Toxicity of Fixed Oils, Essential Oils and Isolated Chemicals to Hetorhabditis amazonensis and Steinernema rarum
by
Alixelhe Pacheco Damascena
*, 
Luis Moreira de Araujo Junior
,
Luiza Akemi Gonçalves Tamashiro
and
Dirceu Pratissoli
Department of Agronomy, Center of Agrarian Sciences and Engineering, Espírito Santo Federal University, Alto Universitário, s/n, Guararema, Alegre 29500-000, ES, Brazil
*
Author to whom correspondence should be addressed.
Stresses 2025, 5(1), 15; https://doi.org/10.3390/stresses5010015
Submission received: 18 December 2024
/
Revised: 26 January 2025
/
Accepted: 6 February 2025
/
Published: 17 February 2025
(This article belongs to the Collection Feature Papers in Human and Animal Stresses)
Abstract
:Non-target organisms are not well studied. The objective of this work was to evaluate the effect of seven essential oils, two fixed oils, d-limonene and eugenol on the mortality, behavior and infectivity of entomopathogenic nematodes (ENPs). The oils were diluted at 1% (v/v) in water with Tween® 80 PS at 0.05% (v/v), and water with Tween® alone was used as the control treatment. In the mortality test, 2 mL of solution containing 50 µL of the nematode suspension, 20 µL of oil/compounds solution isolated with Tween 80, and 1930 µL of water were placed in plastic containers. After four days, the number of dead juveniles was counted. In the bioassay of the behavior of the EPNs, the frequency of lateral body beats of the infective juveniles in liquid medium was analyzed after exposure to the solutions. In the infectivity test, after contact of the EPNs with oils and essential oil chemical compounds, the juveniles were washed and applied to second-instar Spodoptera eridania larvae. All oils and isolated compounds caused mortality in H. amazonensis and S. rarum, with Ocimum canum and the isolated compound eugenol showing the highest efficacy against H. amazonensis and O. canum, Eucalyptus citriodora, Zingiber officinale, Salvia sclarea and the isolated compound eugenol being the most effective against S. rarum. There was a reduction in the number of lateral beats of H. amazonensis and S. rarum for all treatments, with the exception of Cymbopogon winterianus in H. amazonensis and Annona muricata in S. rarum. The infectivity of H. amazonenis and S. rarum on S. eridania was reduced when exposed to the solutions, with the exception of the isolated compound d-limonene in both species, soursop for H. amazonenis and rosemary for S. rarum, which were classified as non-toxic to the species tested. The results obtained in this study may be useful for the choice of oils and essential oil chemical compounds with potential use in integrated pest management programs.
1. Introduction
In recent years, the use of oils in pest management has gained prominence due to their toxicological properties against several insect species and their ability to reduce the risk of cross-resistance due to the complex chemical structure of the constituents in the essential oil and their rapid degradation compared to synthetic insecticides, causing less damage to human health and the environment [1,2,3].
There are many studies reporting the efficiency of essential oils and their chemical compounds in the management of harmful organisms, such as phytoparasitic nematodes and agricultural and forestry pests. However, the action of oils and essential oil chemical compounds on non-target organisms, such as parasitoids, predators and entomopathogenic nematodes (ENPs), is poorly studied. EPNs are beneficial nematodes that contribute to the biological control of various pests, especially those belonging to the order Lepidoptera [4,5,6]. These organisms have some attributes such as a short life cycle, a wide host range, environmental safety and persistence in the environment, which place them as potential agents for the biological control of pests [7]. They are obligate parasites and have a symbiotic relationship with bacteria of the genus Xenorhabdus in the case of Steinernema and Photorhabdus in Heterorhabditis, capable of infecting and killing the host [8].
Considering the existence of several studies evaluating the efficiency of oils and essential oil chemical compounds in pest management and few studies on the action of oils on non-target organisms, the objective of this work is to evaluate the mortality, infectivity and behavior of the entomopathogenic nematodes Hetorhabditis amazonensis IBCB 10 (Rhabditida: Heterorhabditidae) and Steinernema rarum PAM 25 (Rhabdita: Steinernematidae) when exposed to treatments with d-limonene, eugenol, basil, eucalyptus, ginger, salvia, rosemary, citronella, neem and soursop.
2. Results
2.1. Chemical Characterization of Essential Oils
In the chromatographic profile of the essential oils tested, the major components were as follows: citronellal (78.32%) for eucalyptus; α-zingiberene (16.34%) and geranial (12.23%) for ginger; 1,8-cineole // eucalyptol (32.00%), camphor (20.48%) and α-pinene (18.73%) for rosemary; citronellal (42.52%), geraniol (21.64%) and citronellol (15.72%) for citonella; linalool acetate (65.59%) and linalool (24.00%) for Salvia; and linalool (86.24%) for basil (Table 1).
2.2. Mortality of Entomopathogenic Nematodes Subjected to the Application of Oils and Oil-Derived Compounds
All isolated oils and compounds resulted in EPN mortality (F = 2.35; p < 0.001). For H. amazonensis, sweet basil oil (O. canum) and the isolated compound eugenol presented the highest mortalities, with 92.41 ± 9.88% and 100 ± 0.00%, respectively, differing from the other treatments. The highest mortalities for S. rarum were observed with the oils of basil (O. canum), eucalyptus (E. citriodora), ginger (Z. officinale) and sage (S. sclarea) and for the isolated compound eugenol, which was significantly different from the other oils and essential oil chemical compounds. For most products, there was no difference in mortality between species, with the exception of eucalyptus oil (E. citriodora), which caused higher mortality in S. rarum (Table 2).
