant assay (by impregnated filter papers) Significant fumigant toxicity against the fourth-instar larvae of tomato (LC50 = 25.03 µL/L) and reduction in activity leafminer (Tuta absoluta (Meyrick)) of general esterases (α and β)(p < 0.05) [25]. High mortality of the first (97.7%), second Contact assay (on treated filter papers) against (95.5%), third (91.1%), and fourth (97.7%) S. cilicica Davis the Colorado potato beetle instar larvae and the adults (84.4%) at (Leptinotarsa decemlineata Say). 20 µL/cm2 after 96 h [24]. Fumigant assay (by impregnated filter papers) The knockdown rate of 100% at the S. cuneifolia Ten on field-collected sand flies (Diptera: concentration of 20.0 µL/L after 0.5 h [32]. Psychodidae: Phlebotomie). High mortality of the first (93.3%), second Contact assay (on treated filter papers) against (91.1%), third (95.5%), and fourth (88.8%) L. decemlineata. instar larvae and the adults (86.6%) at 20 µL/cm2 after 96 h [24]. Significant toxicity (LC50 = 36.0 µg/mL), the reduction in the adult emergence by a quarter Aqueous suspension of essential oil against S. hortensis L. of the control (p < 0.05), and 100% oviposition the larvae of the C. quinquefasciatus. deterrence by the concentration of 200 ppm [33]. Fumigant assay (by impregnated filter papers) The mortality of 100% at the concentration of against the adults of bean weevils (Bruchus 20.0 µL/L after 24 h [34] dentipes (Baudi)). Fumigant assay (by impregnated filter papers) The 100% mortality of adult females at against the cotton whitefly (Bemisia tabaci) on 2.4 mL/cm3 of essential oil after 24 h [35]. the eggplant leaves. Fumigant assay (by impregnated filter papers) The mortality of 100% at 2 µL/L of essential against the adults of B. tabaci on oil after 12 h [36]. cucumber leaves. Toxic to the adults with LC values of 5.36 Contact assay (on treated filter papers) against 50 and 6.41 µL/cm2 on the males and females, the adults of C. maculatus. respectively [37]. The 91.2% adult mortality at 60 mL/L and the Fumigant assay (by impregnated filter papers) 94.5% egg mortality at 4.3 mL/L of essential against the adults of C. maculatus. oil after 24 h [38]. Fumigant assay (by impregnated filter papers) The 100% mortality at the concertation of against the adults of maize weevil 10 µL/L after 96 h exposure time [39]. (Sitophilus zeamais Motschulsky). Significant feeding inhibition (44.35% at the concentration of 0.025%), decrease in the Leaf dipping method against the larvae of amount of protein, lipid, carbohydrates, and mulberry pyralid (Glyphodes pyloalis Walker) the activity of α-amylase, esterase, and glutathione S-transferase (p < 0.05) [40]. Significant reduction in the relative growth (0.01 mg/day) and consumption Antifeedant assay (by treated flour disk) on (0.31 mg/day) rates of larvae treated by first-instar larvae of the Indian meal moth 0.22 µL/cm2 of essential oil compared to (Plodia interpunctella Hübner). control (0.05 and 0.10 mg/day, respectively) (p < 0.05) [41]. In-vivo repellent assay (by counting the A protection time of 4.16 h at ED (effective number of bites on the back of rabbits) against 50 dose) of 5.63 mg/cm2 [42]. the adult females of A. stephensi. Int. J. Environ. Res. Public Health 2021, 18, 6050 4 of 16

Table 1. Cont.

Pests Satureja Species Bioassay and Target Pest Efficiency Contact assay (by direct spraying) on the The 68.8% mortality of third- and larvae of the American White Butterfly fourth-instars larvae at 1.67 µL/cm2 (Hypantria cunea Drury). after 96 h [43] Spraying on black chokeberry inflorescences Significant reduction in the amount of α- and ingested by the larvae of grey Knot-horn β-glucosidase of treated larvae and the (Acrobasis advenella (Zinck)). emergence and longevity of adults [17]. Fumigant assay (by impregnated filter papers) A mortality of 88.3% at 60 µL/L after 24 h on the third-instar larvae of Mediterranean (LC = 30.09 µL/L) [44]. flour moth (Ephestia kuehniella Zeller). 50 Significant reduction in laid eggs (3.89%) and Oviposition deterrence and feeding-site assays feeding site of larvae (27.35%) compared to (by choice test with treated black chokeberry control groups (17.15% and 4.69%, infructescences) on A. advenella. respectively) [45]. Fumigant assay (by impregnated filter papers) Significant toxicity against both insects with against the adults of lesser grain borer LC values of 16.47 and 25.75 µL/L after 72 h, (Rhyzopertha dominica (Fabricius)) and 50 respectively [46]. T. castaneum. Fumigant assay (by impregnated filter papers) against the adults of saw-toothed beetle High fumigant and contact toxicity against all (Oryzaephilus surinamensis (L.)), R. dominica, the pests with LC values of 8.15, 12.83, 2.49, and S. intermedia C. A. Mey khapra beetle (Trogoderma granarium Everts), 50 35.61 µL/L, and 418.38 µg/mL, and T. castaneum, and contact assay (leaf respectively [47]. dipping method) on the adult female of the oleander aphid (Aphis nerii). Fumigant assay (by impregnated filter papers) Significant fumigant toxicity against both against cabbage aphid (Brevicoryne brassica L.) S. isophylla L. insects with LC values of 7.33 and and black bean aphid (Aphis fabae Scop) on 50 14.29 µL/L, respectively [48]. acacia leaves. Significant fumigant toxicity against adult Fumigant assay (by impregnated filter papers) females (LC50 = 14.29 µL/L) and nymph against A. fabae on acacia leaf. production detergency at 8.53 µL/L (p < 0.05) [49]. Fumigant assay (by impregnated filter papers) High mortality of R. dominica (98.7%) and T. against the adults of R. dominica and castaneum (90.0%) at 35.3 and 55.0 µL/L T. castaneum. concentrations respectively, after 72 h [50]. In vivo mosquito repellents assay for human Significant reduction in the number of S. khuzestanica Jamzad skin (from elbow to wrist) against the adults of mosquito bites compared to the control group A. stephensi. (p < 0.01) [51]. Significant mortality of the fourth-instar larvae Toxicity assay (by impregnated potato leaves and adults with LC values of 23.36 and in Petri dishes) on the adults of L. decemlineata. 50 167.96 ppm, respectively [52]. Fumigant and repellent assays (by Significant fumigant toxicity impregnated filter papers in glass vials and (LC = 2.51 mg/L) and repellent action (100% Petri dishes, respectively) against the adults of 50 at the concentration of 1% v/v after 8 h) [31]. T. castaneum. Significant fumigant toxicity Fumigant assay (by impregnated filter papers) (LC = 17.51 µL/L) and reduction in activity against the fourth-instar larvae of T. absoluta. 50 of general esterases (α and β)(p < 0.05) [25]. Aqueous suspension of essential oil on the Significant larvicidal activity with LC value S. montana L. fourth-instar larvae of common house 50 of 37.70 mg/L [53]. mosquito (Culex pipiens L.). Repellent assay (by treated green bean leaves A complete repellency (100%) at the in Petri dishes) on the Western flower thrips concentration of 2.0% after 1 h [54]. (Frankliniella occidentalis). Significant toxicity with LC values of 2.95 Contact assay (topical application) against the 50 and 4.59 µg/fly on the male and female adults, fruit fly (Drosophila suzukii (Matsumura)). respectively [26]. Aqueous suspension of essential oil against High larvicidal effectiveness with LC50 value the third-instar larvae of C. quinquefasciatus of 25.6 µL/L [55]. High mortality of the first (100%), second Contact assay (on treated filter papers) against (97.7%), third (95.5%), and fourth (97.7%) L. decemlineata. instar larvae and the adults (88.8%) at the concentration of 20 µL/cm2 after 96 h [24]. S. parnassica Heldr & Aqueous suspension of essential oil on the Significant larvicidal activity with LC50 value Sart ex Boiss fourth-instar larvae C. pipiens. of 37.70 mg/L [53]. Int. J. Environ. Res. Public Health 2021, 18, 6050 5 of 16

Table 1. Cont.

