Next Article in Journal
Effects of Exogenous Salicylic Acid on Drought Response and Characterization of Dehydrins in Impatiens walleriana
Next Article in Special Issue
First Detection of Meloidogyne luci (Nematoda: Meloidogynidae) Parasitizing Potato in the Azores, Portugal
Previous Article in Journal
Managing an Invasive Weed Species, Parthenium hysterophorus, with Suppressive Plant Species in Australian Grasslands
Previous Article in Special Issue
The Genus Pratylenchus (Nematoda: Pratylenchidae) in Israel: From Taxonomy to Control Practices
 
 
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Nematicidal Activity of Essential Oils on a Psychrophilic Panagrolaimus sp. (Nematoda: Panagrolaimidae)

1
Department of Plant Diseases, Institute for Plant Protection and Environment, 11000 Belgrade, Serbia
2
Institute for Multidisciplinary Research, University of Belgrade, 11000 Belgrade, Serbia
3
Agroecology and Cropping Practices Group, Maize Research Institute, 11000 Belgrade, Serbia
4
Faculty of Technology Leskovac, University of Nis, 16000 Leskovac, Serbia
*
Author to whom correspondence should be addressed.
Plants 2020, 9(11), 1588; https://doi.org/10.3390/plants9111588
Received: 9 October 2020 / Revised: 5 November 2020 / Accepted: 9 November 2020 / Published: 17 November 2020
(This article belongs to the Special Issue Plant Parasitic Nematodes)

Abstract

:
Essential oils (EOs) have historically been used for centuries in folk medicine, and nowadays they seem to be a promising control strategy against wide spectra of pathogens, diseases, and parasites. Studies on free-living nematodes are scarce. The free-living microbivorous nematode Panagrolaimus sp. was chosen as the test organism. The nematode possesses extraordinary biological properties, such as resistance to extremely low temperatures and long-term survival under minimal metabolic activity. Fifty EOs from 22 plant families of gymnosperms and angiosperms were tested on Panagrolaimus sp. The aims of this study were to investigate the in vitro impact of EOs on the psychrophilic nematode Panagrolaimus sp. in a direct contact bioassay, to list the activity of EOs based on median lethal concentration (LC50), to determine the composition of the EOs with the best nematicidal activity, and to compare the activity of EOs on Panagrolaimus sp. versus plant parasitic nematodes. The results based on the LC50 values, calculated using Probit analysis, categorized the EOs into three categories: low, moderate and highly active. The members of the laurel family, i.e., Cinnamomum cassia and C. burmannii, exhibited the best nematicidal activity. Aldehydes were generally the major chemical components of the most active EOs and were the chemicals potentially responsible for the nematicidal activity.

1. Introduction

Nematodes are mostly microscopic size invertebrates that inhabit terrestrial and aquatic areas. Beside their significant economic importance as human, animal and plant parasites, they can also be beneficial, free-living microbivorous organisms. It has been estimated that about 2.5 million tons of pesticides are used on crops each year [1]. Such a practice has resulted in the decline of many beneficial organisms, such as nitrogen-fixing soil bacteria [2], blue-green algae [3], mycorrhizal fungi [4], water fishes [5], aquatic mammals [6], and birds [7]. In addition, the pesticide residues in food and water are massive long-term threats for human health at a global level. According to the European legislation (Regulation (EC) no. 1107/2009), the application of non-chemical and natural alternatives should be the first choice in plant protection and integrated pest management. The Regulation requires that substances or products produced or placed on the market do not have any harmful effect on human or animal health or any unacceptable effects on the environment, such as an impact on non-target species and impact on biodiversity and the ecosystem.
The use of essential oils (EOs) is known from folk medicine centuries ago [8]. Nowadays, it seems to be a promising control strategy against different nematode plant and animal parasites (Bursaphelenchus xylophilus, Cooperia spp., Ditylenchus dipsaci, Haemonchus contortus, Meloidogyne chitwoodi, M. incognita, M. javanica, Oesophagostomum spp., Pratylenchus penetrans, Steinernema feltiae, Trichostrongylus spp., Tylenchulus semipenetrans) [9,10,11,12,13,14,15,16,17,18,19,20,21,22,23]. Microbivorous nematodes contribute to decomposition of organic matter and the release of nutrients for plant uptake [24], which makes them important components of the soil microfauna. A free-living, microbivorous nematode, Panagrolaimus sp. Fuchs, was chosen as a test organism. Panagrolaimus sp. is a non-target organism, easy to maintain, does not have a complex life cycle, in contrast to plant parasitic nematodes [25], and possesses some extraordinary biological properties. This nematode, known as the Antarctic nematode, is famous for its resistance to intracellular freezing and extremely cold environmental conditions [26]. Panagrolaimus aff. detritophagus is the first viable multicellular organism, isolated from 30,000–40,000-year-old permafrost deposits [27].
This study aims to: (i) investigate the in vitro impact of EOs on the psychrophilic nematode Panagrolaimus sp. in a direct contact bioassay, (ii) list the activity of the EOs based on median lethal concentration (LC50), (iii) determine the composition of the EOs with the best nematicidal activity, and (iv) compare the activity of EOs on the non-target panagrolaimid nematode versus plant parasitic nematodes.

2. Results

The nematicidal activity of the EOs on the Panagrolaimus sp. juveniles are presented in Table 1.
The results based on the median lethal concentration (LC50) of 50 EOs are in range from 0.033 to 5.641 µL/mL. The list of all EOs could be divided into three groups. The first group is made up of those with LC50 values higher than 1 µL/mL, the next group with LC50 values in the range 0.1 to 1 µL/mL, and the last group with the LC50 values lower than 0.1 µL/mL. The lowest nematicidal impact is observed in the first group containing EOs from different plants with a significant content of gymnosperms, represented by the families Pinaceae and Cupressaceae. In the same group are some members of angiosperms, such as Burseraceae, Myrtaceae, etc. The second group with a moderate nematicidal effect on the panagrolaimid nematode had EOs originating mainly from the family Lamiaceae and some representatives from individual families. This study demonstrates, for the first time, the nematicidal activity of Turnera diffusa, Taxandria fragrans and Uncaria tomentosa EOs originating from the families Passifloraceae, Myrtaceae, and Rubiaceae, respectively. The best nematicidal activity among the three species was exhibited by Uncaria tomentosa EO, with an LC50 of 0.222 µL/mL.
The highest nematicidal impact was observed with three representatives from the family Lauraceae, namely Litsea citrata, Cinnamomum cassia, and C. burmannii, two representatives from the family Apiaceae—i.e., Foeniculum vulgare and Coriandrum sativum—and the single species Cymbopogon flexuosus from the family Poaceae, with LC50 values ranging from 0.033 to 0.091 µL/mL. The best nematicidal effect on panagrolaimid nematodes was shown by Cinnamomum. burmannii EO, extracted from the bark. The chemical composition of the EOs with the best nematicidal performance on Panagrolaimus sp., with the retention time (RT, in minutes) and the retention indices obtained experimentally and from the literature (RIexp and RIlit, respectively), are given in Table 2, Table 3, Table 4, Table 5, Table 6 and Table 7.
According to the gas chromatography/mass spectrometry (GC/MS) result obtained, 24 compounds were identified, representing 99.2% of total Litsea. citrata EO composition. The main components belong to oxygen-containing monoterpenes (contributing 84.3%), with citral—i.e., geranial (43.4%) and neral (32.2%)—as their representatives present in the highest percentage. They are followed by monoterpene hydrocarbons with 12.2% and limonene as their representative with a contribution of 9.4%, and sesquiterpene hydrocarbons ((E)-caryophyllene, β-elemene and α-humulene) with a contribution of 1.9% to the total EO composition (Table 2).
According to the results of GC/MS analysis of Foeniculum. vulgare EO, 18 compounds were identified, representing 99.1% of total EO composition. The main components were aromatic compounds (78.5%), with (E)-anethole as their representative present in the highest percentage (74.3%), followed by oxygen-containing monoterpenes (14.8%) and their representatives fenchone (2.1%) and carvone (2.1%), and monoterpene hydrocarbons (5.8%) with the highest amount of limonene (2.3%) (Table 3).
The results of the GC/MS analysis of the Cymbopogon. flexuosus EO revealed 32 compounds, representing 97.3% of total EO composition. The main components were oxygen-containing monoterpenes (86.3%) with geranial and neral (citral), contributing 40.3% and 30.9%, respectively, geranyl acetate and geraniol (5.4% and 4.5%, respectively), followed by sesquiterpene hydrocarbons (4.0%) and their representative (E)-caryophyllene (2.1%) (Table 4).
GC/MS analysis of the Coriandrum. sativum EO resulted in identifying 29 compounds, representing 97.5% of total EO composition. The main components were aldehydes (contributing 51.8%), with (2E)-decenal as their representative, followed by aliphatic alcohols (among which (2E)-decen-1-ol was present in the highest percentage of 16.3%) and oxygen-containing monoterpenes (21.7%) with linalool as the most abundant compound (18.4%) (Table 5).
The GC/MS analysis of Cinnamomum. cassia EO revealed 32 compounds, representing 99.3% of total EO composition. The main components belong to the group of aromatic compounds, contributing 91.8%, followed by sesquiterpene hydrocarbons (6.7%). (E)-Cinnamaldehyde and eugenol acetate were identified as the representatives of aromatic compounds contributing 76.7% and 7.4%, respectively. On the other hand, δ-cadinene with a contribution of 6.2% to the total EO composition, was identified as a representative compound from the sesquiterpene hydrocarbons group (6.7%) (Table 6).
According to the GC/MS results, 43 compounds, representing 98.1% of total C. burmanii EO composition, were identified. The main components belong to aromatic compounds (contributing 84.5% in the total EO composition), with (E)-cinnamaldehyde as their representative (80.5%). They are followed by sesquiterpene hydrocarbons (7.0%) with δ-cadinene and α-copaene as their members present in the amounts of 1.7% and 1.5%, respectively and oxygenated monoterpenes (5.5%) with α-terpineol (1.9%) as their main representative (Table 7).