2.3. Behavior of Entomopathogenic Nematodes Subjected to the Application of Oils and Oil-Derived Compounds
The interaction between the factors (treatments × time) was significant for the species H. amazonensis (F = 5.69; p < 0.001). At time 0, the lowest number of body side taps was observed in the presence of eucalyptus oil (E. citriodora) (45.11 ± 22.90), which was statistically different from the other oils and essential oil chemical compounds. After 30 min, the lowest values of body beats were observed for the isolated compound eugenol (1.00 ± 1.80) and for the oils of basil (O. canum) (16.22 ± 9.57), eucalyptus (E. citriodora) (5.22 ± 5.84) and rosemary (R. officinalis) (3.11 ± 6.31), all of which statistically differed from the other treatments. After 60 min, the lowest values of side beats remained associated with the same oils mentioned above.
Analyzing over time, there was a reduction in the number of lateral beats of H. amazonensis for all oils, essential oil chemical compounds and the control, with the exception of citronella oil (C. winterianus), which maintained a consistent number of beats, showing no statistical difference between 0, 30 and 60 min (Table 3).
For S. rarum, the interaction between the factors (treatments × time) was significant (F = 10.12; p < 0.001). At time 0, the lowest number of side body stroke rate was observed in the presence of eucalyptus (E. citriodora) and salvia (S. sclarea) oils, with values of 43.44 ± 34.00 and 53.67 ± 30.31, respectively. Similar to what was observed for H. amazonensis, at time points 30 and 60, the isolated compound eugenol and basil (O. canum), eucalyptus (E. citriodora) and rosemary (R. officinalis) oils resulted in lower beat values. At time 60, the number of lateral beats of S. rarum was 0.00 ± 0.00 for eugenol, 1.44 ± 1.01 for basil (O. canum), 5.78 ± 16.96 for eucalyptus (E. citriodora) and 0.00 ± 0.00 for rosemary oil (R. officinalis).
When analyzed over time, there was a reduction in the number of beats for all oils, essential oil chemical compounds and the control, with the exception of soursop oil (A. muricata), which showed no statistical difference over time (Table 4).
2.4. Infectivity of Entomopathogenic Nematodes in Spodoptera eridania Larvae Subjected to the Application of Essential Oils, Fixed Oils and Oil-Derived Compounds
The number of infective juveniles of H. amazonensis needed to kill 80% of the fourth instar larvae of S. eridania was 400 IJ/insect, and for S. rarum, it was 100 IJ/insect (Table 5).
The infectivity of H. amazonensis reduced when exposed to the oils and major compounds tested, with the exception of the isolated compound d-limonene and soursop oil (A.muricata), which did not differ statistically from the control. There was no infectivity of H. amazonensis when exposed to the major compound eugenol (0.0%) (Table 6).
For S. rarum, the major compound d-limonene and rosemary oil (R. officinalis) did not differ from the control, indicating that the infectivity of S. rarum was not reduced. S. rarum did not infect S. eridania when exposed to the major compound eugenol and citronella (C. winterianus) oil (0.0%) (Table 7).
In the classification of toxicity in S. eridania larvae, the major compound d-limonene was considered non-toxic to H. amazonensis and S. rarum. Soursop oil was classified as non-toxic for H. amazonensis, and rosemary oil was classified as non-toxic for S. rarum. The isolated compound eugenol was considered toxic to both EPN species tested (Table 8).
3. Discussion
The essential oils, fixed oils and essential oil chemical compounds tested were lethal to H. amazonensis and S. rarum. Studies have reported that isolated oils and compounds can kill plant-parasitic nematodes [8,9]. Many essential oils are known for their nematicidal activity [8,10,11] and are used in the management of various agricultural and forestry pests [12,13,14]. It turns out that the oils not only kill plant-parasitic nematodes (PPNs) but also beneficial nematodes (EPNs). Therefore, attention must be paid to using these oils as a tool in integrated pest management since commercial products based on these oils are available on the market.
Sweet basil (O. canum) and the isolated compound eugenol promoted higher mortalities in H. amazonensis, and the oils of basil (O. canum), eucalyptus (E. citriodora), ginger (Z. officinale), sage (S. sclarea) and the eugenol compound were the most toxic to S. rarum. The mode of action of the oils and isolated compounds in nematodes is not well understood and needs further studies [15]. However, the cuticle of nematodes is one of the main structures that guarantee their development and survival. It is mainly constituted of lipids, considered as organic compounds insoluble in water and soluble in solvents such as oil [13,16]. Furthermore, the absence of chitin in nematodes facilitates the penetration of oils [17]. Therefore, the mortality of nematodes due to the oils is probably related to their lipophilic properties. In general, oils have an affinity for the body surface of mites and insects. When they penetrate the cuticle of these organisms, they dissolve lipids [16,18], which we hypothesized to occur in EPNs.
The oils and oil-derived compounds tested have an effect on the lateral movement of nematodes (number of beats), reflecting their locomotion. The reduction in the number of side beats of the nematode’s body may or may not be stopped in the presence of the oils and may vary over time. In the presence of adverse conditions, EPNs can still present quiescent behavior, also known as cryptobiosis, in which they reduce their metabolic activity [19]. The compatibility of EPNs with products in general varies according to the characteristics of the EPN species and strain, influenced by temperature and exposure time [20,21,22].