Pests Satureja Species Bioassay and Target Pest Efﬁciency

Fumigant assay (by impregnated filter papers) Significantly toxic with KT50 value (time to S. parvifolia (Phil.) Epling on the adult-females of the head louse 50% knockdown) of 36.06 min at 60 µL of (Pediculus humanus capitis De Geer). essential oil concentration [56]. Repellent assay (by treated filter papers in The repellency of 100% and 76.0% at the Petri dishes) against the nymphs of kissing concentration of 0.5% (w/v) after bug (Triatoma infestans Klug). 1 and 24 h [57]. Fumigant and repellency assays (by Significant fumigant toxicity impregnated filter papers in glass vials and S. rechingeri Jamzad (LC = 3.27 mg/L) and repellent action (100% Petri dishes, respectively) against the adults of 50 at the concentration of 1% v/v) after 8 h [31]. T. castaneum. Significant fumigant toxicity Fumigant assay (by impregnated filter papers) (LC = 34.33 µL/L) and reduction in activity against the fourth-instar larvae of T. absoluta. 50 of general esterases (α and β)(p < 0.05) [25]. Fumigant assay (by impregnated filter papers) Significant toxicity with LC value of S. sahendica Bornm 50 against the adults of C. maculatus. 22.42 µL/L [28]. Fumigant assay (by impregnated filter papers) The 94.27% mortality at the concentration of S. spicigera Boiss against the adults of granary weevil 20.0 µL/L after 86 h [58]. (Sitophilus granarius (L.)). Fumigant assay (by impregnated filter papers) The mortality of 100% at concertation of against S. zeamais. 10 µL/L after 96 h exposure time [39]. High mortality of the first (100%), second Contact assay (on treated filter papers) against (100%), third (95.5%), and fourth (95.5%) instar L. decemlineata. larvae and the adults (80.0%) at 20 µL/cm2 after 96 h [24]. Aqueous suspension of essential oil on the Significant larvicidal toxicity with LC value S. spinosa L. 50 fourth-instar larvae C. pipiens. of 37.70 mg/L [53]. Aqueous suspension of essential oil on the Significant larvicidal toxicity with LC value S. thymbra L. 50 fourth-instar larvae C. pipiens. of 37.70 mg/L [53]. Fumigant assay (by impregnated filter papers) The 100% egg mortality of E. kuehniella and P. against E. kuehniella and P. interpunctella. interpunctella at 200 µL/L after 96 h [59]. Fumigant assay (by impregnated filter papers) The 100% mortality of E. kuehniella, P. against the adults of E. kuehniella, P. interpunctella (at 9 and 25 µL/L respectively, interpunctella, and bean weevil after 24 h), and A. obtectus (195 µL/L (Acanthoscelides obtectus Say). after 144 h) [22]. Significant adulticidal toxicity (LC = 13.92 µL/L after 12 h) and reduction Fumigant assay (by impregnated filter papers) 50 in the larval and adult emergence and egg against E. kuehniella. production compared to control groups (p < 0.05) [60]. Fumigant (by impregnated filter papers on the The 100% mortality of adults and larvae at adults) and aqueous suspension (on the larvae) 32.2 µg/mL and 3 mg/mL of essential oil assays on African malaria mosquito (Anopheles respectively, after 24 h [61]. gambiae Giles). Spraying on grape leaves against the nymphs Significant mortality on nymphs and female adults of the vine mealybug (LC50 = 2.7 mg/mL) and adults (Planococcus ficus (Signoret)). (LC50 = 6.3 mg/mL) after 24 h [62]. In vivo larvicidal assay in basins against the Significant larval mortality (96.00% at 29 mg/L larvae of dengue vector of the essential oil) after 24 h [23]. (Aedes albopictus Skuse). High mortality of the first (100.0%), second Contact assay (on treated filter papers) against (95.5%), third (97.7%), and fourth (95.5%) L. decemlineata. instar larvae and the adults (97.7%) at 20 µL/cm2 after 96 h [24]. S. wiedemanniana Contact toxicity (on treated filter papers) Significant toxicity with LC50 of 1.0 mg/mL (Avé-Lall) Velen against the adult females L. pseudobrassicae. after 1 h [29]. Fumigant (by impregnated filter papers) and Significant fumigant toxicity repellency assays (by treated leaf discs) against Mites and Ticks S. bachtiarica (LC = 44.06 µL/L) and high repellent action the two-spotted spider mite (Tetranychus 50 at 44.06 µL/L after 24 h [27]. urticae Koch) in Petri dishes. The 96.6% mortality of nymphs and adults of Fumigant assay (by impregnated filter papers) S. hortensis T. urticae at concentration of 3.13 µL/L against T. urticae on fresh leaves of bean. after 96 h [63]. Fumigant (by impregnated filter papers) and Significant fumigant and contact toxicity with contact (leaf dipping method) assays on the LC50 values of 7.074 µL/L and 0.876% (v/v), adults of T. urticae. respectively [64]. Significant toxicity against the adults and eggs Fumigant assays (by impregnated filter with 24 h LC values of 1.44 and papers) against T. urticae on bean leaves. 50 1.31 µL/L [65]. Int. J. Environ. Res. Public Health 2021, 18, 6050 6 of 16

Table 1. Cont.

Pests Satureja Species Bioassay and Target Pest Efficiency Fumigant (by impregnated filter papers) and Significant fumigant toxicity S. khuzestanica repellency assays (by treated leaf discs) against (LC50 = 31.11 µL/L) and high repellent action T. urticae in Petri dishes. at 18.85 µL/L after 24 h [27]. Significant adulticidal (24 h LC = 0.98 µL/L) Fumigant assay (by impregnated filter papers) 50 S. sahendica and ovicidal (72 h LC = 0.54 µL/L) against T. urticae on bean leaf discs. 50 toxicity [66]. Fumigant assay (by treated cotton wick) on the The complete mortality (100%) at 40.0 µL/L S. thymbra adults of the Mediterranean tick within 3 h [67]. (Hyalomma marginatum). Immersion of the cotton root-knot nematode The 100% paralysis of the second-stage (Meloidogyne incognita (Kofold & White)) and Nematodes S. hellenica Halácsy juveniles (J2) of both species at the the root-knot nematode (Meloidogyne javanica concentration of 2000 µL/L after 96 h [68]. (Treub)) in aqueous suspension of essential oil. Immersion of the mixed stages of pine wood The 100% mortality of nematodes exposed to a S. montana nematode (Bursaphelenchus xylophilus Nickle) 2 mg/mL solution after 24 h [69]. in aqueous suspension of essential oil. Spraying of the aqueous suspension of Significant decrease in the population growth essential oil on B. xylophilus co-cultured with of nematode compared to the control groups Pinus pinaster shoot. (p < 0.05) [70]. Spraying of the aqueous suspension of essential oil on the Columbia root-knot Significant decrease in the population growth nematode (Meloidogyne chitwoodi Golden) of nematode compared to the control groups co-cultured with Solanum tuberosum (p < 0.05) [71]. hairy roots.

Furthermore, as shown in Table1, in addition to agricultural pests, the acute toxicity and repellent action of Satureja essential oils against larvae and adults of blood-sucking mosquitos that carry pathogenic agents were also approved. For example, high susceptibility of the Asian malaria mosquito (A. stephensi) and the ﬁlariasis vector mosquito (C. quinquefasciatus) to the essential oil of S. bachtiarica was reported, in which 100% larval mortality of both insects was attained by the concentration of 160 ppm after 24 h exposure time [30].

3. Relationship between Compositions of Satureja Essential Oils with Pesticidal Properties The major compounds of essential oils of different Satureja species’ insecticidal, acaricidal, and nematicidal activities are depicted in Table2. Some compounds such as γ-terpinene, borneol, carvacrol, p-cymene, and thymol were identiﬁed in many species. For example, thymol with high percentage is the main compound of S. aintabensis, S. bachtiarica, S. cilicica, S. intermedia, S. isophylla, S. montana, S. parnassica, S. sahendica, S. spinosa, S. thymbra, and S. wiedemanniana essential oils. However, some compounds, such as estragole, piperitenone, piperitenone oxide, α-terpineol, β-caryophyllene, and β-myrcene, were recognized in a species: estragole in the S. hortensis, Piperitenone and piperitenone oxide in S. parvifolia essential oil, and β-myrcene in S. isophylla essential oil (Table2).