3. Discussion

Essential oils with the highest nematicidal activity, demonstrated in this study, have been reported to be efficient against wide spectra of pathogens, diseases, and parasites.
The Litsea citrata EO showed antibacterial, antifungal, acaricidal, and nematicidal activities. The fruit essential oil of Litsea cubeba (syn. Litsea citrata) exhibited antibacterial activity against Bacillus cereus, Staphylococcus aureus, Vibrio parahaemolyticus, and Klebsiella pneumoniae [28]. As an antifungal agent it was effective against Candida krusei and C. guilliermondii but did not act against C. albicans, C. tropicalis and C. parapsilosis [29]. The Litsea cubeba EO had acaricidal activity against house dust mites, Dermatophagoides farinae and D. pteronyssinus, and stored food mites, Tyrophagus putrescentiae [30]. The LC50 values of ajowan, allspice and litsea were 0.431, 0.609 and 0.504 mg/mL, respectively, and exhibited good nematicidal activity against B. xylophilus [31]. Citral, i.e., geranial and neral, were the main compounds in the Litsea citrata EO in this study. Citral (3,7-dimethyl-2,6-octadienal) is the monoterpene aldehyde representing natural mixture of the two geometric isomers: geranial (trans-isomer) with a strong lemon odor and neral (cis-isomer) with a lemon odor that is less intense and sweeter than geranial [32].
The Foeniculum vulgare EO exhibited antifungal, antibacterial, antiviral, and nematicidal activities. In the inverted petriplate method, the volatile oil showed complete zone inhibition against Aspergillus niger, A. flavus, Fusarium graminearum, and F. moniliforme at a 6-µL dose [33]. Hot water extracts of fennel seeds was effective against Enterococcus faecalis, S. aureus, Escherichia coli, Pseudomonas aeruginosa, Salmonella typhimurium, S. typhi, and Shigella flexneri [34]. The DNA virus Herpes simplex type-1 (HSV-1) and the RNA virus parainfluenza type-3 (PI-3) were inhibited by the Foeniculum. vulgare EO [35]. Essential oils of Carum carvi, F. vulgare, Mentha rotundifolia, and M. spicata showed the highest nematicidal activity against M. javanica juveniles [9].
Trans-anethole was the most abundant compound in the Foeniculum vulgare EO, reaching 74% of the total identified constituents. Propenylbenzenes, such as anethole, were reported to be mutagenic for Salmonella tester strains and also carcinogenic in the induction of hepatomas in B6C3F1 mice and skin papillomas in CD-1 mice [36].
The Cymbopogon flexuosus lemongrass EO was reported to have antibacterial, antifungal and anti-inflammatory activity. The EO from C. flexuosus exhibited an antimicrobial effect against B. subtilis, Staphylococcus aureus, A. flavus and A. fumigatus [37]. The lemongrass (C. flexuosus) inflorescence EO was inhibitory to Pyricularia oryzae, Dreshlera oryzae, A. niger and Penicillium italicum [38]. Lemongrass EO, which has citral as its main component, has exhibited an anti-inflammatory effect in both animal and human cells [39]. In this study, the content of the lemongrass EO’s major compounds, geranial and neral, was similar to their content in the L. citrata EO with slightly lower amounts—40.3% and 30.9%, respectively.
The Coriandrum sativum EO exhibited antifungal, antibacterial, insecticidal, and nematicidal activities. The Coriandrum sativum EO showed excellent antifungal activity against seedborne pathogens P. oryzae, Bipolaris oryzae, Alternaria alternata, Tricoconis padwickii, Drechslera tetramera, D. halodes, Curvularia lunata, F. moniliforme, and F. oxysporum [40]. The methanolic extract of C. sativum showed antibacterial activity against E. coli, P. aeruginosa, S. aureus, and K. pneumoniae [41]. The leaf oil had significant toxic effects against the larvae of Aedes aegypti with an LC50 value of 26.93 ppm and an LC90 value of 37.69 ppm, and the stem oil has toxic effects against the larvae of A. aegypti with an LC50 value of 29.39 ppm and an LC90 value of 39.95 ppm [42]. Among the 28 plant EOs tested for their nematicidal activities against the pine wood nematode, B. xylophilus, the best nematicidal activity was achieved with the EO of coriander [43]. In this study, the major compound in the C. sativum EO was trans-2-decenal with 28.2%, affiliated to the group of medium-chain aldehydes. Aliphatic aldehydes (mainly C10–C16 aldehydes), with their unpleasant odor, are the main components of the volatile oil from the fresh herb [44]. Aldehydes present in the coriander EO are important biologically active substances due to their possible toxic activity against tropical mosquitoes transmitting dangerous illnesses [45].
The Cinnamomum cassia EO exhibited antimicrobial, antiviral, insecticidal, and nematicidal activities. The cassia EO acted as fungal growth inhibitor against A. flavus and A. oryzae [46] and as a bacterial inhibitor of S. aureus and E. coli [47]. The silver nanoparticles derived from cinnamon extract enhanced the antiviral activity and were found to be effective against highly pathogenic avian influenza virus subtype H7N3, when incubated with the virus prior to infection and introduced to cells after infection [48]. The chloroform extract from C. cassia was the most effective against Dermestes maculatus larvae, the pest of Egyptian mummies [8]. Cassia oil was efficient against Sitophilus zeamais [49], and the booklice Liposcelis bostrychophila [50]. As judged by the 24-h LC50 values, two cassia oils (0.084–0.085 mg/mL) and four cinnamon oils (0.064–0.113 mg/mL) were toxic toward adult B. xylophilus [51].
As opposed to cassia, Cinnamomum burmannii EO has been less studied. The Cinnamomum burmannii EO exhibited significant antibacterial properties against five common foodborne pathogenic bacteria, namely, B. cereus, L. monocytogenes, S. aureus, E. coli, and Salmonella anatum [52].
The major component of cinnamon bark EO is (E)-cinnamaldehyde. In the contact with bacterial membrane, cinnamaldehyde causes the loss of membrane functionality or the loss of channel proteins in the membrane, resulting in death of bacterial cells [53]. Besides this, (E)-cinnamaldehyde was significantly more effective than its corresponding acid (cinnamic acid) and alcohol (cinnamyl alcohol) and could be used as a fumigant with contact action in the control of house dust mites, D. farinae and D. pteronyssinus [54].
It has been emphasized that the major components play important roles in the toxicity of EOs [31,42,55] and the majority of them belong to the class of terpenes. Terpenes are the largest class of secondary metabolites and basically consist of five carbon isoprene units, which are assembled to each other (many isoprene units) by thousands of ways. Terpenes are simple hydrocarbons, while terpenoids (monoterpenes, sesquiterpenes, diterpenes, sesterpenes, and triterpenes) are a modified class of terpenes with different functional groups and an oxidized methyl group moved or removed at various positions [56].
Organic compounds that contain the group -CHO (the aldehyde group; i.e., a carbonyl group (C=O) with a hydrogen atom bound to the carbon atom) are known as aldehydes. In systematic chemical nomenclature, aldehyde names end with the suffix -al [57].
In this study, the major components and presumably the most active components (geranial, neral, trans-2-decenal, and trans-cinnamaldehyde) of Litsea citrata, Cymbopogon flexuosus, Coriandrum sativum, Cinnamomum cassia, and C. burmannii EOs are aldehydes. Aldehydes are highly reactive molecules that may have a variety of effects on biological systems. Although some aldehyde-mediated effects are beneficial, many effects are deleterious, including cytotoxicity, mutagenicity, and carcinogenicity [58], and generally, they are toxic to the human body [59] and evidently, to nematodes. Despite the potential risks of aldehyde exposure, the toxic mechanisms are only understood in general terms. Human exposure to aldehydes represents a significant toxicological concern and, therefore, understanding the corresponding molecular mechanism of toxicity is important for accurate risk assessment and remediation. In this perspective, it has been shown that environmental and endogenous aldehydes can be described by their relative softness and electrophilicity, which are important electronic determinants of the respective second order reaction rates with nucleophilic targets on macromolecules. These soft-soft and hard-hard adduct reactions appear to mediate toxicity by impairing the function of macromolecules (e.g., proteins, DNA, and RNA) that play critical roles in cytophysiological processes. However, more research is needed to broaden our understanding of how these specific covalent reactions disable macromolecular targets [60].
Comparing the results for the toxicity of EOs for nematodes with a different oral apparatus, they are mostly in agreement. However, some results for Panagrolaimus sp. deviate from those obtained for plant parasitic nematodes.
The Rosmarinus officinalis (syn. Salvia rosmarinus) EO at 2 µg/mL induced 100% mortality of Xiphinema index adults [61], while in this study, the same EO was characterized as having low toxicity and classified into the first group of EOs.
The LC50 of the M. spicata EO was 0.2 mg/mL, for M. javanica juveniles [62], while in this study the LC50 of the same oil was 0.505 µL/mL against Panagrolaimus sp. juveniles. Good nematicidal activity against male, female and juvenile nematodes of B. xylophilus was achieved, among other EOs, with the essential oils of Boswellia carterii [31]. In this study, Boswellia serata was classified into the group of EOs with low toxicity. The Pinus pinea EO was found to be toxic against M. incognita juveniles with an estimated LC50 of 44 ppm [63], while in this study EOs from gymnosperms, e.g., Pinus pinaster (LC50: 5.078 µL/mL), generally showed low toxicity to Panagrolaimus species.
Variations in acute toxicity among EOs of the same plant species are greatly influenced by production, storage conditions, climatic or edaphic factors [64]. The chemical content varies even within the same crop. Significant variations were found in many EO components, both across years and throughout harvest dates within locations [65]. However, the different impact of the same EO on free-living versus plant parasitic nematodes may be due to different feeding behaviors, different dimensions, and different metabolic activities and demonstrate a possible direction in the search for active compounds that will be at the same time toxic to plant parasitic nematodes and not have unacceptable effects on the environment and non-target species.