Regarding the infectivity of EPNs in S. eridania, the isolated compound eugenol was toxic to the EPNs, reducing the infectivity of S. rarum and H. amazonensis, possibly due to the mortality of infective juveniles (IJ). It is considered a volatile phenolic compound, reported to have insecticidal, fungicidal and bactericidal properties [23,24,25,26,27]. In addition, this compound can kill or inhibit the development of plant-parasitic nematodes, reducing the number of galls and egg masses in plant roots [28,29]. This compound can affect nematode embryogenesis or kill second-instar juveniles [30,31]. Despite the effectiveness of eugenol in the management of pests [32], diseases [15] and nematodes [28], the toxic action of this compound on non-target organisms should also be considered.
Of the oils and essential oil chemical compounds tested, only the compound d-limonene was classified as non-toxic for S. rarum and H. amazonensis, and soursop and rosemary oils were non-toxic to H. amazonensis and S. rarum, respectively. Orange oil, whose major compound is d-limonene, is toxic to plant-parasitic nematodes [33,34,35] and several insect pests [36,37,38]. In recent years, d-limonene has gained prominence in botanical insecticide formulations [38], and together with neem oil (A. indica), it was one of the most used oils as a bioinsecticide in the state of California, USA [39]. Therefore, the results obtained indicate that d-limonene holds potential as a botanical insecticide. Soursop and rosemary oils are still underexplored in the management of pests and diseases. Given the selectivity attributed to these oils, they present potential for inclusion in the composition of botanical insecticides.
4. Materials and Methods
4.1. Obtaining Entomopathogenic Nematodes
Populations of EPNs were obtained from the Collection of Entomopathogenic Nematodes at the Banco do Instituto Biológico de Campinas, São Paulo, Brazil. The infective juveniles (IJs) of H. amazonensis and S. rarum were multiplied in larvae of Tenebrio molitor (Linnaeus, 1758) (Coleoptera: Tenebrionidae). Ten T. molitor larvae were used per Petri dish (9 cm in diameter), coated with filter paper moistened with a 1 mL suspension containing nematode IJs at a concentration of 500 IJs/cm2. The dead larvae were transferred to White’s traps [40] and stored in an incubator chamber (BOD) at 25 °C. After 11 days, the IJs were collected and placed in plastic containers with distilled water and stored in climatized chambers (18 ± 1 °C, 70 ± 10% RH and a 12-hour photophase). IJs were used within 48 h of collection.
4.2. Obtaining the Isolated Oils and Compounds
The essential oils and essential oil chemical compounds used were as follows: essential oil of eucalyptus (Eucalyptus citriodora—Ferquima batch 114, São Paulo, Brazil), essential oil of rosemary (Rosmarinus officinalis—Destilaria Bauru batch DBKT-ALIP1218/312), essential oil of sage (Salvia sclarea—Ferquima batch 227, Catanduva, São Paulo, Brazil), sweet basil essential oil (Ocimum canum—Terraflor lot 20027, Alto Paraíso de Goiás, Brazil), citronella essential oil (Cymbopogon winterianus—Ferquima, lot 158, São Paulo, Brazil), neem fixed oil (Azadirachta indica—Ribeirão Comercial Agricola Ltd.a, Guaraíta, Goiás, Brasil —0.15% azadirachtin A and 0.12% azadirachtin B), eugenol (isolated compound—Maquira dental products industry, Maringá, Paraná, Brazil) and d-limonene (isolated compound—Fraction Químicos Fractions, Barueri, São Paulo, Brazil, batch 190715/01).
Ginger essential oil (Zingiber officinale Roscoe) was obtained via hydrodistillation of the root “in natura”. The ginger was cut into small portions of approximately 300 g and subjected to hydrodistillation in triplicate. Each material was placed in a 2 L flask, and 500 mL of water was added. The flask was connected to a Clevenger and subjected to heating. Thus, the hydrodistillation process was carried out for three consecutive hours [41]. After 3 h, the hydrolate (essential oil and water) was collected, separated via centrifugation, transferred to an Eppendorf tube and stored in a refrigerator at 0 °C. The mass of the oil was measured to calculate the yield.
To obtain soursop fixed oil (Annona muricata Linn), 400 g of soursop residue was weighed, and the seeds were separated and dried in a forced air circulation oven (MARCONI, model MA 035/5) at 55 °C for 72 h so that the seeds become dry. The husks were manually removed from the seeds. The mass of the peeled seeds was measured to determine the yield. The contents were stored in a freezer at −20 °C for proximate analysis and oil extraction. Extraction was performed via extrusion [42]. Then, 100 g of seeds were weighed, and the oil was extracted using the Gourmet Oil Extractor (HOME UP, model MQO 001). The lipid fraction was transferred to Falcon tubes and centrifuged at 2500 rpm for five minutes. The final volume of oil was measured, and the yield calculated.
4.3. Chemical Characterization of Essential Oils and Oil-Derived Compounds
All essential oils and oil-derived compounds were characterized via gas chromatography to assess their chemical composition and purity. The identification of chemical compounds present in each essential oil was performed via gas chromatography coupled to a mass spectrometer (GC–MS) equipped with a selective mass detector, model QP-PLUS-2010 (Shimadzu). The analysis employed a stationary phase fused silica capillary column Rtx-5MS that was 30 m long and 0.25 mm inner diameter, using helium as carrier gas. The quantification and determination of retention rates (RR) of the compounds present in the essential oils was performed via gas chromatography (GC) using a Shimadzu GC-2010 Plus, equipped with a flame ionization detector (FID) and a capillary column Rtx-5MS, 30 m long and 0.25 mm inner diameter. The carrier gas used was nitrogen. In both analyses, the injector temperature was 220 °C, the detector temperature was 300 °C, and the column’s initial temperature was 60 °C, which was programmed to increase by 3 °C per minute until reaching a maximum temperature of 240 °C. The identification of the compounds was obtained by comparing their mass spectra with those existing in the equipment’s database and with literature data using retention rate (RR).
