INTRODUCTION

Soybean, Glycine max (L.) Merr (Fabales: Fabaceae), is a globally significant crop, playing a pivotal role in oil and protein production (Graham and Vance 2003; Hamza et al., 2024). Argentina is the world’s third-largest producer of soybeans, with an annual output of 51 million tonnes, accounting for 13% of global production (USDA, 2022). Nevertheless, various pests and fungal diseases can cause considerable damage to these crops in Argentina, resulting in significant annual economic losses (Jerez et al., 2023; Murúa et al., 2018; Ploper, 2004). The fall armyworm (FAW), Spodoptera frugiperda JE Smith (Lepidoptera: Noctuidae), and the blister beetle (BB), Epicauta atomaria Germar (Coleoptera: Meloidae), are phytophagous insects that affect various agricultural crops, including soybeans (De Freitas Bueno et al., 2011; Campos-Soldini et al., 2021; Overton et al., 2021). FAW can cause significant yield losses in soybean, especially at post-bloom stages, where intervention thresholds have been reported at 25% defoliation, compared to 50% at pre-bloom (Overton et al., 2021). In contrast, no established thresholds have been reported for BB. Additionally, Cercospora kikuchii (Tak. Matsumoto and Tomoy.) MW Gardner, Cercospora sojina K Hara (Mycosphaerellales: Mycosphaerellaceae), and Sclerotium rolfsii Sacc. (Amylocorticiales: Atheliaceae) are phytopathogenic fungi responsible for various diseases in soybean (Barro et al., 2023; Billah et al., 2017; Bhamra and Borah, 2022; Hartman et al., 1999; Sautua et al., 2019). Although soybean yield losses caused by these pathogens are difficult to estimate, as they, along with other pathogens, are part of the “late-season soybean diseases” (LSD). Collectively, these diseases account for an average of 10% of annual losses, but can reach up to 30%, depending on environmental conditions (Carmona et al., 2016). In Argentina, it was estimated that damage caused by C. kikuchii reduced soybean crop yields by 11% in 2018 and 2019 (Lavilla and Ivancovich, 2021). Consequently, farmers often turn to synthetic pesticides to mitigate these issues. These synthetic pesticides can be harmful to both human and environmental health, especially when used excessively or inappropriately (Alaoui et al., 2024; Aparicio and De Gerónimo, 2024; Rani et al., 2021). Therefore, it is essential to seek and promote new tools that facilitate the more sustainable control of these pests and diseases.

Eucalyptol (1, 8-cineole) is a monoterpene oxide comprising up to 85% of the total essential oils extracted from eucalyptus species (Campos and Berteina-Raboin, 2022). It is also present in essential oils from rosemary (Salvia rosmarinus Spenn.), lavender (Lavandula sp), and laurel (Laurus nobilis L.), albeit in smaller proportions (Borges et al., 2019; Cavanagh and Wilkinson, 2002; Chahal et al., 2017). Currently, there is increasing interest in eucalyptol, not only in the pharmaceutical and cosmetic industries (Cai et al., 2021; Hoch et al., 2023) but also in agriculture. This interest in eucalyptol stems from its notable toxicity against various pest insects and phytopathogenic fungi (Jiang et al., 2020; Tahiri et al., 2022; Tripathi and Mishra, 2016), coupled with its facile biodegradability and minimal impact on the environmental and human health (Batish et al., 2008).

So far, the potential of eucalyptol as a prospective active compound in biopesticide formulations for controlling the mentioned insects and phytopathogenic fungi is still understudied. However, some studies have revealed that essential oils rich in eucalyptol exhibit pronounced toxicity against these insects and fungi (Sekhar et al., 2020; Usseglio et al., 2022; Wagner and Campos-Soldini, 2022; Wagner et al., 2021). Based on these considerations, we aim to pursue the following research objectives: i) evaluate the insecticidal and fungicidal activity of eucalyptol against the mentioned species of insect and fungi, and ii) investigate the possible phytotoxic effect of eucalyptol on soybean plants.