Table 2. Main components of the Satureja species essential oils documented as promising insecticidal, acaricidal, and nematicidal agents.

Essential Oil Main Components S. aintabensis p-Cymene (33%) and thymol (32%) [29]. S. bachtiarica Thymol (28.0%), caryophyllene oxide (17.0%), carvacrol (13.2%), borneol (11.6%), and linalool (9.6%) [31]. S. cilicica Thymol (68.9%), p-cymene (7.8%), borneol (2.9%), and linalool (1.8%) [29]. S. cuneifolia Carvacrol (48.7%), p-cymene (38.1%), α-terpineol (1.9%), and borneol (1.9%) [72]. S. hellenica p-Cymene (27.46%), carvacrol (23.25%), and borneol (6.79%) [68]. S. hortensis Estragole (82.1%), β-ocimene (11.9%), and limonene (2.3%) [46]. S. intermedia Thymol (48.1%), carvacrol (11.8%), p-cymene (8.1%), and γ-terpinene (8.1%) [47]. S. isophylla Thymol (41.5%), p-cymene (25.9%), γ-terpinene (16.9%), β-myrcene (2.1%), and α-terpinene (1.6%) [50]. S. khuzestanica Carvacrol (48.0%), p-cymene (18.5%), and γ-terpinene (11%) [21]. Int. J. Environ. Res. Public Health 2021, 18, 6050 7 of 16

Table 2. Cont.

Essential Oil Main Components S. montana Carvacrol (58.3%), p-cymene (18.3%), γ-terpinene (9.2%), and thymol (4.8%) [73]. S. parnassica Carvacrol (6.4%), thymol (44.4%), γ-terpinene (12.3%), p-cymene (8.4%), and β-caryophyllene (4.4%) [53]. S. parvifolia Piperitenone oxide (67.3%), piperitenone (7.2%), and pulegone (1.9%) [74]. S. rechingeri Carvacrol (82.5%), γ-terpinene (2.7%), p-cymene (2.6%), and terpinene-4-ol (2.0%) [31]. S. sahendica p-Cymene (30.2%), thymol (29.6%), and γ-terpinene (27.7%) [75]. S. spicigera Carvacrol (90.1%), p-cymene (4.1%), and γ-terpinene (2.6%) [29]. S. spinosa Carvacrol (47.1%), thymol (12.4%), γ-terpinene (6.5%), p-cymene (5.5%), and β-caryophyllene (5.0%) [53]. S. thymbra Carvacrol (57.1%), p-cymene (21.9%), thymol (8.0%), and γ-terpinene (4.4%) [29]. S. wiedemanniana Carvacrol (40%) and thymol (14%) [29].

The identified compounds in the essential oils of Satureja species are categorized in the monoterpene hydrocarbon, monoterpenoid, sesquiterpene hydrocarbon, sesquiterpenoid, and phenylpropanoid groups (see Table3). Indeed, the majority of recognized compounds are in the monoterpene group, with lower molecular weight than others, and only three compounds belong to other categories. There is sufficient evidence that the monoterpenes, especially monoterpenoids, have high pesticidal properties, and some novel and reliable outcomes in this field are shown in Table3. For example, the toxicity of thymol, as one Int. J. Environ. Res. Public Health 2021, 18,of x FOR main PEER components REVIEW in several species of the Satureja genus, was reported against9 of 18 the Int. J. Environ. Res. Public Health 2021, 18, x FOR PEER REVIEW 9 of 18 African cotton leafworm (Spodoptera littoralis Boisduval), the bed bugs (Cimex lectularius L.), the Colorado potato beetle (Leptinotarsa decemlineata Say), the granary weevil (Sitophilus Int. J. Environ. Res. Public Health 2021, 18granarius, x FOR PEER(L.)), REVIEW thegreen peach aphid (Myzus persicae (Sulzer)), and the root-knot9 nema-of 18 p-cymenetodep-cymene (Meloidogyne and and limonene limonene javanica with with borneol(Treub) borneol Chitwood)isis anotheanotherr consideration consideration [73,76,77]. already It already can be reported concluded reported by Pavela by from Pavela these Int. J. Environ. Res. Public Health 2021[83]., 18, [83]. x FOR PEER REVIEW 9 of 18 studies that the presence of higher total monoterpenoid content of essential oils had a positive correlation with their pesticidal activity [78–81]. Thus, the acaricidal, insecticidal, Table Table3. Characteristics 3. Characteristicsp-cymene and andpesticidal pesticidal limonene activities activities with of borneolof main main components components is anothe identifiedr identified consideration in in Satureja Satureja already species. species. reported by Pavela and nematicidal effects of Satureja essential oils may be related to the high amounts of Int. J. Environ. Res. Public Health 2021, 18[83]., x FOR PEER REVIEW Molecular 9 of 18 p-cymenecompounds and listedlimonene in Table with3. borneol It was also Molecularis anothe demonstratedr consideration that the already phenolic reported monoterpenoids by Pavela Classification Components Structure Formula Weight Pesticidal Activities Classification Components[83].such as thymolStructure with CH(CHFormula3)2 functional Weight group displayedPesticidal significantly Activities higher pesticidal Table 3. Characteristics and pesticidal activities of main components(g/mol) identified in Satureja species. effects compared to other terpenes, such(g/mol) as carvacrol and eugenol with CH3 and OCH3 Table 3. Characteristicsp-cymenefunctional and and pesticidal groups, limonene activities respectively with borneol of main [82 iscomponents,83 Molecularanothe]. However,r consideration identified the synergistic in Satureja already species. acaricidal, reported by insecticidal, Pavela [83]. Classification Componentsand nematicidalStructure effects ofFormula minor components Weight such The inhibition as α- andPesticidal ofβ -pinene,acetylcholine Activities camphor, esterase menthol, Monoterpene hy- Molecular p-Cymenesabinene, and thujene shouldC10H also14 be134.22(g/mol) considered Theand [inhibition84 insecticidal–87]. For of activity instance,acetylcholine on the the rice synergisticesterase MonoterpeneClassificationdrocarbon hy-Table 3.Components Characteristicsinsecticidal and pesticidalStructure action activities of terpenes Formulaof main that components haveWeight methyl identified functional in SaturejaPesticidal groups species. such Activities as p-cymene and p-Cymene C10H14 134.22 weeviland insecticidal (Sitophilus oryzae activity (L.)) on [87]. the rice drocarbon limonene with borneol is another consideration(g/mol) already reported by Pavela [83]. Molecular weevil (Sitophilus oryzae (L.)) [87]. Classification Components Structure Formula Weight The inhibitionPesticidal of acetylcholine Activities esterase Monoterpene hy-Table 3. Characteristics and pesticidal activities of main components identified in Satureja species. p-Cymene C10H14 (g/mol)134.22 Fumigantand insecticidal toxicity against activity the adults on the of rice drocarbon γ-Terpinene C10H16 136.23 The inhibition of acetylcholine esterase Monoterpene hy- Molecularthe houseflyweevil Weight ( (SitophilusMusca domestica oryzae L.) (L.)) [88]. [87]. Classificationp Components-Cymene StructureC Formula10H14 134.22 and insecticidalPesticidal activity Activitieson the rice (g/mol)Fumigant toxicity against the adults of drocarbon γ-Terpinene C10H16 136.23 the weevilhousefly (Sitophilus (Musca domesticaoryzae (L.)) L.) [87]. [88]. The inhibition ofThe acetylcholine inhibition of acetylcholine esterase MonoterpeneMonoterpene hy- Fumigant toxicityesterase against and the insecticidal adults of activity p-Cymenep-CymeneLimonene CC1010HCH1416H 134.22136.23 134.22and insecticidal activity on the rice drocarbonhydrocarbon 10 14 FumigantM. toxicity domesticaon the against [88]. rice weevil the (Sitophilusadults of γ-Terpinene C10H16 136.23 weevil (Sitophilus oryzae (L.)) [87]. Fumigantthe housefly toxicity (Musca against domestica (L.))the [adults87 L.)]. [88]. of Limonene C10H16 136.23 Fumigant toxicityFumigant against toxicity the against adults the of 10 16 γ-Terpineneγ-Terpinene C CH10H 16 136.23 136.23 M. domesticaadults of the [88]. housefly (Musca the housefly (Muscadomestica domesticaL.) [88 L.)]. [88]. The inhibition of acetylcholine esterase FumigantFumigant toxicity toxicityFumigant against against toxicity the the againstadults adults theof of LimoneneLimoneneα-Terpinene CC1010CH16H 136.23136.23 136.23and insecticidal activity on S. oryzae γ-Terpinene C10H1016 16 136.23 M. domesticaadults of M. [88]. domestica [88]. theFumigant housefly toxicity (Musca[87]. against domestica the L.) adults [88]. of Limonene C10H16 136.23 The inhibition of acetylcholine esterase M.The domestica inhibition [88]. of acetylcholine α-Terpineneα-Terpinene C10HC1016H 16 136.23 136.23and insecticidalesterase activity and insecticidal on S. oryzae activity on S. oryzae [87]. TheFumigant inhibition toxicity of acetylcholine[87]. against the esterase adults of Limonene C10H16 136.23 The inhibition of acetylcholine 10 16 The inhibition of acetylcholine esterase β-Myrceneβ-Myrcene C CH10H16 136.23 136.23and insecticidalM. domesticaesterase activity and on [88]. insecticidal S. oryzae activity α-Terpinene C10H16 136.23 and insecticidal activity on S. oryzae The inhibition[87]. of acetylcholine on S. oryzae [87 esterase]. FumigantThe inhibition and contact of acetylcholine[87]. toxicity, and esteraseac- α-Terpinene C10H16 136.23 and insecticidal activity on S. oryzae β-Myrcene C10H16 136.23 etylcholineand insecticidal esterase inhibitionactivity on activity S. oryzae β-Ocimene C10H16 136.23 [87]. againstThe inhibition the German of acetylcholinecockroach[87]. (Blattella esterase 10 16 α-Terpinene C H 136.23 FumigantTheand inhibition insecticidalgermanica and contactof (L)) activityacetylcholine [89]. toxicity, on S. oryzaeandesterase ac- β-Myrcene C10H16 136.23 and insecticidal[87]. activity on S. oryzae etylcholineThe inhibition esterase of acetylcholine inhibition activity esterase β-Ocimene C10H16 136.23 Strong fumigant toxicity[87]. against the Monoterpenoid β -MyrceneCarvacrol CC1010HH1416O 150.22136.23 againstand insecticidalthe German activity cockroach on S. (Blattella oryzae adults of M. domestica [90]. Fumigantgermanica and contact[87]. (L)) toxicity, [89]. and ac- Theetylcholine inhibition esterase of acetylcholine inhibition esterase activity β-Ocimene C10H16 136.23 Fumigant and contact toxicity, and ac- β-Myrcene C10H16 136.23 againstand insecticidal the German activity cockroach on S. oryzae(Blattella Strongetylcholine fumigant esterase[87]. toxicity inhibition against activity the Monoterpenoid Carvacrolβ-Ocimene C10CH1014HO16 150.22136.23 Larvicidalgermanica and pupicidal (L)) activity[89]. Piperitenone C10H14O 150.22 against the German cockroach (Blattella Fumigantagainstadults C.and quinquefasciatus of contact M. domestica toxicity, [91]. [90]. and ac- germanica (L)) [89]. etylcholine esterase inhibition activity β-Ocimene C10H16 136.23 Strong fumigant toxicity against the Monoterpenoid Carvacrol C10H14O 150.22 againstAntifeedant the Germanon the adult cockroach insects of ( BlattellaS. adults of M. domestica [90]. littoralisStrong, M. fumigantgermanica persicae, and toxicity(L)) L. [89].decemline- against the Monoterpenoid Carvacrol C10H14O 150.22 Larvicidal and pupicidal activity Piperitenone C10H14O 150.22 Thymol C10H14O 150.22 ata, andagainst adultstoxicity C. of quinquefasciatusagainst M. domestica second-stage [90]. [91]. juveniles of the phytopathogenic nem-