4.4. Mortality of Entomopathogenic Nematodes Subjected to the Application of Oils and Essential Oil Chemical Compounds
The experiments were carried out at the Center for Scientific and Technological Development in Phytosanitary Management of Pests and Diseases (NUDEMAFI), located at the Center for Agricultural Sciences and Engineering at the Federal University of Espírito Santo (CCAE-UFES).
To evaluate the toxic effect of the major oils/compounds on entomopathogenic nematodes, essential oils, fixed oils and oil-derived compounds were diluted to 1% (v/v) following the methodology of Barua et al. (2020) [15]. As a control (negative control), water and 0.05% (v/v) Tween® 80 PS were used. The 1% concentration of oils was used because, in preliminary tests, this concentration was used to kill Spodoptera eridania larvae, showing potential for their management.
The suspensions containing nematodes were prepared by counting, in triplicate, the number of juveniles present in an aliquot, estimating that 15 infective juveniles were present in 50 µL. Therefore, 2 mL of solution, containing 50 µL of the nematode suspension, 20 µL of oil/compounds solution isolated with Tween 80, and 1930 µL of water, were placed in plastic pots (3.5 cm Ø). The recipients were placed in climatized chambers at a temperature of 20 ± 1 °C and a RH of 70 ± 10%.
Four days after the experiment was set up, the number of dead juveniles was evaluated by counting and observing under a stereoscopic microscope (Tecnival). Individuals with extended/straight bodies after stimulation with the stylet were considered dead, and individuals who moved after stimulation with the stylet were considered alive, according to the methodology of [11].
The design used was completely randomized, in a factorial scheme (10 × 2), with ten oils and a control and two species of entomopathogenic nematodes (H. amazonensis and S. rarum), with 10 replicates. The data were subjected to analysis of variance, and the means were compared using the Scott–Knott test at a 5% probability level in R statistical software 4.4.2 (ExDes.pt package) [43]. Mortality was corrected using Abbott’s formula (1925) [44].
4.5. Behavior of Entomopathogenic Nematodes Subjected to the Application of Oils and Oil-Derived Compounds
To evaluate the effect of oils on the mobility of H. amazonenis and S. rarum, the methodology proposed by [45] was followed with adaptations, analyzing the frequency of lateral body beats of infective juveniles in a liquid medium.
Solutions containing infective juveniles and the isolated oils/compounds were prepared similarly to the mortality test. The solutions were placed in plastic containers and, at the same time, under a stereoscopic microscope (Tecnival), the number of lateral body strikes was counted for three randomly selected nematodes during one minute at three respective times: 0 min, 30 min and 60 min, at a temperature of 25 °C and 70% RH.
The design used was completely randomized, in a factorial scheme (11 × 3), with ten oils and a control and three time points, with three replicates for each time point. The data were subjected to analysis of variance, and the means were compared using the Scott–Knott test at a 5% probability level in R statistical software 4.4.2 (ExDes.pt package) [43].
4.6. Infectivity of Entomopathogenic Nematodes in Spodoptera eridania Larvae Subjected to the Application of Essential Oils, Fixed Oils and Essential Oil Chemical Compounds
The infectivity of entomopathogenic nematodes in Spodoptera eridania larvae was evaluated following the application of essential oils, fixed oils and essential oil chemical compounds. This host was used because the oils used in this study can be used to manage S. eridania.
To verify the number of infective juveniles of each species of entomopathogenic nematode to be used in the experiment with S. eridania, preliminary tests were carried out for the two species of entomopathogenic nematode, with different concentrations of IJs from H. amazonensis and S. rarum.
First, 2 mL of the suspension containing 48-hour-old IJs was prepared, with concentrations varying according to the treatments: 0, 25, 50, 100, 150, 200, 300, 400 IJ/insect, and 2 mL of distilled water was added to the control. The recipients were kept in an incubator at a temperature of 25 °C and 70% RH. Mortality assessments were performed eight days after nematode inoculation. Once mortality was verified, the larvae were individually transferred to White trap [40] to verify the emergence of nematodes.
The experiment was carried out in a completely randomized design, with 8 treatments and 10 replicates. The data obtained were evaluated using R statistical software 4.4.2 [43], and the means were compared using the Tukey test at a 5% significance level.
To verify the virulence of H. amazonensis and S. rarum after exposure to oils and essential oil chemical compounds, 2nd instar larvae of Spodoptera eridania (Cramer) (Lepidoptera: Noctuidae) were used. The caterpillars were sourced from the stock creation Nucleus for Scientific and Technological Development in Phytosanitary Management of Pests and Diseases (NUDEMAFI), where they were fed an adapted artificial diet [13].
A 10 mL suspension containing the infective juveniles and 2 mL of a solution of isolated oils/compounds and Tween 80 were placed in glass tubes (2.5 × 8.5 cm) and kept at a temperature of 16 ± 1 °C and RH of 60 ± 10% for 30 min. Subsequently, 3 mL of the supernatant was removed, and the same volume of distilled water was added in order to remove any oil residue and/or isolated compound, according to the methodology of Özdemir et al. (2020) [46]. The same procedure was performed three times to ensure the elimination of the oil residue and/or isolated compound. After this step, an aliquot containing 400 IJ infective juveniles of the respective nematodes was removed from this suspension. A triple count of 20 µL samples was performed, and the samples were placed in plastic pots (3.5 cm Ø) containing filter paper, artificial diet and a 2nd instar larva of S. eridania.