MATERIALS AND METHODS

Chemical compound

Eucalyptol (1, 8-cineole), characterized by its analytical-grade quality (99% purity), was obtained from Merck-Sigma-Aldrich®, Argentina, and is commercially available at http://www.sigmaaldrich.com/. Chlorpyrifos (10.5% w/v) (Huagro Hormix, Huagro SA, Argentina) and difenoconazole (25% w/v) (Janfry®, Gleba SA, Argentina) and 2, 4-D (66.9% w/v) (Enlist®,Corteva Agriscience™, Argentina).

Insects and fungi

BB adults were collected manually from their host plants (Salpichroa origanifolia (Lam.) Baill. and Amaranthus hybridus L.) located in the vicinity of soybean fields near Diamante, Argentina, during the spring period (October and November) of 2022. FAW larvae were acquired from the moth colony in the CICYTTP insectarium, Diamante, established in 2020. Both species were maintained in the laboratory under controlled conditions at 27 ± 1°C, 70 ± 5% relative humidity, and a light-dark photoperiod of 16/8 h. BB adults were feed with fresh chard leaves, while FAW larvae were nourished using an artificial diet based on chickpea flour and wheat germ (Murúa et al., 2003).

The fungi C. kikuchii (strain NRBC 6713), C. sojina (strain NRBC 6715), and S. rolfsii (strain CCC 143-2018), were sourced from microbial collections affiliated with the Facultad de Bioquímica y Ciencias Biológicas at the Universidad Nacional del Litoral, Argentina, and the Centro de Referencia de Micología (CEREMIC) at the Universidad Nacional de Rosario, Argentina.

Insecticidal activity

The fumigant insecticidal activity of eucalyptol was evaluated following the protocol outlined by Baghouz et al. (2024), with slight adaptations. Briefly, groups of five insects (BB adults or FAW 1st instar larvae) were placed in 127 mL glass vials fitted with rubber lids. A 1 cm² Whatman filter paper disk was affixed to the underside of each rubber lid. The filter paper disks were impregnated with varying aliquots of pure eucalyptol, using an automatic pipette, to achieve concentrations of 19.7, 27.6, 35.4, 47.2, and 78.7 µL/L air (for experiments with BB) and 3.1, 6.3, 9.4, 12.6, and 19.7 µL/L air (for experiments with FAW). To support the filter paper on the lid and prevent direct contact of the insects with eucalyptol, a porous fabric mesh was used between the lids and the vials. To prevent vapour escape, the vials were hermetically sealed with Parafilm. Negative controls only contained a filter paper disk free of chemical substances, while positive controls incorporated a filter paper disk with chlorpyrifos at equivalent concentrations to those used with eucalyptol in both species. Each treatment was replicated five times under controlled conditions at a temperature of 27 ± 1°C and a light-dark photoperiod of 16/8 h. Each replication was conducted on different days. Mortality was recorded after 6 h of exposure, for BB and 24 h, for FAW. Insects were deemed dead if they remained motionless in response to stimuli provided by entomological brushes and forceps.

Fungicidal activity

The fungicidal activity of eucalyptol against C. kikuchii, C. sojina, or S. rolfsii was evaluated using the disc diffusion method, as described by Sequín et al. (2023), with some adaptations. Fungal hyphal suspensions were obtained by carefully collecting mycelium from 7-day-old colonies of C. kikuchii, C. sojina, or S. rolfsii grown on PDA (Potato Dextrose Agar). The hyphal fragments in each suspension underwent microbiological surface quantification and were subsequently adjusted to a concentration ranging from 4.0 × 10² to 4.3 × 10³ CFU/mL. Following this, 100 µL of each suspension was inoculated at the centre of a 9 cm diameter Petri dish containing 10 mL of YMDA (4 g/L yeast extract, 4 g/L malt extract, 10 g/L dextrose, 15 g/L agar), ensuring even distribution across the medium surface.