4. Materials and Methods

4.1. Nematode Culture and Direct Contact Bioassay

A culture of Panagrolaimus sp. was grown monoxenically on previously frozen agricultural compost and extracted from it with a Baerman funnel [66] over 24 h. Using a compound microscope and a micropipette, juveniles were separated from adult nematodes, counted in aliquots of 50 in 20 µL of water suspension and the live specimens were used in the experiments. The 50 commercial plant EOs from 22 families were purchased from the market and used to investigate their in vitro nematicidal activity against the panagrolaimid nematode Panagrolaimus sp. (Table 1). Serial dilutions starting from 0.2 µL/mL, in a double decreasing range up to 0.00975 µL/mL of EOs, were made and stabilized with 0.1-µL/mL Break-Thru® 446 oil enhancer. The direct contact bioassay was performed in small glass petri dishes containing 2 mL of solution and 50 nematodes incubated at 18 °C in the dark. The experiments were performed in five replicates. The lethal effect was monitored after 24 h. An aqueous solution of the emulsifier without EO served as the control. Prior to the assessment of the EOs, the mortality of panagrolaimid nematodes in the aqueous solution was compared with the mortality of nematodes in 0.1-µL/mL emulsifier and no significant differences between the treatments were observed. The nematodes were considered dead if they did not react on touching with a small needle.

4.2. Chemical Analyses

The gas chromatography/mass spectrometry (GC/MS) analysis was performed on an Agilent 6890N network gas chromatograph attached to a mass spectrometer (Agilent 5975B) equipped with a fused silica capillary column (HP-5ms) with dimensions as follows: 30-m length, 0.25-mm internal diameter, 0.25-μm film thickness, coated with 5% diphenyl- and 95% dimethyl-polysiloxane. The samples were diluted in diethyl ether (1:10) and a volume of 1.0 μL was injected. The injector was set at 220 °C and performed in the split mode at a ratio of 1:20. Helium was used as the carrier gas at a flow rate of 0.9 mL/min. The oven temperature increased from 60 to 246 °C at a rate of 3 °C/min. Temperatures of the mass selective detector (MSD) transfer line, ion source and quadruple mass analyzer were set at 280, 230 and 150 °C, respectively. The ionization voltage was 70 eV and the scan range was 35–400 m/z.
Compound identifications were based on comparisons of their mass spectra with the mass spectra obtained from the National Institute of Standards and Technology database and by comparisons of the retention indices with values reported in the literature (RIlit) [67]. A homologous series of n-alkanes (C8–C34) was run under the same operating conditions as the EO to determine the experimental retention indices (RIexp). The relative amounts of individual components (expressed in percentages) were calculated via peak area normalization, without the use of correction factors. Compounds present in traces (tr) with their amounts less than 0.05% are indicated (Table 2, Table 3, Table 4, Table 5, Table 6 and Table 7).

4.3. Statistical Data Analysis

In order to evaluate the nematicidal activity of the EOs, median lethal concentration (LC50) was calculated using the Probit Analysis program [68]. The Panagrolaimus mortality was corrected using Abbott’s formula [69]. The nematicidal activity, i.e., acute toxicity of the examined EOs based on the median lethal concentration, was designated as high (LC50: <0.1 µL/mL), moderate (LC50: 0.1–1 µL/mL) and low (LC50: >1 µL/mL) (Table 1).