Evaluations were carried out after eight days by observing the dead larvae. The larvae were then transferred individually to the White trap [40] to confirm the mortality caused by EPNs.
The design used was completely randomized, with 10 replicates for treatment. Data were subjected to the non-parametric Kruskal–Wallis test, and the means were compared using Dunn’s test at a 5% probability level in the R statistical software (ExDes.pt package) [43]. The infectivity reduction was calculated based on the following formula: Reduction (%) = (1 − It/Ic) × 100, where It corresponded to mortality in the treatments and Ic to mortality in the control [47]. The products were classified as to selectivity based on the IOBC guide, with the following classifications: (1) non-toxic (<30%), (2) slightly toxic (30–79%), (3) moderately toxic (80–99%) and (4)) toxic (>99%).
5. Conclusions
The results obtained in this study may be useful for the choice of oils and essential oil chemical compounds with potential use in integrated pest management programs. All oils tested were lethal to H. amazonensis and S. rarum. However, in terms of IJ infectivity, the major compound, d-limonene, was considered non-toxic to H. amazonensis and S. rarum, while soursop oil was considered non-toxic to H. amazonensis and rosemary oil was considered non-toxic to S. rarum, according to the toxicological classification of the IOBC. The isolated compound eugenol was considered toxic to EPNs, making it not suitable for use as it negatively affected the survival, behavior and infection of beneficial nematodes. Given the potential of EPNs and other organisms in the biological control of pests, it is recommended to verify the selectivity of oils on such organisms in order to detect which oils are incompatible with beneficial organisms and should not be used in integrated pest management.
Author Contributions
Conceptualization, A.P.D. and L.A.G.T.; methodology, A.P.D.; software, L.M.d.A.J.; validation, A.P.D., L.A.G.T. and L.M.d.A.J.; formal analysis, L.M.d.A.J.; investigation, A.P.D.; resources, A.P.D.; data curation, A.P.D.; writing—original draft preparation, A.P.D.; writing—review and editing, A.P.D. and D.P.; visualization, A.P.D.; supervision, D.P.; project administration, D.P.; funding acquisition, A.P.D. and D.P. All authors have read and agreed to the published version of the manuscript.
Funding
This research received no external funding.
Data Availability Statement
All datasets used or analyzed during this study are included in this article.
Acknowledgments
The authors would like to acknowledge the following agencies: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq and Fundação de Apoio à Pesquisa do Espírito Santo (FAPES).
Conflicts of Interest
The authors declare no conflict of interest.
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Table 1.
Tested essential oils and their major compounds (major compounds representing more than 10% of the total composition based on peak area).
Table 1.
Tested essential oils and their major compounds (major compounds representing more than 10% of the total composition based on peak area).
| Essential Oils | Major Compounds (>10%) | |
|---|---|---|
| Common Name | Scientific Name | |
| Eucalyptus | Eucalyptus citriodora Hook | Citronellal (78.32), citronellol (9.90), isopulegol (7.28), citronellol acetate (1.23), Ecaryophyllene (1.21), NIa (0.81) |
| Ginger | Zingiber officinale Roscoe | 2-heptanol (0.79), α-pinene (1.64), camphene (5.88), myrcene (1.47), β-phellandrene (5.04), 1,8-cineole(=eucalyptol) (5.53), minalol (0.91), borneol (1.35), α-terpineol (1.06), citronellol (1.57), neral (9.06), geraniol (1.17), geranial (12.23), NI (10.44), α-amorfeno (1.00), α-curcumeno (5.02), α-zingiberene (16.34),α-farnesene (8.97), β-sesquiphellandrene (7.22), germacrene B (7.22), (E)trans-nerolidol (0.64), NI (2.03) |
| Rosemary | Rosmarinus officinalis | α-pinene (18.73), NI (0.88), tricyclene (1.06), α-pinene (19.73%), myrcene (1.79), camphene (7.00), β-pinene (3.37), p-cymene (2.53), 1,8- cineole(=eucalyptol) (32.00%), γ-terpinene (0.52), camphor (20.48%), linalool (2.10), isoborneol (2.36), terpinen-4-ol (0.76), α-terpineol (2.74), geraniol (1.16), isobornyl acetate (1.93), NI (0.59%) |
| Citonella | Cymbopogon winterianus | Limonene (1.03), linalool (0.66), isopulegol (0.72), citronellal (42.52), citronellol (15.72), geraniol (21.64), citronellyl acetate (3.10), geraniol acetate (3.33), β-elemene (1.35), NI (0.88), Germacrene D (2.09), α-Muurolene (0.95), γ-cadinene (0.64), δ-cadinene (2.10), elemol (2.26), NI (1.01) |
| Salvia | Salvia sclarea | Linalool (24.00), α-Terpineol (3.31), Linalool acetate (65.59), Neryl acetate (1.43), Geranyl (2.66), (E)-Caryophyllene (1.72), germacrene D (1.30) |
| Basil | Ocimum brasilicum L. | Linalool (86.24), α-Pinene (1.05), limonene (2.70), (E)-Caryophyllene (4.75), α-Humulene (1.80), NI (3.46) |
NI = Not identified.