Sterile 5 mm diameter Whatman N^o 4 filter paper discs were impregnated with 5, 2.5, and 1 µL of eucalyptol per disc, plus 5 µL of dimethyl sulfoxide (DMSO). Negative controls consisted solely of discs saturated with 5 µL of DMSO per disc, while positive controls contained 5 µL of difenoconazole (concentration: 0.2 µg of a.i for µL) from a commercial source, which was used as a positive control per disc. Subsequently, the impregnated discs were placed on the surface of the PDA-inoculated Petri dishes. The Petri dishes were flipped and incubated in an oven at 25 ± 1°C, maintaining a 16/8 h light-dark cycle for a duration of 7 days. Each treatment was replicated four times on different days. Mycelial inhibition halo diameter was measured at the experiment’s conclusion using a digital caliper, values expressed in millimetres (mm).

Phytotoxic activity

The potential phytotoxic effect of eucalyptol on soybean was evaluated, following a protocol similar to that of the International Seed Testing Association (1976), but with slight modifications. Briefly, single soybean seeds were planted inside plastic boxes containing a 2 cm-thick layer of sterilized sand (weight: 30 g). Each sand layer was treated with a 3 mL solution of eucalyptol (concentration: 1,150 µg/mL) for the experimental samples, or distilled water for negative controls, or 2, 4-D (1.25 µg/mL) for positive controls. In all cases, distilled water with 1% v/v Tween 20 as diluent was used.

Each box with its soybean seed was considered one replicate, totalling 12 replicates per treatment. The boxes were hermetically sealed with a lid and placed in a germination chamber at a constant temperature of 25 ± 1°C, with a photoperiod of 16/8 h light-dark cycle for six days. At the end of this period, the hypocotyl and radicle of each seedling were measured using a digital caliper. The dry weight of each seedling was also determined after dehydrating them in an oven at 50°C for 3 days until a constant weight was achieved.

Statistical analysis

For BB and FAW experiments, lethal concentration doses producing 50% (LC₅₀) and 90% (LC₉₀) mortality were determined using Probit analysis (Finney, 1971) with POLO-PLUS Software (LeOra Software, 2002–2014). Significant differences between LC₅₀ and LC90 values were considered when the 95% confidence limits did not overlap. Insecticidal, fungicidal and phytotoxic activity were assessed using the Kruskal-Wallis test, followed by a Conover test for post hoc comparisons (Conover, 1999), utilizing InfoStat version 2018 statistical software, and with α = 0.05.

RESULTS

Insecticidal activity

Figure 1 illustrates the mortality percentages caused by the fumigant action of different eucalyptol concentrations against FAW and BB. Table 1 summarises the calculated LC₅₀ and LC₉₀ values for eucalyptol and chlorpyrifos (positive control) against both species. Eucalyptol exhibited significant fumigant insecticidal activity in a concentration-dependent manner against FAW 1st instar larvae (H = 24.61; df = 5; p < 0.05) and BB adults (H = 22.33; df = 5; p < 0.05). Median mortality reached 100% at concentrations equal to or higher than 9.4 µL/L air for FAW and 47.2 µL/L air for BB, respectively. The calculated LC_₅₀ values were 6.1 µL/L air for FAW and 34.6 µL/L air for BB. Chlorpyrifos (positive control) showed potent fumigant activity with LC50 values below 3.1 and 19.7 µL/L of air against FAW and BB, respectively (table 1). Negative controls showed no mortality in either species.

Fungicidal activity

Table 2 presents the median values of the mycelial inhibition halo diameters caused by the fungicidal action of eucalyptol at different concentrations against C. kikuchii, C. sojina, and S. rolfsii. Eucalyptol demonstrated significant fungicidal activity against C. kikuchii and C. sojina. Specifically, only mycotoxicity was observed at the highest evaluated concentration (5 µL/disk). At this concentration, mycelial inhibition halo diameters of 6.0 ± 0.0 mm and 10.0 ± 2.5 mm (median ± interquartile range) were observed for C. kikuchii and C. sojina, respectively. These values differed significantly from the negative controls, where no mycelial inhibition was evident (table 2). In contrast, the positive control (difenoconazole: 5 µl/disk), applied to both C. kikuchii and C. sojina, exhibited mycelial inhibition halo diameters significantly similar to the maximum eucalyptol concentration. However, neither eucalyptol nor the negative control nor difenoconazole inhibited the growth of S. rolfsii mycelium.