Strongatode fumigant M. javanica toxicity [73]. against the Monoterpenoid Carvacrol C10H14O 150.22 Larvicidal and pupicidal activity Piperitenone C10H14O 150.22 Antifeedantadults of on M. the domestica adult insects [90]. of S. against C. quinquefasciatus [91]. littoralisLarvicidal, M. persicae, and pupicidal and L. decemline- activity Piperitenone C10H14O 150.22 Thymol C10H14O 150.22 ata, andagainst toxicity C. quinquefasciatus against second-stage [91]. juvenilesAntifeedant of the on phytopathogenic the adult insects nem- of S. Larvicidal and pupicidal activity Piperitenone C10H14O 150.22 littoralisatode, M. persicae, M. javanica and [73].L. decemline- Antifeedantagainst C. quinquefasciatuson the adult insects [91]. of S. Thymol C10H14O 150.22 ata, and toxicity against second-stage littoralis, M. persicae, and L. decemline- juveniles of the phytopathogenic nem- Thymol C10H14O 150.22 ata, and toxicity against second-stage Antifeedantatode on M. the javanica adult insects [73]. of S. juveniles of the phytopathogenic nem- littoralis, M. persicae, and L. decemline- atode M. javanica [73]. Thymol C10H14O 150.22 ata, and toxicity against second-stage juveniles of the phytopathogenic nem-

atode M. javanica [73].