Table 2.
Corrected mortality (%) (±standard deviation) of Heterorhabditis amazonensis and Steinernema rarum following exposure to essential oils, fixed oils and essential oil chemical compounds in the laboratory (25 ± 2 °C, relative humidity of 60 ± 10%).
Table 2.
Corrected mortality (%) (±standard deviation) of Heterorhabditis amazonensis and Steinernema rarum following exposure to essential oils, fixed oils and essential oil chemical compounds in the laboratory (25 ± 2 °C, relative humidity of 60 ± 10%).
| Treatments | Heterorhabditis amazonensis | Steinernema rarum |
|---|---|---|
| D-limonene | 62.50 ± 15.92 Ac | 63.89 ± 11.19 Ab |
| Eugenol | 100.00 ± 0.00 Aa | 100.00 ± 0.00 Aa |
| Basil | 92.41 ± 9.88 Aa | 87.22 ± 12.84 Aa |
| Eucalyptus | 67.86 ± 10.27 Bc | 86.11 ± 10.88 Aa |
| Ginger | 82.59 ± 11.61 Ab | 84.44 ± 10.41 Aa |
| Salvia | 80.36 ± 10.35 Ab | 74.44 ± 14.39 Aa |
| Rosemary | 57.59 ± 17.69 Ac | 53.89 ± 18.15 Ab |
| Citonella | 69.65 ± 12.77 Ac | 57.78 ± 20.15 Ab |
| Neem | 58.48 ± 23.91 Ac | 66.67 ± 28.81 Ab |
| Soursop | 76.79 ± 14.85 Ab | 63.33 ± 15.76 Ab |
| F interaction | 23.54 | |
| p-value | <0.001 | |
Means followed by the same lowercase letter in the column and the same uppercase in the row do not differ from each other according to the Scott–Knott test at a 5% significance level.
Table 3.
Mean number of body strokes of Heterorhabditis amazonensis (±standard deviation) following the application of essential oils, fixed oils and essential oil chemical compounds at three time intervals (0, 30 and 60 min), in the laboratory (25 ± 2 °C, relative humidity of 60 ± 10%).
Table 3.
Mean number of body strokes of Heterorhabditis amazonensis (±standard deviation) following the application of essential oils, fixed oils and essential oil chemical compounds at three time intervals (0, 30 and 60 min), in the laboratory (25 ± 2 °C, relative humidity of 60 ± 10%).
| Treatments | Time (Minutes) | ||
|---|---|---|---|
| 0 | 30 | 60 | |
| Control | 138.44 ± 27.41 Aa | 108.00 ± 21.36 Ba | 79.67 ± 14.22 Ca |
| D-limonene | 99.44 ± 37.87 Ab | 52.78 ± 33.40 Bb | 28.78 ± 22.25 Cc |
| Eugenol | 73.22 ± 23.29 Ac | 1.00 ± 1.80 Bd | 0.00 ± 0.00 Bd |
| Basil | 77.22 ± 32.28 Ac | 16.22 ± 9.57 Bd | 4.00 ± 4.21 Bd |
| Eucalyptus | 45.11 ± 22.90 Ad | 5.22 ± 5.84 Bd | 0.56 ± 0.52 Bd |
| Ginger | 67.78 ± 29.53 Ac | 58.22 ± 9.98 Ab | 31.44 ± 25.23 Bc |
| Salvia | 84.33 ± 23.55 Ac | 41.00 ± 17.53 Bb | 31.67 ± 12.88 Bc |
| Rosemary | 79.78 ± 22.41 Ac | 3.11 ± 6.31 Bd | 0.00 ± 0.00 Bd |
| Citonella | 77.11 ± 28.86 Ac | 65.22 ± 27.21 Ab | 77.67 ± 16.84 Aa |
| Neem | 66.56 ± 23.34 Ac | 33.22 ± 16.90 Bc | 25.11 ± 11.93 Bc |
| Soursop | 80.11 ± 23.05 Ab | 60.11 ± 13.07 Bb | 40.78 ± 8.27 Cb |
| F interaction | 5.69 | ||
| p-value | <0.001 | ||
Means followed by the same lowercase letter in a column and the same uppercase in a row do not differ from each other according to the Scott–Knott test at a 5% significance level.
Table 4.
Average number of body strokes of Steinernema rarum (±standard deviation) subjected to the application of essential oils, fixed oils and essential oil chemical compounds in three time intervals (0, 30 and 60 min) in the laboratory (25 ± 2 °C, relative humidity of 60 ± 10%).
Table 4.
Average number of body strokes of Steinernema rarum (±standard deviation) subjected to the application of essential oils, fixed oils and essential oil chemical compounds in three time intervals (0, 30 and 60 min) in the laboratory (25 ± 2 °C, relative humidity of 60 ± 10%).