Author Contributions

Conceptualization, V.O., S.K., M.T. and S.I.-S.; Methodology, V.O., S.K., M.T. and J.S.S.; Formal Analysis, V.O., M.T. and J.S.S.; Investigation, V.O. and S.I.-S.; Resources, S.K.; Data Curation, V.O., M.T. and J.S.S.; Writing—Original Draft Preparation, V.O., M.T. and J.S.S.; Writing—Review and Editing, S.K. and S.I.-S.; Visualization, V.O., M.T. and J.S.S.; Supervision, S.I.-S.; Funding Acquisition, S.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Serbian Ministry of Education, Science and Technological Development.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Koul, O.; Walia, S.; Dhaliwal, G.S. Essential oils as green pesticides: Potential and constraints. Biopestic. Int. 2008, 4, 63–84. [Google Scholar]
  2. Santos, A.; Flores, M. Effects of glyphosate on nitrogen fixation of free-living heterotrophic bacteria. Lett. Appl. Microbiol. 1995, 20, 349–352. [Google Scholar] [CrossRef]
  3. Saygideger, S.D.; Okkay, O. Effect of 2,4-dichlorophenoxyacetic acid on growth, protein and chlorophyll—A content of Chlorella vulgaris and Spirulina platensis cells. J. Environ. Biol. 2008, 29, 175–178. [Google Scholar] [PubMed]
  4. Zaller, J.G.; Heigl, F.; Ruess, L.; Grabmaier, A. Glyphosate herbicide affects belowground interactions between earthworms and symbiotic mycorrhizal fungi in a model ecosystem. Sci. Rep. 2014, 4, 5634. [Google Scholar] [CrossRef] [PubMed][Green Version]
  5. Ibrahim, L.; Preuss, T.G.; Ratte, H.T.; Hommen, U. A list of fish species that are potentially exposed to pesticides in edge-of-field water bodies in the European Union—A first step towards identifying vulnerable representatives for risk assessment. Environ. Sci. Pollut. Res. 2013, 20, 2679–2687. [Google Scholar] [CrossRef]
  6. Leonards, P.E.; Zierikzee, Y.; Brinkman, U.A.T.; Cofino, W.P.; van Straalen, N.M.; van Hattum, B. The selective dietary accumulation of planar polychlorinated biphenyls in the otter (Lutra lutra). Environ. Toxicol. Chem. 1997, 16, 1807–1815. [Google Scholar] [CrossRef]
  7. Brain, R.A.; Anderson, J.C. The agro-enabled urban revolution, pesticides, politics, and popular culture: A case study of land use, birds, and insecticides in the USA. Environ. Sci. Pollut. Res. 2019, 26, 21717–21735. [Google Scholar] [CrossRef][Green Version]
  8. Abdel-Maksoud, G.; El-Amin, A.-R.; Afifi, F. Insecticidal activity of Cinnamomum cassia extractions against the common Egyptian mummies’ insect pest (Dermestes maculatus). Int. J. Conserv. Sci. 2014, 5, 355–368. [Google Scholar]
  9. Oka, Y.; Nacar, S.; Putievsky, E.; Ravid, U.; Yaniv, Z.; Spiegel, Y. Nematicidal activity of essential oils and their components against the root-knot nematode. Phytopathology 2000, 90, 710–715. [Google Scholar] [CrossRef][Green Version]
  10. Pérez, M.P.; Navas-Cortés, J.A.; Pascual-Villalobos, M.J.; Castillo, P. Nematicidal activity of essential oils and organic amendments from Asteraceae against root-knot nematodes. Plant Path 2003, 52, 395–401. [Google Scholar] [CrossRef][Green Version]
  11. Park, I.; Park, J.; Kim, K.; Choi, K.; Choi, I.; Kim, C. Nematicidal activity of plant EOs and components from garlic (Allium sativum) and cinnamon (Cinnamomum verum) oils against the pine wood nematode (Bursaphelenchus xylophilus). Nematology 2005, 7, 767–774. [Google Scholar] [CrossRef]
  12. Elbadri, G.A.; Lee, D.W.; Park, J.C.; Yu, H.B.; Choo, H.Y.; Lee, S.M.; Lim, T.H. Nematocidal screening of essential oils and herbal extracts against Bursaphelenchus xylophilus. Plant Pathol. J. 2008, 24, 178–182. [Google Scholar] [CrossRef][Green Version]
  13. Barbosa, P.; Lima, A.S.; Vieira, P.; Dias, L.S.; Tinoco, M.T.; Barroso, J.G.; Pedro, J.G.; Figueriedo, A.C.; Mota, M. Nematicidal activity of essential oils and volatiles derived from Portuguese aromatic flora against the pinewood nematode, Bursaphelenchus xylophilus. J. Nematol. 2010, 42, 8–16. [Google Scholar] [PubMed]
  14. Ntalli, N.G.; Ferrari, F.; Giannakou, I.; Menkissoglu-Spiroudi, U. Phytochemistry and nematicidal activity of the essential oils from 8 Greek Lamiaceae aromatic plants and 13 terpene components. J. Agric. Food Chem. 2010, 58, 7856–7863. [Google Scholar] [CrossRef]
  15. Andrés, M.F.; González-Coloma, A.; Sanz, J.; Burillo, J.; Sainz, P. Nematicidal activity of essential oils: A review. Phytochem. Rev. 2012, 11, 371–390. [Google Scholar] [CrossRef][Green Version]
  16. Caboni, P.; Saba, M.; Tocco, G.; Casu, L.; Murgia, A.; Maxia, A.; Spiroudi, U.M.; Ntalli, N. Nematicidal activity of mint aqueous extracts against the root-knot nematode Meloidogyne incognita. J. Agric. Food Chem. 2013, 61, 9784–9788. [Google Scholar] [CrossRef]
  17. Kim, S.I.; Lee, J.K.; Na, Y.E.; Yoon, S.T.; Oh, Y.J. Nematicidal and ovicidal activities of Dryobalanops aromatica and Mentha haplocalyx var. piperascens-derived materials and their formulations against Meloidogyne incognita second-stage juveniles and eggs. Nematology 2014, 16, 193–200. [Google Scholar] [CrossRef]
  18. Faria, J.M.S.; Sena, I.; Ribeiro, B.; Rodrigues, A.M.; Maleita, C.M.N.; Abrantes, I.; Bennett, R.; Mota, M.; Da Silva Figueiredo, A.C. First report on Meloidogyne chitwoodi hatching inhibition activity of essential oils and essential oils fractions. J. Pest Sci. 2016, 89, 207–217. [Google Scholar] [CrossRef]
  19. André, W.P.P.; Ribeiro, W.L.C.; Oliveira, L.M.B.D.; Macedo, I.T.F.; Rondon, F.C.M.; Bevilaqua, C.M.L. Óleos essenciais e seus compostos bioativos no controle de nematoides gastrintestinais de pequenos ruminantes. Acta Sci. Vet. 2018, 46, 1514–1522. [Google Scholar] [CrossRef][Green Version]
  20. Ferreira, L.E.; Benincasa, B.I.; Fachin, A.L.; Contini, S.H.T.; França, S.C.; Chagas, A.C.S.; Beleboni, R.O. Essential oils of Citrus aurantifolia, Anthemis nobile and Lavandula officinalis: In Vitro anthelmintic activities against Haemonchus contortus. Parasites Vectors 2018, 11, 269. [Google Scholar] [CrossRef][Green Version]