Int. J. Environ. Res. Public Health 2021, 18, x FOR PEER REVIEW 9 of 18

Int. J. Environ. Res. Public Health 2021, 18, x FOR PEER REVIEW 9 of 18 p-cymene and limonene with borneol is another consideration already reported by Pavela p[83].-cymene and limonene with borneol is another consideration already reported by Pavela [83]. Table 3. Characteristicsp-cymene and and pesticidal limonene activities with of borneol main components is another identifiedconsideration in Satureja already species. reported by Pavela Int. J. Environ. Res. Public Health 2021[83]., 18, x FOR PEER REVIEW 9 of 18 Table 3. Characteristics and pesticidal activities of main components identified in Satureja species. Molecular ClassificationTable Components 3. Characteristics andStructure pesticidal activitiesFormula of main componentsMolecularWeight identified inPesticidal Satureja species. Activities Classification Componentsp-cymene Structureand limonene withFormula borneol is anotheWeight(g/mol)r consideration alreadyPesticidal reported Activities by Pavela Molecular [83]. (g/mol) Classification Components Structure Formula Weight Pesticidal Activities Table 3. Characteristics and pesticidal activities of main components(g/mol) identified The in inhibition Satureja species. of acetylcholine esterase Monoterpene hy- p-Cymene C10H14 Molecular134.22 Theand inhibition insecticidal of acetylcholine activity on the esterase rice Monoterpenedrocarbon hy- Classification p-CymeneComponents Structure FormulaC10H14 Weight134.22 andweevilPesticidal insecticidal (Sitophilus Activities activity oryzae on (L.)) the [87]. rice drocarbon The inhibition of acetylcholine esterase Monoterpene hy- (g/mol) weevil (Sitophilus oryzae (L.)) [87]. p-Cymene C10H14 134.22 and insecticidal activity on the rice drocarbon weevil (Sitophilus oryzae (L.)) [87]. The Fumigantinhibition oftoxicity acetylcholine against esterase the adults of Monoterpene hy-γ-Terpinene C10H16 136.23 p-Cymene C10H14 134.22 and insecticidal activity on the rice drocarbon Fumigantthe housefly toxicity (Musca against domestica the adults L.) [88]. of γ-Terpinene C10H16 136.23 weevil (Sitophilus oryzae (L.)) [87]. the housefly (Musca domestica L.) [88]. Fumigant toxicity against the adults of γ-Terpinene C10H16 136.23 Fumigantthe housefly toxicity (Musca against domestica the adults L.) [88]. of Limonene C10H16 136.23 FumigantFumigant toxicity toxicityM. against domestica against the adults[88]. the adultsof of Limoneneγ-Terpinene CC1010HH16 16 136.23136.23 the housefly (MuscaM. domestica domestica [88]. L.) [88]. Fumigant toxicity against the adults of Limonene C10H16 136.23 M. domestica [88]. Fumigant toxicity against the adults of Limonene C10H16 136.23 The inhibition of acetylcholine esterase M. domestica [88]. α-Terpinene C10H16 136.23 Theand inhibition insecticidal of acetylcholine activity on S. esterase oryzae α-Terpinene C10H16 136.23 and insecticidal [87].activity on S. oryzae The inhibition of acetylcholine esterase [87]. α-Terpinene C10H16 136.23 and insecticidal activity on S. oryzae The inhibition of acetylcholine esterase [87]. Int. J. Environ. Res. Public Healthα-Terpinene2021, 18, 6050 C10H16 136.23 andThe insecticidal inhibition activity of acetylcholine on S. oryzae esterase8 of 16 β-Myrcene C10H16 136.23 Theand inhibition insecticidal[87]. of acetylcholine activity on S. esterase oryzae β-Myrcene C10H16 136.23 and insecticidal [87].activity on S. oryzae The inhibition of acetylcholine esterase Table 3. Cont. Fumigant and contact[87]. toxicity, and ac- β-Myrcene C10H16 136.23The inhibitionand insecticidal of acetylcholine activity esterase on S. oryzae β-Myrcene C10H16 136.23 andFumigantetylcholine insecticidal and esterase activity contact on inhibition toxicity,S. oryzae activityand ac- β-Ocimene C10H16 136.23Molecular Weight [87]. Classiﬁcation Components Structure Formula Pesticidal Activities (g/mol)againstetylcholine the Germanesterase[87]. cockroachinhibition activity(Blattella β-Ocimene C10H16 136.23 Fumigant and contact toxicity, and ac- Fumigantagainst and the contactgermanica German toxicity, cockroach(L)) [89].and ac- (Blattella Int. J. Environ. Res. Public Health 2021, 18, x FOR PEER REVIEW etylcholine esteraseFumigant inhibition and contact activity toxicity,10 of 18 β-Ocimene C10H16 136.23 etylcholine esterasegermanica andinhibition acetylcholine (L)) [89].activity esterase β-Ocimene C10H16 136.23 against the German cockroach (Blattella β-Ocimene C10H16 against136.23 the Germaninhibition cockroach activity (Blattella against the Strong fumigantgermanicaGerman toxicity (L)) cockroach [89]. against (Blattella the Int.Monoterpenoid J. Environ. Res. Public HealthCarvacrol 2021, 18 , x FOR PEER REVIEW C10H14O 150.22 germanica (L)) [89]. 10 of 18 Int. J. Environ. Res. Public Health 2021, 18, x FOR PEER REVIEW germanica (L)) [8910]. of 18 Strongadults fumigant of M. toxicity domestica against [90]. the Int.Monoterpenoid J. Environ. Res. Public HealthCarvacrol 2021, 18 , x FOR PEER REVIEW C10H14O 150.22 10 of 18 adults of M. domestica [90]. Int. J. Environ. Res. Public Health 2021, 18, x FOR PEER REVIEW StrongStrongStrong fumigant fumigantfumigant toxicity toxicitytoxicity against againstagainst the 10 thethe of 18 1010 1614 Strong fumigant toxicity against MonoterpenoidMonoterpenoidMonoterpenoid PulegoneCarvacrol CarvacrolCarvacrol CCC10HCHH1410OHO 14OO 150.22152.23150.22 150.22 Int. J. Environ. Res. Public Health 2021, 18, x FOR PEER REVIEW adultsadultsadults of M. of ofthedomestica M.M. adults domesticadomestica of[90].M. domestica [90].[90]. 10 [ 90of]. 18

StrongLarvicidal fumigant and toxicitypupicidal against activity the PiperitenonePulegone CC1010HH1614OO 152.23150.22 Strong fumigant toxicity against the Pulegone C10H16O 152.23 Larvicidalagainstadults C.of and quinquefasciatusM. pupicidaldomestica [90].activity [91]. Int. J. Environ. Res. PublicPiperitenone Health 2021, 18, x FOR PEER REVIEW C10H14O 150.22 Strongadults fumigant ofLarvicidal M. domestica toxicity and pupicidal against[90]. activity10 the of 18 PulegonePiperitenone C10CH1016HO14 O152.23 150.22 LarvicidalLarvicidalagainstadults and C. of pupicidal againstand quinquefasciatus M. pupicidaldomesticaC. quinquefasciatusactivity [90].activity [91]. [ 91 ]. Int. J. Environ.Int. J. Environ. Res. Public Res. PublicHealthGeranialPiperitenone Health 2021 ,2021 18 , ,x 18 FOR , x FOR PEER PEER REVIEW REVIEW CC1010HH14O16O 150.22152.23 StrongLarvicidal fumigant and pupicidaltoxicity10 against ofactivity 18 10 the of 18 PiperitenonePulegone C10H1614O 152.23150.22 againstAntifeedantagainst C. quinquefasciatus C. on quinquefasciatus the adult [91]. insects [91]. of S. Strongagainstadults fumigant C. Antifeedantof quinquefasciatus M. toxicity domestica on the against adult[90]. [91]. insects the Int. J. Environ. Res. Public HealthPulegone 2021, 18 , x FOR PEER REVIEW C10H16O 152.23 littoralis, M. persicae, and L. decemline-10 of 18 AntifeedantLarvicidalLarvicidaladults and ofofonand S.M. pupicidalthe littoralispupicidal domestica adult, M. insectsactivity persicae, activity[90]. ofand S.L. GeranialGeranial CC1010HH1616OO 152.23 Thymol C10H14O 150.22 Antifeedantlittoralisata, and , on toxicityM. the decemlineatapersicae, adult against insects and, and second-stageL. toxicityof decemline- S. against Thymol C10H14O 150.22Larvicidalagainstagainst C. C. quinquefasciatusand quinquefasciatus pupicidal activity[91]. [91]. littoralisAntifeedantStrong, M. persicae,fumigant onsecond-stage and the toxicity L. adult decemline- juveniles insectsagainst of of the S. 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Strongjavanicaand synergistic fumigant [73]. toxicity effect against on PulegonePulegone C10CH16HO O152.23 152.23Acutejuvenilesagainst toxicity of C. the andquinquefasciatus phytopathogenic synergistic effect[91]. nem- on BorneolBorneol CC1010HH101818OO16 154.25 adults ofthe M. adults domestica of M. domestica [90]. [90]. thethe C. C. quinquefasciatus quinquefasciatusatode M. javanica larvae larvae [73]. [86]. [86]. AcuteLarvicidalFumigantLarvicidal toxicity and and pupicidal and contact pupicidalsynergistic activity toxicity, activity effect and on Borneol C10H1618O 154.25 GeranialGeranial CC10HH16OO 152.23152.23 Geraniol C10H18O 154.25 AcuteneurophysiologicalagainsttheLarvicidalagainst C. toxicity C. quinquefasciatus quinquefasciatus C. and quinquefasciatusand pupicidal synergistic impacts [91]. larvae activityagainst effect[91]. [86]. C.on GeranialBorneol CC1010HH1618OO 152.23154.25 Larvicidal and pupicidal activity Geranial C10H16O 152.23Fumigant andlectularius contact [77].toxicity, and AcuteFumigantLarvicidaltheagainst toxicityC. quinquefasciatus C.and againstand quinquefasciatusand contact pupicidal synergisticC. quinquefasciatus toxicity, larvae activity effect[91]. [86].and[ 91 on ]. BorneolGeraniol CC1010HH1818O 154.25 neurophysiological impacts against C. Geranial C10H1816O 152.23 Geraniol C H O 154.25 neurophysiologicalFumiganttheagainst C. quinquefasciatus C.and quinquefasciatus contact impacts toxicity, larvae against [91]. [86]. and C. AcuteThe toxicity inhibition andlectularius synergistic of acetylcholine [77]. effect on esterase Borneol C10H1818O 154.25 lectularius [77]. GeraniolLinalool CC10HH18OO 154.25154.25 neurophysiologicalAcuteandFumigant insecticidal toxicity andAcute and contact activity toxicitysynergistic impacts toxicity, andon against synergisticS. effect oryzae and C.on 10 18 the C. quinquefasciatus larvae [86]. BorneolBorneol C CH10HO18O 154.25 The 154.25 inhibition ofeffect acetylcholine on the C. quinquefasciatus esterase 10 18 the C. quinquefasciatuslectularius [77]. larvae [86]. Geraniol C H O 154.25 TheAcuteneurophysiologicalFumigant inhibition toxicity and ofand contactacetylcholine[87]. synergistic impactslarvae toxicity, [86 against]. effectesterase and on C. BorneolLinalool CC1010HH1818O 154.25 and insecticidal activity on S. oryzae LinaloolGeraniol CC1010HH1818OO 154.25154.25 neurophysiologicalandthe insecticidal C. quinquefasciatuslectularius activity impacts [77]. larvae on againstS. oryzae [86]. C. FumigantTheAcute inhibition toxicity and contact andof[87]. acetylcholine synergistictoxicity, and effectesterase on Borneol C10H18O 154.25 Fumigant and contact toxicity, Geraniol C10H18O 154.25 neurophysiologicalThethe inhibition C. quinquefasciatuslectularius ofimpacts [87].acetylcholine [77].against larvae C. esterase[86]. LinaloolGeraniol C10CH1018HO18 O154.25 154.25TheandFumigant inhibition insecticidal andand of neurophysiological contactactivityacetylcholine toxicity, on S. oryzaeesterase impacts and 10 18 against C. lectularius [77]. Terpinene-4-ol C 10H 18O 154.25 and insecticidallectularius [77]. activity on S. oryzae GeraniolLinalool C10H18O 154.25 TheTheneurophysiologicalFumigantand inhibition inhibition insecticidal and of of acetylcholine contact [87].acetylcholine activity impacts toxicity, on esterase againstS. esterase oryzae and C. The inhibitionThe of acetylcholine inhibition[87]. of acetylcholine esterase Terpinene-4-olGeraniolLinalool CC1010HH1818O 154.25 Theneurophysiological andinhibitionand insecticidal insecticidal of lectulariusacetylcholine activity [87].activity impacts [77]. on esterase on S. againstS.oryzae oryzae C. Linalool C10H18O 154.25Fumigant andesterase contact and insecticidal toxicity, activityand Terpinene-4-olLinalool C10H1818OO 154.25154.25 andTheand insecticidal inhibition insecticidallectularius activity of[87]. acetylcholine activity on [77].S. oryzae on S. esteraseoryzae Geraniol C10H18O 154.25 neurophysiological[87].on impacts S. oryzae against[87]. C. The inhibition[87]. of [87]. acetylcholine esterase Terpinene-4-ol C10H18O 154.25 TheandFumigant inhibition insecticidal toxicitylectularius of activityacetylcholine on [77]. the on adults S. oryzaeesterase of S. α-TerpineolLinalool CC1010HH1818OO 154.25154.25 Theand inhibition insecticidalThe of inhibitionacetylcholine activity of on acetylcholine S. esterase oryzae 10 18 Fumigant toxicitygranarius[87]. on the [76]. adults of S. Terpinene-4-olTerpinene-4-ol C CH10H18OO 154.25 154.25Theand inhibition insecticidalesterase of acetylcholine activity and insecticidal on S. esterase oryzae activity Linaloolα-Terpineol CC1010HH1818O 154.25 TheThe inhibitionand inhibition insecticidal of acetylcholine of acetylcholine [87].activity esterase on S. esteraseoryzae Terpinene-4-ol C10H18O 154.25 Fumigantand insecticidal granariustoxicity [87].activity on [76].S. the oryzae onadults [S.87 ].oryzae of S. α-TerpineolTerpinene-4-ol C10H1818OO 154.25154.25 and insecticidal activity[87]. on S. oryzae Linalool C10H18O 154.25 and insecticidalgranarius activity [76]. on S. oryzae Fumigant toxicityFumigant[87]. [87]. on toxicity the adults on the adultsof S. of Piperitenoneα-Terpineolα-Terpineol C10CH18HO O154.25 154.25TheLarvicidal inhibition activity of [87].acetylcholine against C. pipiensesterase C10H1014O182 166.22 granariusS. granarius[76]. [76]. Terpinene-4-olPiperitenoneoxide C10H18O 154.25 TheLarvicidalFumigantand inhibition insecticidal activity toxicity of acetylcholine[92]. activityagainst on the C.on adults pipiens S. esterase oryzae of S. α-Terpineol C10H18O 154.25 C10H14O2 166.22 Fumigant toxicity on the adults of S. Terpinene-4-oloxide C10H18O 154.25 Fumigantand insecticidal toxicitygranarius[92]. [87].activity on [76].the on adults S. oryzae of S. Piperitenoneα-TerpineolPiperitenoneα-Terpineol C1010HH1818OO 154.25154.25 TheLarvicidal inhibition activity Larvicidalof acetylcholine against activity C. against pipiensesteraseC. C10CH14HO2O 166.22 166.22 granarius [76]. oxide 10 14 2 granarius[87].pipiens [76]. [ 92]. Terpinene-4-olPiperitenoneoxide C10H18O 154.25 Larvicidaland insecticidal activity[92]. activity against on C. S. pipiens oryzae C10H14O2 166.22 Fumigant toxicity on the adults of S. Geranyloxide acetate C12H20O2 196.29 Fumigant toxicity[92].[87]. on the adults of S. Piperitenoneα-Terpineol C10H18O 154.25 FumigantLarvicidal toxicity granariusactivity on againstthe [76]. adults C. ofpipiens S. GeranylPiperitenone acetate C1210H2014OO22 196.29166.22 Larvicidal activityFumigantgranarius against toxicity C.[76]. pipiens on the adults of PiperitenoneGeranyloxide acetate C10CH1214HO202 O2 166.22 196.29FumigantLarvicidal toxicity activity[92]. on against the adults C. pipiens of S. α-Terpineoloxide C10H18O 154.25 granarius[92]. S. [76]. granarius [76]. C10H14O2 166.22 Fumigant toxicitygranarius on [76].the adults of S. Geranyloxide acetate C12H20O2 196.29 Fumigant toxicity[92]. on the adults of S. 10 18 granarius [76]. α-Terpineol C H O 154.25 TheFumigant inhibition toxicity of acetylcholine on the adults esterase of S. Geranyl acetate C12H20O2 196.29 granarius [76]. Sesquiterpene hy- Piperitenoneβ-Caryo- TheLarvicidal inhibition activity ofThe acetylcholine inhibition against of acetylcholine C.esterase pipiens Sesquiterpene 1015 1424 2 granarius [76]. Sesquiterpene hy- β-Caryophylleneβ-Caryo- CC HCH15HO 24 204.35166.22 Fumigant204.35Fumigantand insecticidal toxicity toxicityesterase on the activity andon adults the insecticidal on ofadults S.S. oryzae activity of S. drocarbonhydrocarbon GeranylPiperitenonephylleneGeranyloxide acetate acetate CC12C12H15H20H20O24O2 2 196.29204.35196.29 andLarvicidal insecticidal activity activity[92]. against on S. C. oryzae pipiens C10H14O2 166.22 Fumigantgranarius toxicitygranarius [76].[87]. onon S. [76].the oryzae adults [87]. of S. drocarbon phyllene The inhibition of acetylcholine esterase Sesquiterpene hy- GeranylPiperitenoneβ-Caryo-oxide acetate C12H20O2 196.29 Larvicidal activity[87].[92]. against C. pipiens C15H24 204.35 and insecticidalgranarius activity [76]. on S. oryzae drocarbon phyllene C10H14O2 166.22 The inhibition of acetylcholine esterase Sesquiterpene hy- β-Caryo-oxide The inhibition of acetylcholine[87].[92]. esterase Sesquiterpene hy- β-Caryo- C15H24 204.35 The andFumigant Insecticidal inhibition insecticidal toxicity effects of activityacetylcholine on against the on adults theS. oryzaeesterase larvae of S. Sesquiterpenedrocarbon hy- GeranylCaryophyllenephylleneβ-Caryo- acetate CC1215HH2024 O2 204.35196.29 and Insecticidal insecticidal effects activity against on S. oryzae the larvae Sesquiterpenoiddrocarbon Caryophyllenephyllene CC1515HH2424O 220.35204.35 TheandFumigantand inhibition pupae insecticidal toxicityofgranarius fallof [87].acetylcholine activityarmyworm on [76].the onadults S. ( Spodop-esterase oryzae of S. 1215 2024 2 [87]. SesquiterpeneSesquiterpenoiddrocarbon hy- Geranyl βphyllene-Caryo-oxide acetate CC HH OO 220.35196.29 and pupae of fall armyworm (Spodop- oxide 15 24 tera frugiperdagranarius (Smith)) [76]. [93]. C H 204.35 Fumigant Insecticidalandtera insecticidal frugiperda toxicity effects [87]. activity(Smith)) on against the on adults[93]. the S. oryzaelarvae of S. drocarbon GeranylCaryophyllenephyllene acetate C12H20O2 196.29 Sesquiterpenoid C15H24O 220.35 and pupae ofgranarius fall[87]. armyworm [76]. (Spodop- oxide InsecticidalThe Insecticidal inhibition effects effects ofagainst acetylcholine against the larvae the esteraselarvae Sesquiterpene hy-CaryophylleneβCaryophyllene-Caryo- tera frugiperda (Smith)) [93]. SesquiterpenoidSesquiterpenoid CCC15H1524H24OO24 220.35220.35204.35 andTheand pupaeand Insecticidal inhibitionpupae insecticidal of fall of armyworm effects fallof acetylcholine armywormactivity against (Spodop- on the S.( Spodop-esterase oryzae larvae Sesquiterpenedrocarbon hy- Caryophylleneβphyllene-Caryo-oxideoxide Sesquiterpenoid CC1515HH2424O 204.35220.35 andand Insecticidaltera pupaeterainsecticidalfrugiperda frugiperda of effects fall(Smith)) [87].activity armyworm (Smith)) against [93]. on the [93].S. ( Spodop-oryzae larvae drocarbon Caryophyllenephylleneoxide The inhibition of acetylcholine esterase Sesquiterpene hy- β-Caryo- [87]. Sesquiterpenoid CC1515HH2424O 204.35220.35 andand pupae insecticidaltera frugiperda of fall activity armyworm (Smith)) on S.[93]. ( Spodop-oryzae oxide drocarbon phyllene tera frugiperda (Smith)) [93]. Insecticidal effects[87]. against the larvae Caryophyllene Sesquiterpenoid C15H24O 220.35 and Insecticidal pupae of effects fall armyworm against the (Spodop- larvae Caryophylleneoxide Sesquiterpenoid C15H24O 220.35 and pupaetera frugiperda of fall armyworm (Smith)) [93]. (Spodop- oxide Insecticidal effects against the larvae Caryophyllene tera frugiperda (Smith)) [93]. Sesquiterpenoid C15H24O 220.35 and pupae of fall armyworm (Spodop- oxide tera frugiperda (Smith)) [93].