Insecticidal activity

To date, the insecticidal activity of eucalyptol through fumigant action against FAW larvae and BB has not been reported. However, studies have shown that, when applied topically, eucalyptol exhibits toxicity (59.6% mortality) against FAW at a dose of ≈ 0.01223 µL/larva (Bibiano et al., 2022). In contrast, at lower doses (≈ 0.00326 µL of eucalyptol/mg of larva), its toxicity is practically negligible (Niculau et al., 2013). Within the mode of application by fumigation, previous studies reveal that essential oils from lavender and rosemary, rich in eucalyptol (34.33 and 18.72%, respectively), demonstrate outstanding activity against BB, with LC50 values of 28.9 and 23.3 µl/L air, respectively (Wagner and Campos-Soldini, 2022; Wagner et al., 2021). Although this better activity than eucalyptol could be attributed to the addition or synergy with other compounds present in the oils as it was suggested in the case of Tenebrio molitor (L) (Coleoptera: Tenebrionidae) and Spodoptera littoralis Boisd (Lepidoptera: Noctuidae) (Lima et al., 2011; Pavela, 2014).

Eucalyptol also shows fumigant toxicity in other beetle pests, such as stored grain insects Sitophilus oryzae L (Coleoptera: Curculionidae), Tribolium castaneum Herbst, Tribolium confusum Jacquelin du Val (Coleoptera: Tenebrionidae), and Rhyzopertha dominica Fabricius (Coleoptera: Bostrichidae) (Lee et al., 2004; Abdelgaleil et al., 2009; Kheloul et al., 2023).

As observed in other insect species, the toxicity induced by eucalyptol in FAW and BB could be attributed to the inhibition of acetylcholinesterase (AChE) enzyme activity, which disrupts the insect’s nervous system, leading to paralysis and eventual death (Abdelgaleil et al., 2009; Picollo et al., 2008).

Fungicidal activity

While previous studies highlight the significant potential of eucalyptol as a fungicide against various phytopathogenic fungi (Morcia et al., 2012; Shukla et al., 2012; Oxenham et al., 2005; Dammak et al., 2019; Jiang et al., 2020), this study is the first to report its fungicidal activity against C. kikuchii and C. sojina. However, our research group previously determined that, at the same concentration of 5 µl/disk, the essential oil extracted from lavender, rich in eucalyptol (34.33%), exhibits potent fungicidal activity against C. kikuchii and C. sojina, with mycelial inhibition halos of 34.0 and 29.5 mm, respectively (Wagner et al., 2021). This indicates a fungicidal activity much superior of the natural oil to that observed for pure eucalyptol. This enhanced activity is likely attributed to additive or synergistic effects with other major components present in the essential oil (Hassan et al., 2020; Yan et al., 2021).

On the contrary, in our experiments, eucalyptol does not exert a significant inhibitory effect on the mycelial growth of S. rolfsii. These results contradict findings by Kottearachchi et al. (2012), who report 100% inhibition of S. rolfsii mycelial growth when treated with high concentrations of eucalyptol (0.5 and 1.5%). However, the same authors note that at lower concentrations, the inhibition percentage decreases to less than 30%.

It is well-established that many essential oils, rich in terpenes, possess the ability to induce alterations in the fungal cell wall, plasma membrane, and mitochondria, thereby substantiating their toxicity (Kishore et al., 2007; Pawar and Thaker, 2006). Indeed, toxicity studies conducted against the phytopathogenic fungus Botrytis cinerea confirm the detrimental effects of eucalyptol on the organelles of this fungus’s cells (Yu et al., 2015). It is plausible that the observed mycotoxicity of eucalyptol against C. kikuchii and C. sojina may be attributed to some of these reasons.