  21. Saha, S.; Lachance, S. Effect of essential oils on cattle gastrointestinal nematodes assessed by egg hatch, larval migration and mortality testing. J. Helminthol. 2020, 94, e111. [Google Scholar] [CrossRef] [PubMed]
  22. Pardavella, I.; Nasiou, E.; Daferera, D.; Trigas, P.; Giannakou, I. The use of essential oil and hydrosol extracted from Satureja hellenica for the Control of Meloidogyne incognita and M. javanica. Plants 2020, 7, 856. [Google Scholar] [CrossRef]
  23. Oka, Y.; Ben-Daniel, B.; Cohen, Y. Nematicidal activity of the leaf powder and extracts of Myrtus communis against the root-knot nematode Meloidogyne javanica. Plant Path 2012, 1–9. [Google Scholar] [CrossRef]
  24. Ferris, H.; Venette, R.C.; Van der Meulen, H.R.; Lau, S.S. Nitrogen mineralization by bacterial–feeding nematodes: Verification and measurement. Plant Soil 1998, 203, 159–171. [Google Scholar] [CrossRef]
  25. Oro, V.; Knezevic, M.; Dinic, Z.; Delic, D. Bacterial microbiota isolated from cysts of Globodera rostochiensis (Nematoda: Heteroderidae). Plants 2020, 9, 1146. [Google Scholar] [CrossRef]
  26. Seybold, A.C.; Wharton, D.A.; Thorne, M.A.; Marshall, C.J. Establishing RNAi in a non–model organism: The Antarctic nematode Panagrolaimus sp. DAW1. PLoS ONE 2016, 11, e0166228. [Google Scholar] [CrossRef][Green Version]
  27. Shatilovich, A.V.; Tchesunov, A.V.; Neretina, T.V.; Grabarnik, I.P.; Gubin, S.V.; Vishnivetskaya, T.A.; Onstott, T.C.; Rivkina, E.M. Viable nematodes from late Pleistocene permafrost of the Kolyma river lowland. Dokl. Biol. Sci. 2018, 480, 100–102. [Google Scholar] [CrossRef]
  28. Su, Y.-C.; Ho, C.-L. Essential oil compositions and antimicrobial activities of various parts of Litsea cubeba from Taiwan. Nat. Prod. Comm. 2016, 11, 4515–4518. [Google Scholar] [CrossRef][Green Version]
  29. Ebani, V.V.; Nardoni, S.; Bertelloni, F.; Giovanelli, S.; Rocchigiani, G.; Pistelli, L.; Mancianti, F. Antibacterial and antifungal activity of essential oils against some pathogenic bacteria and yeasts shed from poultry. Flavour Fragr. J. 2016, 31, 302–309. [Google Scholar] [CrossRef]
  30. Jeon, Y.-J.; Lee, H.-S. Chemical composition and acaricidal activities of essential oils of Litsea cubeba fruits and Mentha arvensis leaves against house dust and stored food mites. J. Essent. Oil Bear. 2016, 19, 1721–1728. [Google Scholar] [CrossRef]
  31. Park, I.-K.; Kim, J.; Lee, S.-G.; Shin, S.-C. Nematicidal activity of plant essential oils and components from ajowan (Trachyspermum ammi), allspice (Pimenta dioica) and litsea (Litsea cubeba) essential oils against pine wood nematode (Bursaphelenchus xylophilus). J. Nematol. 2007, 39, 275–279. [Google Scholar] [PubMed]
  32. Di Mola, A.; Massa, A.; De Feo, V.; Basile, A.; Pascale, M.; Aquino, R.P.; De Caprariis, P. Effect of citral and citral related compounds on viability of pancreatic and human B-lymphoma cell lines. Med. Chem. Res. 2017, 26, 631–639. [Google Scholar] [CrossRef]
  33. Singh, G.; Maurya, S.; De Lampasona, M.P.; Catalan, C. Chemical constituents, antifungal and antioxidative potential of Foeniculum vulgare volatile oil and its acetone extract. Food Control 2006, 17, 745–752. [Google Scholar] [CrossRef]
  34. Kaur, G.J.; Arora, D.S. Antibacterial and phytochemical screening of Anethum graveolens, Foeniculum vulgare and Trachyspermum ammi. BMC Complement. Altern. Med. 2009, 9, 30. [Google Scholar] [CrossRef][Green Version]
  35. Orhan, I.E.; Ozcelik, B.; Kartal, M.; Kan, Y. Antimicrobial and antiviral effects of essential oils from selected Umbelliferae and Labiatae plants and individual essential oil components. Turk. J. Biol. 2012, 36, 239–246. [Google Scholar]
  36. Kim, S.G.; Liem, A.; Stewart, B.C.; Miller, J.A. New studies on trans-anethole oxide and trans-asarone oxide. Carcinogenesis 1999, 20, 1303–1307. [Google Scholar] [CrossRef][Green Version]
  37. Kakarla, S.; Ganjewala, D. Antimicrobial activity of essential oils of four lemongrass (Cymbopogon flexuosus Steud) varieties. Med. Aromat. Plant Sci. Biotechnol. 2009, 3, 107–109. [Google Scholar]
  38. Sarma, A.; Saikia, R.; Sarma, T.C.; Boruah, P. Lemongrass [Cymbopogon flexuosus (Steud) Wats] inflorescence oil: A potent anti fungal agent. J. Essent. Oil Bear. 2004, 7, 87–90. [Google Scholar] [CrossRef]
  39. Han, X.; Parker, T.L. Lemongrass (Cymbopogon flexuosus) essential oil demonstrated anti–inflammatory effect in pre-inflamed human dermal fibroblasts. Biochim. Open 2017, 4, 107–111. [Google Scholar] [CrossRef]
  40. Mandal, S.; Mandal, M. Coriander (Coriandrum sativum L.) essential oil: Chemistry and biological activity. Asian Pac. J. Trop. Biomed. 2015, 5, 421–428. [Google Scholar] [CrossRef][Green Version]
  41. Ratha bai, V.; Kanimozhi, D. Evaluation of antimicrobial activity of Coriandrum sativum. IJSRR 2012, 1, 1–10. [Google Scholar]
  42. Chung, I.M.; Ahmad, A.; Kim, S.J.; Naik, P.M.; Nagella, P. Composition of the essential oil constituents from leaves and stems of Korean Coriandrum sativum and their immunotoxicity activity on the Aedes aegypti L. Immunopharmacol. Immunotoxicol. 2012, 34, 152–156. [Google Scholar] [CrossRef] [PubMed]
  43. Kim, J.; Seo, S.M.; Lee, S.G.; Shin, S.C.; Park, I.K. Nematicidal activity of plant essential oils and components from coriander (Coriandrum sativum), oriental sweetgum (Liquidambar orientalis), and valerian (Valeriana wallichii) essential oils against pinewood nematode (Bursaphelenchus xylophilus). J. Agric. Food Chem. 2008, 56, 7316–7320. [Google Scholar] [CrossRef] [PubMed]
  44. Potter, T.L.; Fagerson, I.S. Composition of coriander leaf volatiles. J. Agric. Food Chem. 1990, 38, 2054–2056. [Google Scholar] [CrossRef]
  45. Bhuiyan, N.I.; Begum, J.; Sultana, M. Chemical composition of leaf and seed essential oil of Coriandrum sativum L. from Bangladesh. Bangladesh J. Pharmacol. 2009, 4, 150–153. [Google Scholar] [CrossRef]