| Treatments | Time (Minutes) | ||
|---|---|---|---|
| 0 | 30 | 60 | |
| Control | 127.78 ± 30.49 Aa | 108.44 ± 22.03 Aa | 79.67 ± 14.22 Bb |
| D-limonene | 127.00 ± 50.02 Aa | 59.11 ± 35.08 Bb | 40.44 ± 16.79 Bc |
| Eugenol | 119.22 ± 34.58 Aa | 0.56 ± 1.13 Bd | 0.00 ± 0.00 Bd |
| Basil | 101.44 ± 31.76 Ab | 9.22 ± 12.04 Bd | 1.44 ± 1.01 Bd |
| Eucalyptus | 43.44 ± 34.00 Ad | 7.11 ± 4.42 Bd | 5.78 ± 16.96 Bd |
| Ginger | 98.33 ± 32.56 Ab | 90.33 ± 24.93 Aa | 26.67 ± 23.46 Bc |
| Salvia | 53.67 ± 30.31 Ad | 69.33 ± 20.80 Ab | 26.00 ± 13.43 Bc |
| Rosemary | 73.33 ± 16.55 Ac | 1.89 ± 23.35 Bd | 0.00 ± 0.00 Bd |
| Citonella | 76.78 ± 16.55 Ac | 27.00 ± 16.55 Bc | 42.11 ± 18.05 Bc |
| Neem | 95.33 ± 9.28 Ab | 27.67 ± 9.28 Bc | 20.33 ± 13.10 Bc |
| Soursop | 124.33 ± 25.61 Aa | 112.33 ± 28.29 Aa | 120.00 ± 19.30 Aa |
| F interaction | 10.12 | ||
| p-value | <0.001 | ||
Means followed by the same lowercase letter in the column and the same uppercase in the row do not differ from each other according to the Scott–Knott test at the 5% significance level.
Table 5.
Mortality of Spodoptera eridania caused by the entomopathogenic nematodes Hetorhabditis amazonensis and Steinernema rarum at different concentrations.
Table 5.
Mortality of Spodoptera eridania caused by the entomopathogenic nematodes Hetorhabditis amazonensis and Steinernema rarum at different concentrations.
| Concentration | Mortality (%) | |
|---|---|---|
| Hetorhabditis amazonensis | Steinernema rarum | |
| 0 | 0.0 ± 0.0 a | 0.0 ± 0.0 a |
| 25 | 0.0 ± 0.0 a | 60.0 ± 14.1 ab |
| 50 | 20.0 ± 14.1 a | 60.0 ± 14.1 ab |
| 100 | 20.0 ± 14.1 a | 80.0 ± 44.7 b |
| 150 | 20.0 ± 14.1 a | 80.0 ± 44.7 b |
| 200 | 20.0 ± 14.1 a | 80.0 ± 44.7 b |
| 300 | 60.0 ± 32.1 ab | 80.0 ± 44.7 b |
| 400 | 80.0 ± 54.4 b | 100.0 ± 0.0 b |
| p-value | <0.001 | <0.001 |
Means followed by the same letter do not differ from each other at the 5% probability level according to Tukey’s test (p < 0.05).
Table 6.
Infectivity of Hetorhabditis amazonensis exposed to essential oils, fixed oils and major compounds in the laboratory at a temperature of 25 ± 2 °C and a humidity of 60 ± 10%.
Table 6.
Infectivity of Hetorhabditis amazonensis exposed to essential oils, fixed oils and major compounds in the laboratory at a temperature of 25 ± 2 °C and a humidity of 60 ± 10%.
| Oils (1%) | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | 11 |
|---|---|---|---|---|---|---|---|---|---|---|---|
| 2 | 0.5000 | - | - | - | - | - | - | - | - | - | - |
| 3 | 0.0000 * | 0.0000 * | - | - | - | - | - | - | - | - | - |
| 4 | 0.0026 * | 0.0006 * | 0.0001 * | - | - | - | - | - | - | - | - |
| 5 | 0.0026 * | 0.0026 * | 0.0006 * | 0.3209 | - | - | - | - | - | - | - |
| 6 | 0.0026 * | 0.0026 * | 0.0314 | 0.0314 | 0.0814 | - | - | - | - | - | - |
| 7 | 0.0026 * | 0.0006 * | 0.0006 * | 0.3209 | 0.5000 | 0.0814 | - | - | - | - | - |
| 8 | 0.0026 * | 0.0006 * | 0.0006 * | 0.3209 | 0.5000 | 0.0814 | 0.5000 | - | - | - | - |
| 9 | 0.0026 * | 0.0026 * | 0.0314 | 0.0314 | 0.0814 | 0.5000 | 0.0814 | 0.0814 | - | - | - |
| 10 | 0.0026 * | 0.0026 * | 0.0314 | 0.0314 | 0.0814 | 0.5000 | 0.0814 | 0.0814 | 0.5000 | - | - |
| 11 | 0.5000 | 0.5000 | 0.0000 * | 0.0006 * | 0.0006 * | 0.0026 * | 0.0026 * | 0.0026 * | 0.0026 * | 0.0026 * | - |
| Mortality (%) | 100.0 | 100.0 | 0.0 | 40.0 | 70.0 | 40.0 | 70.0 | 70.0 | 40.0 | 40.0 | 100.0 |
| Kruskal–Wallis Chi-square | 43.61 | ||||||||||
| Degrees of freedom | 10 | ||||||||||
| p-value | >0.01 | ||||||||||
* alpha = 0.05. Reject Ho if p ≤ alpha/2 according to Dunn’s test. 1—Control; 2—D-limonene; 3—Eugenol; 4—Basil; 5—Eucalyptus; 6—Ginger; 7—Salvia; 8—Rosemary; 9—Citronella; 10—Neem; 11—Soursop.
Table 7.
Infectivity of Steinernema rarum exposed to essential oils, fixed oils and major compounds in the laboratory at a temperature of 25 ± 2 °C and humidity of 60 ± 10%.
Table 7.