Phytotoxicity

Previous studies have underscored the strong phytotoxicity of eucalyptol against various plant species as lettuce (Qiu et al., 2010), annual ryegrass, radish (Barton et al., 2014), redroot amaranth and annual bluegrass (Shao et al., 2018; Zhou et al., 2019), our preliminary findings suggest that even at high concentrations, eucalyptol is not phytotoxic to soybean seedlings. Consistent with our study on the herbicidal effects of eucalyptol, Vaughn and Spencer (1993), using a similar methodology,

Phytotoxic activity

Figure 2 shows the phytotoxic effect caused by eucalyptol on the radicle growth, hypocotyl growth, and dry weight of soybean seedlings. Eucalyptol at 1,150 µg/mL (≈ 1,249 µL/L) exhibited no phytotoxic activity on soybeans despite even at a concentration 1 × 10³ times higher 2, 4-D (positive control: 1.25 µg/mL). In contrast, 2, 4-D demonstrated significant phytotoxicity, as evidenced by a significant reduction in both radicle length growth (H = 15.17; df = 2; p < 0.05) and seedling dry weight (H = 7.09; df = 2; p < 0.05). However, hypocotyl growth remained unaffected by both eucalyptol and 2, 4-D.

DISCUSSION

In general, eucalyptol exhibited fumigant insecticidal activity against FAW 1st instar larvae and BB adults, as well as fungicidal activity against C. kikuchii and C. sojina. Importantly, eucalyptol showed no phytotoxic effects on soybean.

Insecticidal activity

To date, the insecticidal activity of eucalyptol through fumigant action against FAW larvae and BB has not been reported. However, studies have shown that, when applied topically, eucalyptol exhibits toxicity (59.6% mortality) against FAW at a dose of ≈ 0.01223 µL/larva (Bibiano et al., 2022). In contrast, at lower doses (≈ 0.00326 µL of eucalyptol/mg of larva), its toxicity is practically negligible (Niculau et al., 2013). Within the mode of application by fumigation, previous studies reveal that essential oils from lavender and rosemary, rich in eucalyptol (34.33 and 18.72%, respectively), demonstrate outstanding activity against BB, with LC₅₀ values of 28.9 and 23.3 µl/L air, respectively (Wagner and Campos-Soldini, 2022; Wagner et al., 2021). Although this better activity than eucalyptol could be attributed to the addition or synergy with other compounds present in the oils as it was suggested in the case of Tenebrio molitor (L) (Coleoptera: Tenebrionidae) and Spodoptera littoralis Boisd (Lepidoptera: Noctuidae) (Lima et al., 2011; Pavela, 2014).

Eucalyptol also shows fumigant toxicity in other beetle pests, such as stored grain insects Sitophilus oryzae L (Coleoptera: Curculionidae), Tribolium castaneum Herbst, Tribolium confusum Jacquelin du Val (Coleoptera: Tenebrionidae), and Rhyzopertha dominica Fabricius (Coleoptera: Bostrichidae) (Lee et al., 2004; Abdelgaleil et al., 2009; Kheloul et al., 2023).

As observed in other insect species, the toxicity induced by eucalyptol in FAW and BB could be attributed to the inhibition of acetylcholinesterase (AChE) enzyme activity, which disrupts the insect’s nervous system, leading to paralysis and eventual death (Abdelgaleil et al., 2009; Picollo et al., 2008).

Fungicidal activity

While previous studies highlight the significant potential of eucalyptol as a fungicide against various phytopathogenic fungi (Morcia et al., 2012; Shukla et al., 2012; Oxenham et al., 2005; Dammak et al., 2019; Jiang et al., 2020), this study is the first to report its fungicidal activity against C. kikuchii and C. sojina. However, our research group previously determined that, at the same concentration of 5 µl/disk, the essential oil extracted from lavender, rich in eucalyptol (34.33%), exhibits potent fungicidal activity against C. kikuchii and C. sojina, with mycelial inhibition halos of 34.0 and 29.5 mm, respectively (Wagner et al., 2021). This indicates a fungicidal activity much superior of the natural oil to that observed for pure eucalyptol. This enhanced activity is likely attributed to additive or synergistic effects with other major components present in the essential oil (Hassan et al., 2020; Yan et al., 2021).