  46. Kocevski, D.; Du, M.; Kan, J.; Jing, C.; Lacanin, I.; Pavlovic, H. Antifungal effect of Allium tuberosum, Cinnamomum cassia, and Pogostemon cablin essential oils and their components against population of Aspergillus species. J. Food Sci. 2013, 78, M731–M737. [Google Scholar] [CrossRef]
  47. Huang, D.F.; Xu, J.-G.; Liu, J.-X.; Zhang, H.; Hu, Q.P. Chemical constituents, antibacterial activity and mechanism of action of the essential oil from Cinnamomum cassia bark against four food related bacteria. Microbiology 2014, 83, 357–365. [Google Scholar] [CrossRef]
  48. Munazza, F.; Najam-us-Sahar, S.Z.; Deeba, A.; Farhan, A. In vitro antiviral activity of Cinnamomum cassia and its nanoparticles against H7N3 influenza A virus. J. Microbiol. Biotechnol. 2016, 26, 151–159. [Google Scholar] [CrossRef]
  49. Yang, Y.; Isman, M.B.; Tak, J.-H. Insecticidal activity of 28 essential oils and a commercial product containing Cinnamomum cassia bark essential oil against Sitophilus zeamais Motschulsky. Insects 2020, 11, 474. [Google Scholar] [CrossRef]
  50. Liu, X.C.; Cheng, J.; Zhao, N.N.; Liu, Z.L. Insecticidal activity of essential oil of Cinnamomum cassia and its main constituent, trans-cinnamaldehyde, against the booklice, Liposcelis bostrychophila. Trop. J. Pharm. Res. 2014, 13, 1697–1702. [Google Scholar] [CrossRef][Green Version]
  51. Kong, J.-O.; Lee, S.-M.; Moon, Y.-S.; Lee, S.-G.; Ahn, Y.-J. Nematicidal activity of cassia and cinnamon oil compounds and related compounds toward Bursaphelenchus xylophilus (Nematoda: Parasitaphelenchidae). J. Nematol. 2007, 39, 31–36. [Google Scholar] [PubMed]
  52. Shan, B.; Cai, Y.-Z.; Brooks, J.D.; Corke, H. Antibacterial properties and major bioactive components of cinnamon stick (Cinnamomum burmannii): Activity against foodborne pathogenic bacteria. J. Agric. Food Chem. 2007, 55, 5484–5490. [Google Scholar] [CrossRef] [PubMed]
  53. Song, Y.R.; Choi, M.S.; Choi, G.W.; Park, I.K.; Oh, C.S. Antibacterial activity of cinnamaldehyde and estragole extracted from plant essential oils against Pseudomonas syringae pv. actinidiae causing bacterial canker disease in kiwifruit. Plant Pathol. J. 2016, 32, 363–370. [Google Scholar] [CrossRef] [PubMed][Green Version]
  54. Wang, Z.; Kim, H.K.; Tao, W.; Wang, M.; Ahn, Y.-J. Contact and fumigant toxicity of cinnamaldehyde and cinnamic acid and related compounds to Dermatophagoides farinae and Dermatophagoides pteronyssinus (Acari: Pyroglyphidae). J. Med. Entomol. 2011, 48, 366–371. [Google Scholar] [CrossRef][Green Version]
  55. Echeverrigaray, S.; Zacaria, J.; Beltrão, R. Nematicidal activity of monoterpenoids against the root-knot nematode Meloidogyne incognita. Phytopathology 2010, 100, 199–203. [Google Scholar] [CrossRef][Green Version]
  56. Perveen, S. Terpenes and Terpenoids; IntechOpen: Rijeka, Croatia, 2018; pp. 1–13. [Google Scholar] [CrossRef]
  57. Daintith, J. A Dictionary of Chemistry, 6th ed.; Oxford University Press: Oxford, UK, 2008; pp. 16–17. [Google Scholar]
  58. Lindahl, R. Aldehyde dehydrogenases and their role in carcinogenesis. Crit. Rev. Biochem. Mol. Biol. 1992, 27, 283–335. [Google Scholar] [CrossRef]
  59. Laskar, A.A.; Younus, H. Aldehyde toxicity and metabolism: The role of aldehyde dehydrogenases in detoxification, drug resistance and carcinogenesis. Drug Metab. Rev. 2019, 1–23. [Google Scholar] [CrossRef]
  60. Lopachin, R.M.; Gavin, T. Molecular mechanisms of aldehyde toxicity: A chemical perspective. Chem. Res. Toxicol. 2014, 27, 1081–1091. [Google Scholar] [CrossRef]
  61. Avato, P.; Laquale, S.; Argentieri, M.P.; Lamiri, A.; Radicci, V.; D’Addabbo, T. Nematicidal activity of essential oils from aromatic plants of Morocco. J. Pest Sci. 2017, 90, 711–722. [Google Scholar] [CrossRef]
  62. Santana, O.; Andrés, M.F.; Sanz, J.; Errahmani, N.; Abdeslam, L.; González-Coloma, A. Valorization of essential oils from Moroccan aromatic plants. NPC 2014, 9, 1109–1114. [Google Scholar] [CrossRef][Green Version]
  63. Ibrahim, S.K.; Traboulsi, A.F.; El-Haj, S. Effect of essential oils and plant extracts on hatching, migration and mortality of Meloidogyne incognita. Phytopathol. Mediterr. 2006, 45, 238–246. [Google Scholar] [CrossRef]
  64. Kim, J.; Seo, S.-M.; Park, I.-K. Nematicidal activity of plant essential oils and components from Gaultheria fragrantissima and Zanthoxylum alatum against the pine wood nematode, Bursaphelenchus xylophilus. Nematology 2011, 13, 87–93. [Google Scholar] [CrossRef]
  65. Napoli, E.; Giovino, A.; Carrubba, A.; Siong, V.H.Y.; Rinoldo, C.; Nina, O.; Ruberto, G. Variations of essential oil constituents in oregano (Origanum vulgare subsp. viridulum (= O. heracleoticum) over cultivation cycles. Plants 2020, 9, 1174. [Google Scholar] [CrossRef] [PubMed]
  66. Hooper, D.J. Extraction of free-living stages from soil. In Laboratory Methods for Work with Plant and Soil Nematodes, 6th ed.; Southey, J.F., Ed.; Ministry of Agriculture, Fisheries and Food: London, UK, 1986; pp. 5–30. [Google Scholar]
  67. Adams, R.P. Identification of Essential Oil Components by Gas Chromatography/Mass Spectrometry, 4th ed.; Allured Publishing Corporation: Carol Stream, IL, USA, 2007; pp. 1–804. [Google Scholar]
  68. Daum, R.J. Revision of two computer programs for Probit analysis. Bull. Entomol. Soc. Am. 1970, 16, 10–15. [Google Scholar] [CrossRef]
  69. Abbott, W.S. A method of computing the effectiveness of an insecticide. J. Am. Mosq. Control Assoc. 1987, 3, 302–303. [Google Scholar] [CrossRef]
Table 1. LC50 (in µL/mL with 95% confidence limits and the slope values) of 50 plant essential oils investigated on Panagrolaimus sp. juveniles.
Table 1. LC50 (in µL/mL with 95% confidence limits and the slope values) of 50 plant essential oils investigated on Panagrolaimus sp. juveniles.
Species NamePlant PartFamilyLC50 (95% CL)Slope