Infectivity of Steinernema rarum exposed to essential oils, fixed oils and major compounds in the laboratory at a temperature of 25 ± 2 °C and humidity of 60 ± 10%.
| Oils (1%) | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | 11 |
|---|---|---|---|---|---|---|---|---|---|---|---|
| 2 | 0.5000 | - | - | - | - | - | - | - | - | - | - |
| 3 | 0.0000 * | 0.0000 * | - | - | - | - | - | - | - | - | - |
| 4 | 0.0037 * | 0.0037 * | 0.0373 | - | - | - | - | - | - | - | - |
| 5 | 0.0037 * | 0.0037 * | 0.0373 | 0.5000 | - | - | - | - | - | - | - |
| 6 | 0.0002 * | 0.0002 * | 0.1863 | 0.1863 | 0.1863 | - | - | - | - | - | - |
| 7 | 0.0002 * | 0.0002 * | 0.0037 * | 0.1863 | 0.1863 | 0.0373 | - | - | - | - | - |
| 8 | 0.0373 | 0.0373 | 0.0002 * | 0.0373 | 0.0373 | 0.0037 * | 0.1863 | - | - | - | - |
| 9 | 0.0000 * | 0.0000 * | 0.5000 | 0.0373 | 0.0373 | 0.1863 | 0.0037 * | 0.0002 * | - | - | - |
| 10 | 0.0037 * | 0.0037 * | 0.0373 | 0.5000 | 0.5000 | 0.1863 | 0.1863 | 0.0373 | 0.0373 | - | - |
| 11 | 0.0037 * | 0.0037 * | 0.0373 | 0.5000 | 0.5000 | 0.1863 | 0.1863 | 0.0373 | 0.0373 | 0.5000 | - |
| Mortality (%) | 100.0 | 100.0 | 0.0 | 40.0 | 40.0 | 20.0 | 60.0 | 80.0 | 20.0 | 40.0 | 60.0 |
| Kruskal–Wallis Chi-square | 48.57 | ||||||||||
| Degrees of freedom | 10 | ||||||||||
| p-value | >0.01 | ||||||||||
* alpha = 0.05. Reject Ho if p ≤ alpha/2 according to Dunn’s test. 1—Control; 2—D-limonene; 3—Eugenol; 4—Basil; 5—Eucalyptus; 6—Ginger; 7—Salvia; 8—Rosemary; 9—Citronella; 10—Neem; 11—Soursop.
Table 8.
Reduction of infectivity of Steinernema rarum and Heterorhabditis amazonensis in Spodoptera eridania larvae and classification of the toxicity of essential oils, fixed oils and major compounds at a temperature of 25 ± 2 °C and a humidity of 60 ± 10%.
Table 8.
Reduction of infectivity of Steinernema rarum and Heterorhabditis amazonensis in Spodoptera eridania larvae and classification of the toxicity of essential oils, fixed oils and major compounds at a temperature of 25 ± 2 °C and a humidity of 60 ± 10%.
| Heterorhabditis amazonensis | Steinernema rarum | |||
|---|---|---|---|---|
| Oils (1%) | Reduction (%) 1 | Classification 2 | Reduction (%) 1 | Classification 2 |
| Witness | - | - | - | - |
| D-limonene | 0.0 | 1 | 0.0 | 1 |
| Eugenol | 100.0 | 4 | 100.0 | 4 |
| Ocimum canum | 60.0 | 2 | 60.0 | 2 |
| Eucalyptus citriodora | 30.0 | 2 | 60.0 | 2 |
| Zingiber officinale | 60.0 | 2 | 80.0 | 3 |
| Salvia sclarea | 30.0 | 2 | 40.0 | 2 |
| Rosmarinus officinalis | 30.0 | 2 | 20.0 | 1 |
| Cymbopogon winterianus | 60.0 | 2 | 80.0 | 3 |
| Azadirachta indica | 60.0 | 2 | 60.0 | 2 |
| Annona muricata | 0.0 | 1 | 40.0 | 2 |
1 Reduction of infectivity: Red (%) = (1 − It/Ic) × 100. 2 Toxicological classification according to IOBC: 1 non-toxic (<30%), 2 slightly toxic (30–79%), 3 moderately toxic (80–99%) and 4 toxic (>99%).
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Damascena, A.P.; de Araujo Junior, L.M.; Tamashiro, L.A.G.; Pratissoli, D. Toxicity of Fixed Oils, Essential Oils and Isolated Chemicals to Hetorhabditis amazonensis and Steinernema rarum. Stresses 2025, 5, 15. https://doi.org/10.3390/stresses5010015
AMA Style
Damascena AP, de Araujo Junior LM, Tamashiro LAG, Pratissoli D. Toxicity of Fixed Oils, Essential Oils and Isolated Chemicals to Hetorhabditis amazonensis and Steinernema rarum. Stresses. 2025; 5(1):15. https://doi.org/10.3390/stresses5010015
Chicago/Turabian StyleDamascena, Alixelhe Pacheco, Luis Moreira de Araujo Junior, Luiza Akemi Gonçalves Tamashiro, and Dirceu Pratissoli. 2025. "Toxicity of Fixed Oils, Essential Oils and Isolated Chemicals to Hetorhabditis amazonensis and Steinernema rarum" Stresses 5, no. 1: 15. https://doi.org/10.3390/stresses5010015
APA StyleDamascena, A. P., de Araujo Junior, L. M., Tamashiro, L. A. G., & Pratissoli, D. (2025). Toxicity of Fixed Oils, Essential Oils and Isolated Chemicals to Hetorhabditis amazonensis and Steinernema rarum. Stresses, 5(1), 15. https://doi.org/10.3390/stresses5010015