On the contrary, in our experiments, eucalyptol does not exert a significant inhibitory effect on the mycelial growth of S. rolfsii. These results contradict findings by Kottearachchi et al. (2012), who report 100% inhibition of S. rolfsii mycelial growth when treated with high concentrations of eucalyptol (0.5 and 1.5%). However, the same authors note that at lower concentrations, the inhibition percentage decreases to less than 30%.

It is well-established that many essential oils, rich in terpenes, possess the ability to induce alterations in the fungal cell wall, plasma membrane, and mitochondria, thereby substantiating their toxicity (Kishore et al., 2007; Pawar and Thaker, 2006). Indeed, toxicity studies conducted against the phytopathogenic fungus Botrytis cinerea confirm the detrimental effects of eucalyptol on the organelles of this fungus’s cells (Yu et al., 2015). It is plausible that the observed mycotoxicity of eucalyptol against C. kikuchii and C. sojina may be attributed to some of these reasons.

Phytotoxicity

Previous studies have underscored the strong phytotoxicity of eucalyptol against various plant species as lettuce (Qiu et al., 2010), annual ryegrass, radish (Barton et al., 2014), redroot amaranth and annual bluegrass (Shao et al., 2018; Zhou et al., 2019), our preliminary findings suggest that even at high concentrations, eucalyptol is not phytotoxic to soybean seedlings. Consistent with our study on the herbicidal effects of eucalyptol, Vaughn and Spencer (1993), using a similar methodology,

observed that this terpene does not exhibit significant phytotoxicity in soybean seedlings.

It is acknowledged that the phytotoxicity of eucalyptol in other plant species, such as Arabidopsis, potato and onion, is attributed to various causes, such as disruptions in microtubule organization and the inhibition of key processes like mitochondrial respiration, mitosis, and phytohormone production, leading to a negative impact on plant development and growth (Baskin et al., 2004; Verdeguer et al., 2020). Nevertheless, it is conceivable that only very high concentrations of eucalyptol may be detrimental to soybean plants at the seedling stage, opening prospects for its future application in protecting this crop.

CONCLUSIONS

The protection of soybean crops against pest insects and phytopathogenic fungi within the framework of Integrated Pest Management (IPM), based on methods like biological control, planting resistant cultivars, and using biopesticides, has sharply declined in recent decades (Bueno et al., 2023; Bueno et al., 2021; Panizzi, 2013). This decline is primarily attributed to the prevalent use of synthetic pesticides as the main control method, despite the well-known adverse impacts on the environmental and human health. Our findings indicate that eucalyptol has notable potential as an active ingredient for future biopesticide formulations, aiming to reduce, at least partially, the use of synthetic pesticides in soybean cultivation. This potential is primarily based on its insecticidal and fungicidal properties found in our studies. However, as with essential oils, its possible high volatility and rapid degradation, induced by exposure to air, sunlight, moisture, and high temperatures, could significantly reduce its effectiveness. Therefore, the application of eucalyptol may face significant limitations, requiring more frequent and higher quantities of application to the crop, thus increasing costs. These stability issues could be addressed through the implementation of formulations based on nanoencapsulation, which protect the compounds from adverse environmental factors, thereby improving their stability and efficacy (Giunti et al., 2021; Campolo et al., 2018; Gupta et al., 2023; Šunjka and Mechora, 2022). Therefore, we believe further studies are needed to evaluate the economic feasibility and applicability of eucalyptol in large-scale cultivation areas.

Acknowledgments

ACKNOWLEDGMENTS

The authors express their sincere gratitude to the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina) and the Facultad de Ciencia y Tecnología de la Universidad Autónoma de Entre Ríos (FCyT-UADER, Argentina).

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