Pogostemon cablinleavesLamiaceae5.641 (3.18–17.10)2.14
Pinus pinasterneedlesPinaceae5.078 (3.38–9.65)1.65
Santalum albumwoodSantalaceae4.781 (3.45–6.34)2.12
Azadirachta indicaseedsMeliaceae4.482 (2.52–10.01)2.02
Boswellia serrataresinBurseraceae4.394 (3.44–5.53)3.03
Commiphora myrrharesinBurseraceae4.301 (2.81–6.98)2.79
Juniperus virginianawoodJuniperaceae3.782 (2.43–5.48)1.81
Cupressus sempervirensneedlesCupressaceae3.360 (2.47–4.82)1.85
Abies sibiricaneedlesPinaceae3.269 (2.14–5.41)1.58
Cedrus atlanticawoodPinaceae2.943 (2.04–4.43)1.62
Juniperus communisberriesJuniperaceae2.513 (1.64–3.83)1.68
Eucalyptus globulusleavesMyrtaceae1.994 (1.47–2.56)3.70
Myrtus communisleavesMyrtaceae1.933 (1.34–2.65)2.27
Piper nigrumpeppercornsPiperaceae1.775 (1.37–2.25)2.37
Petroselinum crispumseedsApiaceae1.704 (1.14–2.38) 4.08
Zingiber officinalerootsZingiberaceae1.633 (1.28–2.09)1.98
Turnera diffusaleaves/flowersPassifloraceae1.550 (1.14–2.04)3.11
Abies albaneedlesPinaceae1.444 (1.03–1.95)1.87
Taxandria fragransleavesMyrtaceae1.437 (0.99–1.93)2.49
Melaleuca alternifolialeavesMyrtaceae1.150 (0.76–1.57)4.83
Vanilla planifoliabeansOrchidaceae1.135 (0.83–1.50)2.08
Salvia rosmarinusleaves/flowersLamiaceae1.128 (0.88–1.41)3.04
Curcuma longarhizomesZingiberaceae1.116 (0.70–1.62)1.50
Lavandula sp. leaves/flowersLamiaceae0.810 (0.62–1.01)3.49
Laurus nobilisleavesLauraceae0.594 (0.31–0.92)4.80
Melaleuca quinquenervialeavesMyrtaceae0.593 (0.40–0.82)1.76
Origanum vulgareleaves/flowersLamiaceae0.508 (0.38–0.65)3.33
Mentha spicataleaves/flowersLamiaceae0.505 (0.39–0.64)2.78
Pimpinella anisumseedsApiaceae0.450 (0.26–0.63)4.87
Salvia sclarealeaves/flowersLamiaceae0.430 (0.31–0.57)1.81
Anethum graveolensseedsApiaceae0.428 (0.32–0.56)3.00
Mentha piperitaleaves/flowersLamiaceae0.405 (0.23–0.58)3.93
Thymus vulgarisleaves/flowersLamiaceae0.391 (0.29–0.50)2.22
Gaultheria procumbensleavesEricaceae0.367 (0.26–0.48)2.25
Myristica fragransseedsMyristicaceae0.345 (0.23–0.48)4.24
Pelargonium asperumleavesGeraniaceae0.279 (0.20–0.37)3.03
Cymbopogon martinigrass bladesPoaceae0.275 (0.20–0.35)4.06
Syzygium aromaticumbudsMyrtaceae0.272 (0.20–0.34)3.91
Ocimum basilicumleaves/flowersLamiaceae0.263 (0.19–0.35)2.65
Uncaria tomentosabarkRubiaceae0.222 (0.17–0.29)2.47
Illicium verumseedsSchisandraceae0.191 (0.14–0.25)2.94
Cinnamomum verumleavesLauraceae0.172 (0.12–0.23)5.00
Cananga odorataflowersAnnonaceae0.145 (0.10–0.19)5.00
Mellisa officinalisleavesLamiaceae0.124 (0.09–0.16)2.74
Litsea citratafruitsLauraceae0.091 (0.06–0.12)3.14
Foeniculum vulgareseedsApiaceae0.080 (0.05–0.11)3.68
Cymbopogon flexuosusgrass bladesPoaceae0.071 (0.05–0.09)2.92
Coriandrum sativumleavesApiaceae0.044 (0.02–0.04)3.95
Cinnamomum cassiabarkLauraceae0.034 (0.02–0.04)2.00
Cinnamomum burmaniibarkLauraceae0.033 (0.02–0.04)2.73
Table 2. Chemical composition of Litsea citrata essential oil (EO).
Table 2. Chemical composition of Litsea citrata essential oil (EO).
RT *CompoundMolecular
Formula
RIexp **RIlit ***%
18.23Geranial (=E–citral)C10H16O1274126743.4
16.94Neral (=Z-citral)C10H16O1243123832.2
8.49LimoneneC10H16102810299.4
8.571,8-CineoleC10H18O103010311.9
24.27(E)-CaryophylleneC15H24141914191.6
13.17CitronellalC10H18O115311531.4
11.03LinaloolC10H18O110010961.2
5.70α-PineneC10H169339391.1
14.40(E)-IsocitralC10H16O118311801.1
17.42GeraniolC10H18O125512520.9
6.87β-PineneC10H169779790.8
7.106-Methyl-5-hepten-2-oneC8H14O9859850.8
13.63(Z)-IsocitralC10H16O116411640.8
6.76SabineneC10H169739750.6
14.71α-TerpineolC10H18O119011880.6
16.31NerolC10H18O122912290.4
6.10CampheneC10H169489540.3
7.25Dehydro-1,8-cineoleC10H16O9919910.2
23.10β-ElemeneC15H24139213900.2
12.84exo-IsocitralC10H16O114411440.1
14.17Terpinen-4-olC10H18O117711770.1
25.65α-HumuleneC15H24145314540.1
5.51α-ThujeneC10H16926930tr
8.35o-CymeneC10H1410241026tr
Total identified99.2
* RT—retention time, ** RIexp—retention index obtained experimentally, *** RIlit—retention index from the literature, tr—traces.
Table 3. Chemical composition of Foeniculum vulgare EO.
Table 3. Chemical composition of Foeniculum vulgare EO.
RT *CompoundMolecular
Formula
RIexp **RIlit ***%
18.93(E)-AnetholeC10H12O21291128474.3
11.28α-Pinene oxideC10H16O110610999.0
15.06Methyl chavicol (=Estragol)C10H12O119911962.9
5.71α-PineneC10H169339392.3
8.48LimoneneC10H16102810292.3
10.62FenchoneC10H16O108810862.1
16.94CarvoneC10H14O124412432.1
17.39p-Anis aldehydeC8H8O2125412501.3
8.33o-CymeneC10H14102410260.7
12.81CamphorC10H16O114411460.6
8.571,8-CineoleC10H18O103010310.5
11.07LinaloolC10H18O100110960.4
9.53γ-TerpineneC10H16105810590.3
6.10CampheneC10H169489540.1
6.87β-PineneC10H169779790.1
11.79α-CampholenalC10H16O111911260.1
6.76SabineneC10H16973975tr
7.24MyrceneC10H16991990tr
Total identified99.1
* RT—retention time, ** RIexp—retention index obtained experimentally, *** RIlit—retention index from the literature, tr—traces.
Table 4. Chemical composition of Cymbopogon flexuosus EO.
Table 4. Chemical composition of Cymbopogon flexuosus EO.
RT *CompoundMolecular
Formula
RIexp **RIlit ***%
18.24Geranial (=E-citral)C10H16O1274126740.3
16.94Neral (=Z-citral)C10H16O1244123830.9
22.86Geranyl acetateC12H20O2138513815.4
17.45GeraniolC10H18O125512524.5
7.106-Methyl-5-hepten-2-oneC8H14O9859852.7
24.27(E)-CaryophylleneC15H24141914192.1
11.03LinaloolC10H18O110110961.4
28.08γ-CadineneC15H24151415131.4
14.38(E)-IsocitralC10H16O118211801.3
6.10CampheneC10H169489541.1
8.48LimoneneC10H16102810291.1
10.004-NonanoneC9H18O1071-0.9
13.64(Z)-IsocitralC10H16O116411640.9
5.71α-PineneC10H169339390.3
7.241,8-Dehydro-cineoleC10H16O9919900.3
8.561,8-CineoleC10H18O103010310.3
13.03trans-α-NecrodolC10H18O114911480.3
13.16CitronellalC10H18O115211530.3
28.45δ-CadineneC15H24152315230.3
30.72Caryophyllene oxideC15H24O158215820.3
8.76(Z)-β-OcimeneC10H16103610370.2
25.64α-HumuleneC15H24145314540.2
5.43TricycleneC10H169229260.1
8.34o-CymeneC10H14102410260.1
9.14(E)-β-OcimeneC10H16104610500.1