Int. J. Environ. Res. Public Health 2021, 18, x FOR PEER REVIEW 10 of 18

Strong fumigant toxicity against the Pulegone C10H16O 152.23 adults of M. domestica [90].

Larvicidal and pupicidal activity Geranial C10H16O 152.23 against C. quinquefasciatus [91].

Acute toxicity and synergistic effect on Borneol C10H18O 154.25 the C. quinquefasciatus larvae [86].

Fumigant and contact toxicity, and Geraniol C10H18O 154.25 neurophysiological impacts against C. lectularius [77].

The inhibition of acetylcholine esterase Linalool C10H18O 154.25 and insecticidal activity on S. oryzae [87].

The inhibition of acetylcholine esterase Terpinene-4-ol C10H18O 154.25 and insecticidal activity on S. oryzae [87].

Fumigant toxicity on the adults of S. α-Terpineol C10H18O 154.25 granarius [76].

Piperitenone Larvicidal activity against C. pipiens C10H14O2 166.22 oxide [92].

Fumigant toxicity on the adults of S. Geranyl acetate C12H20O2 196.29 granarius [76]. Int. J. Environ. Res. Public Health 2021, 18, 6050 9 of 16

The inhibition of acetylcholine esterase Sesquiterpene hy- β-Caryo- TableC15 3.HCont.24 204.35 and insecticidal activity on S. oryzae drocarbon phyllene [87]. Molecular Weight Int. J. Environ.Classiﬁcation Res. Public Health Components 2021, 18, x FOR PEER Structure REVIEW Formula Pesticidal Activities11 of 18 (g/mol)

Insecticidal effectsInsecticidal against effects the against larvae the CaryophylleneCaryophyllene larvae and pupae of fall SesquiterpenoidSesquiterpenoid C15CH24HO O220.35 220.35and pupae of fall armyworm (Spodop- oxideoxide 15 24 armyworm (Spodoptera frugiperda tera frugiperda (Smith)) [93]. (Smith)) [93]. Fumigant andFumigant contact and toxicity, contact toxicity, and and acetylcholine esterase PhenylpropanoidPhenylpropanoid Estragole Estragole C10CH12HO O148.20 148.20acetylcholine esterase inhibition 10 12 inhibition activity against activity against B. germanicagermanica[89 ].[89].

4. Modes of Action of Essential Oils and Their Components 4. ModesThe of acetylcholinesterase Action of Essential (AChE) Oils and is actively Their Components involved in metabolic conversion of ‘acetylcholine’ in the synaptic cleft of arthropods and has two catalytic and peripheral target The acetylcholinesterase (AChE) is actively involved in metabolic conversion of ‘ac- sites. The insect-speciﬁc cysteine residue positioned at the acetylcholinesterase active site etylcholine’is a proposed in the target synaptic site for cleft developing of arthropo insecticidesds and has totwo reduce catalytic off-target and peripheral toxicity [ 94target]. On

sites.the The other insect-specific hand, inhibition cysteine of pest-specific residue positi acetylcholinesteraseoned at the acetylcholinesterase will decrease active the risk site of is utilizeda proposed pesticides targeton site non-target for developing organisms, insectic suchides as to mammals reduce off-target [94]. Some toxicity essential [94]. oils On and thecompounds other hand, are inhibition reported toof bindpest-specific with these ac targetetylcholinesterase sites to inhibit will the decrease AChE action the risk [95– of97 ]. utilizedPark et pesticides al. [26] revealed on non-target that the essentialorganisms, oil ofsuchS. montanaas mammalshad significant [94]. Some AChE essential inhibitory oils andactivity compounds against theare fruitreported fly (Drosophila to bind with suzukii thes(Matsumura)),e target sites to along inhibit with the high AChE toxicity. action The [95–97].inhibition Park of et AChE al. [26] leads revealed to acetylcholine that the essential accumulation, oil of S. hyperactivity, montana had paralysis, significant and AChE death inhibitoryof the pest. activity Along against with terpenes, the fruit the flywell-known (Drosophila suzukii phenylpropane (Matsumura)), estragole along has with also shownhigh toxicity.AChE inhibitoryThe inhibition effects of AChE [98,99 ].leads It should to acetylcholine be noted that accumulation, the AChE inhibition hyperactivity, can occur paral- in ysis,both and contact death and of the fumigation pest. Along methods with terp of usedenes, essential the well-known oils [100, 101phenylpropane]. Octopamine, estragole as a neu- hasrotransmitter, also shown neuromodulator,AChE inhibitory effects and hormone, [98,99]. isIt should one of thebe importantnoted that biogenicthe AChE amines inhibi- in tioninvertebrates can occur andin both is released contact at and times fumigation of high energy methods demands of used [102 essential]. Octopamine oils [100,101]. receptor Octopamine,alteration is consideredas a neurotransmi as anothertter, mode neuromodulator, of action of essential and hormone, oils or their is componentsone of the [im-103]. portantThe blockage biogenic of amines gamma-amino in invertebrates butyric acidand is (GABA) released and at times nicotinic of high acetylcholine energy demands (nAChR) [102].receptors Octopamine has also receptor been documented alteration is in cons someidered studies as another [97,104]. mode of action of essential oils or Besidetheir components the neurotoxic [103]. modes The blockage of pesticidal of gamma-amino action of essential butyric oils acid and (GABA) compounds, and nicotinicthere are acetylcholine several studies (nAChR) indicating receptors enzymatic has andalso non-enzymatic been documented effects. in Thesome destructive studies [97,104].effects of essential oils and their compounds on esterases and glutathione S-transferases (GSTs)Beside as imperativethe neurotoxic detoxifying modes of enzymes pesticidal in arthropodaction of essential pests are oils reported and compounds, [88,105,106 ]. thereDisruption are several of thestudies function indicating of detoxifying enzymatic enzymes and non-enzymatic may reduce effects. the probability The destructive of pest effectsresistance of essential [107], and oils thisand has their been compounds clearly depicted on esterases by essential and glutathione oils and their S-transferases components. (GSTs)Farahani as imperative et al. [27] showed detoxifying that theenzymes essential in arthropod oil of S. khuzestanica pests are reportedhad adverse [88,105,106]. effects on Disruptioncytochrome of the P450 function monooxygenases of detoxifying (P450, enzymes responsible may reduce for the the oxidative probability metabolism of pest re- of a sistancevariety [107], of xenobiotics and this has and been endogenous clearly dep compounds)icted by essential function oils of twoandspotted their components. spider mites Farahani(Tetranychus et al. urticae[27] showedKoch), that along the with essential toxic andoil of repellent S. khuzestanica activities. had The adverse adverse effects effects on of cytochromethese agents P450 on digestivemonooxygenases enzymes (P450, such as resp lipases,onsible proteases, for the oxidativeα-amylases, metabolismα-glucosidases, of a varietyand β -glucosidasesof xenobiotics wereand endogenous also reported compou [106], whichnds) function can be veryof two effective spotted in spider reducing mites the (Tetranychusnutritional urticae efficiency Koch), of pests.along Effectswith toxic on energyand repellent reservoirs activities. of the The pest adverse by decreasing effects of the theseprotein, agents glucose, on digestive and triglyceride enzymes contentssuch as lipases, and disrupting proteases, the α action-amylases, of immunological α-glucosidases, and andhematological β-glucosidases parameters were also are reported the other [106], reasons whic toh approve can be very the multiple effective modes in reducing of action the of nutritionalthese eco-friendly efficiency bio-pesticides of pests. Effects [108 on,109 energy]. reservoirs of the pest by decreasing the protein, glucose, and triglyceride contents and disrupting the action of immunological 5. Proposed New Formulations for Greenhouse and Field Applications and hematological parameters are the other reasons to approve the multiple modes of action Althoughof these eco-friendly great potential bio-pesticides for acaricidal, [108,109]. insecticidal, and nematicidal activity of Sat- ureja essential oils and compounds have been reported, limitations such as susceptibility to 5.light, Proposed moisture, New oxygen,Formulations and temperature for Greenhouse may and restrict Field their Applications application in the pest management strategies [5]. Indeed, the use of essential oils and their components in non-crop Although great potential for acaricidal, insecticidal, and nematicidal activity of agriculture in the management of stored product pests, flies, and cockroaches is effec- Satureja essential oils and compounds have been reported, limitations such as susceptibility to light, moisture, oxygen, and temperature may restrict their application in the pest management strategies [5]. Indeed, the use of essential oils and their components in non- crop agriculture in the management of stored product pests, flies, and cockroaches is effective [110]. Additionally, the larvicidal activity of essential oils by treating standing wa-

Int. J. Environ. Res. Public Health 2021, 18, 6050 10 of 16

tive [110]. Additionally, the larvicidal activity of essential oils by treating standing water and waterways and their repellent effects on adults may be useful in mosquito management (See Tables1 and3 for examples). Due to the disadvantage of low persistence in environmental conditions, the application of essential oils in crop agriculture can be limited [6]. Soft body and sucking pests (viz., aphids, thrips, and mites) are usually controlled by essential oils on crops, particularly under low pest pressure [110]. For example, Western flower thrip and green peach aphid were successfully controlled by the essential oil-based insecticide Ectrol (EcotecTM, California, USA) on lettuce and strawberry. However, partial efficiency was achieved against larger chewing insect pests, such as coleopterans and lepidopterans [110]. Nanoencapsulation based on the controlled release technique has been offered to overcome the lack of persistence restriction of bio-pesticides [111]. In the nanoencapsulation process, the active agent as a solid, liquid, or gas is surrounded by a thin layer of natural or synthesized polymer or a membrane to keep the core active agent from harmful environmental factors [112]. Generally, reducing the amount of active ingredients and minimizing evaporation and its controlled release are main advantages of nanoencapsulation [111]. However, along with above-mentioned advantages, expensive and difficult processes of the creation of nano-formulations should be considered. In the study of Ahmadi et al. [65], encapsulation of S. hortensis essential oil in chitosan-tripolyphosphate nanoparticles improved its ovicidal and adulticidal toxicity against T. urticae. Along with high toxicity, nanoencapsulation of S. hortensis essential oil in chitosan-tripolyphosphate nanoparticles enhanced its persistence so that 80% and 15% mortality was achieved for nano-encapsulated and pure essential oil formulation after 14 days. Usha Rani et al. [113] evaluated the antifeedant activity of pure and silica nanoparticles-based capsulated α-pinene and linalool against the tobacco cutworm (Spodoptera litura F.) and the castor semi-looper (Achaea janata L.). Although both terpenes had significant antifeedant effects, nano-capsule formulation augmented their effectiveness up to 10 and 25 times for A. Janata and S. litura, respectively. The same results regarding the enhancing toxicity and persistence of other essential oils by encapsulation in polymeric and non-polymeric materials, such as poly(ethylene gly- col), myristic acid-chitosan, and mesoporous material, were also documented [114–116]. The preparation of nano-emulsions is another applicable method to solve the solubility restriction of essential oils in water and is more effective with minute quantities of toxic substances, both in medicinal and agricultural pest management prospects [117,118]. Fur- ther, the combination of essential oils with other protectants such as microbial agents may enhance their effectiveness. For example, the combination of S. sahendica essential oil with entomopathogenic fungus Beauveria bassiana augmented its toxicity against cowpea weevil, and insect pest mortality increased from 50% after a 1-day exposure time to 80% after 7 days [28].

6. Conclusions Along with antibacterial, antifungal, antiviral, and general importance in medicinal, food, and cosmetic industries [119–121], the essential oils isolated from different species of Satureja genus could have great potential in the management of detrimental mite and tick Acari, insects, and nematodes. Pesticidal effects of Satureja species essential oils, which may be commonly related to their main terpenes [67,83,86], were reported as lethal contact and fumigant toxicity to sublethal repellent action, developmental inhibitory effects, adverse effects on the feeding, life cycle, oviposition, and egg hatching, and biochemical disturbances, such as reduction in general esterase content and inhibition of acetylcholinesterase and cytochrome P450 monooxygenases functions (see Tables1 and3 ). Such multiple modes of action of essential oils and their compounds, in addition to reducing pest resistance, can affect a wide range of pests [5,9]. Despite all of the mentioned advantages, high volatility or lack of persistence and insolubility in water are the main restrictions in the commercialization and extensive application of these compounds [110]. Accordingly, their application is principally focused against indoor non-crop pests such as storage pests, ﬂies, Int. J. Environ. Res. Public Health 2021, 18, 6050 11 of 16

and cockroaches [96,114]. Further, the acute toxicity against larvae and repellent activity on the adults of mosquitos that carry pathogens and suck blood were also documented in Tables1 and3 . However, with micro- and nano-encapsulation on the basis of controlled release techniques, their persistence can be increased [122]. Although nano-emulsiﬁcation is also a suitable way to dissolve essential oils in water [123,124], it is possible to in- crease their effectiveness by combined application with microbial control agents, such as entomopathogenic fungi [28]. These less-toxic substances may help in agriculture and environmental protection and can be proposed to countries that apply extreme amounts of synthetic pesticides. However, effects on beneﬁcial and non-target organisms, residues on food products, and more importantly, considering a method for lower cost of Satureja essential oils and their components, should also be investigated in future research.

Author Contributions: Conceptualization, A.E.; methodology, A.E.; investigation, A.E., J.J.S., and M.Z.; resources, A.E., J.J.S., and M.Z.; writing—original draft preparation, A.E. and P.K.; writing— review and editing, A.E., J.J.S., M.Z., and P.K. All authors have read and agreed to the published version of the manuscript. Funding: This research received no external funding. Institutional Review Board Statement: Not applicable. Informed Consent Statement: Not applicable. Acknowledgments: This study received financial support from the University of Mohaghegh Ard- abili, which is greatly appreciated. The publication of this review was financially supported by Chiang Mai University, Thailand. Conflicts of Interest: The authors declare no conflict of interest.

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