10.62TerpinoleneC10H16108810880.1
12.84exo-IsocitralC10H16O114411440.1
14.08Rosefuran epoxideC10H14O2117511770.1
14.72α-TerpineolC10H18O119111880.1
16.32NerolC10H18O122912290.1
6.87β-PineneC10H16977979tr
7.60n-OctanalC8H16O1003998tr
Total identified97.3
* RT—retention time, ** RIexp—retention index obtained experimentally, *** RIlit—retention index from the literature, tr—traces.
Table 5. Chemical composition of Coriandrum sativum EO.
Table 5. Chemical composition of Coriandrum sativum EO.
RT *CompoundMolecular
Formula
RIexp **RIlit ***%
17.78(2E)-DecenalC10H18O1263126328.2
18.10(2E)-Decen-1-olC10H20O1271127116.3
11.08LinaloolC10H18O1101109618.4
26.20(2E)-DodecenalC12H22O146714668.8
15.35n-DecanalC10H20O120612016.2
18.19n-DecanolC10H22O127312695.4
34.07n-TetradecanolC14H30O167316724.0
21.97(2E)-UndecenalC11H20O136313601.7
12.80CamphorC10H16O114311461.2
23.85DodecanalC12H24O140914081.1
8.34o-CymeneC10H14102410260.9
5.71α-PineneC10H169339390.7
15.00(4E)-DecenalC10H18O119811960.6
17.43GeraniolC10H18O125512520.6
10.03cis-Linalool oxide C10H18O2107210720.4
10.62trans-Linalool oxideC10H18O2108810860.4
19.62UndecanalC11H22O130713060.4
22.85Geranyl acetateC12H20O2138413810.4
7.60n-OctanalC8H16O10039980.3
8.48LimoneneC10H16102810290.3
31.86TetradecanalC14H28O161316120.3
8.571,8-CineoleC10H18O103010310.2
9.53γ-TerpineneC10H16105810590.2
14.85(4Z)-DecenalC10H18O119411940.2
6.10CampheneC10H169489540.1
6.88β-PineneC10H169779790.1
14.71α-TerpineolC10H18O119011880.1
13.69BorneolC10H18O11651169tr
14.17Terpinen-4-olC10H18O11771177tr
Total identified97.5
* RT—retention time, ** RIexp—retention index obtained experimentally, *** RIlit—retention index from the literature, tr—traces.
Table 6. Chemical composition of Cynnamomum cassia EO.
Table 6. Chemical composition of Cynnamomum cassia EO.
RT *CompoundMolecular
Formula
RIexp **RIlit ***%
24.54(E)-CinnamaldehydeC9H8O1272126776.7
33.02Eugenol acetateC12H14O3153515217.4
32.39δ-CadineneC15H24151715226.2
29.95(E)-Cinnamyl acetateC11H12O2144814434.0
17.88Phenethyl alcoholC8H10O112611060.8
11.96BenzaldehydeC7H6O9629520.7
21.91(Z)-CinnamaldehydeC9H8O122012170.6
22.78CarvoneC10H14O124312390.4
19.69HydrocinnamaldehydeC9H10O116311630.3
25.28α-MethylcinnamaldehydeC10H10O133213180.3
30.51CoumarinC9H6O2145614320.3
15.10γ-TerpineneC10H16105610540.2
23.202-Phenyl ethyl acetateC10H12O2125912540.2
27.57α-CopaeneC15H24136813740.2
10.93α-PineneC10H169299320.1
10.93CampheneC10H169439460.1
14.391,8-CineoleC10H18O102710260.1
19.88BorneolC10H18O116811650.1
20.19Terpinen-4-olC10H18O117411740.1
26.98EugenolC10H12O2135913560.1
30.99γ-MuuroleneC15H24147014780.1
31.11 β-SelineneC15H24147814890.1
32.51trans-Cadina-1,4-dieneC15H24152615330.1
25.901-epi-CubenolC15H26O162216270.1
12.48β-PineneC10H16973974tr
14.25β-PhellandreneC10H1610251025tr
16.93TerpinoleneC10H1610871086tr
27.27CyclosativeneC15H2413571358tr
28.10SativeneC15H2413821374tr
28.84IsosativeneC15H2414011417tr
29.14(E)-CaryophylleneC15H2414131417tr
31.76α-MuuroleneC15H2414941500tr
Total identified99.3
* RT—retention time, ** RIexp—retention index obtained experimentally, *** RIlit—retention index from the literature, tr—traces.
Table 7. Chemical composition of Cynnamomum burmannii EO.
Table 7. Chemical composition of Cynnamomum burmannii EO.
RT *CompoundMolecular
Formula
RIexp **RIlit ***%
24.51(E)-CinnamaldehydeC9H8O1272126780.5
20.70α-TerpineolC10H18O118911861.9
32.51δ-CadineneC15H24151715221.7
27.57α-CopaeneC15H24136813741.5
21.82(Z)-CinnamaldehydeC9H8O122012171.5
19.60HydrocinnamaldehydeC9H10O116311631.3
19.79BorneolC10H18O116811651.2
20.17Terpinen-4-olC10H18O117411741.2
31.74α-MuuroleneC15H24149415001.2
29.05(E)-CaryophylleneC15H24141314170.8
17.10LinaloolC10H18O110010950.5
11.87BenzaldehydeC7H6O9629520.4
24.54SafroleC10H10O2128812850.4
28.76IsosativeneC15H24140114170.4
31.32α-SelineneC15H24148714980.4
24.75TridecaneC13H28129513000.3
14.29β-PhellandreneC10H16102510250.2
15.84cis-Linalool oxide C10H18O2107110670.2
20.54CryptoneC9H14O118511830.2
28.03SativeneC15H24138213740.2
30.92γ-MuuroleneC15H24147014780.2
31.15β-SelineneC15H24147814890.2
30.21(E)-Cinnamyl acetateC11H12O2144814430.2
36.26epi-α-Murrolol C15H26O163916400.2
13.37α-PhellandreneC10H16100210020.1
14.421,8-CineoleC10H18O102710260.1
14.96γ-TerpineneC10H16105610540.1
16.62p-CymeneneC10H14108710890.1
16.99TerpinoleneC10H16108710860.1
18.87trans-Limonene oxideC10H16O113711370.1
25.24α-MethylcinnamaldehydeC10H10O133213180.1
27.18CyclosativeneC15H24135713580.1
28.25β-ElemeneC15H24138613890.1
28.54(Z)-CaryophylleneC15H24140014080.1
29.82HumuleneC15H24144614520.1
30.51CoumarinC9H6O2145614320.1
36.35α-Muurolol (Torreyol)C15H26O164316440.1
12.83MyrceneC10H16994998tr
17.70Phenethyl alcoholC8H10O11261106tr
19.45IsoborneolC10H18O11541155tr
32.80trans-Cadina-1,4-dieneC15H2415261533tr
33.15α-CalacoreneC15H2015381544tr
32.92Benzyl benzoateC14H12O217721759tr
Total identified98.1
* RT—retention time, ** RIexp—retention index obtained experimentally, *** RIlit—retention index from the literature, tr—traces.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Oro, V.; Krnjajic, S.; Tabakovic, M.; Stanojevic, J.S.; Ilic-Stojanovic, S. Nematicidal Activity of Essential Oils on a Psychrophilic Panagrolaimus sp. (Nematoda: Panagrolaimidae). Plants 2020, 9, 1588. https://doi.org/10.3390/plants9111588

AMA Style

Oro V, Krnjajic S, Tabakovic M, Stanojevic JS, Ilic-Stojanovic S. Nematicidal Activity of Essential Oils on a Psychrophilic Panagrolaimus sp. (Nematoda: Panagrolaimidae). Plants. 2020; 9(11):1588. https://doi.org/10.3390/plants9111588

Chicago/Turabian Style

Oro, Violeta, Slobodan Krnjajic, Marijenka Tabakovic, Jelena S. Stanojevic, and Snezana Ilic-Stojanovic. 2020. "Nematicidal Activity of Essential Oils on a Psychrophilic Panagrolaimus sp. (Nematoda: Panagrolaimidae)" Plants 9, no. 11: 1588. https://doi.org/10.3390/plants9111588

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop