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Agrobacterium tumefaciens C58 presence affects Bacillus velezensis 32a ecological fitness in the tomato rhizosphere Full text
2020
Abdallah, D. B. | Krier, F. | Jacques, Philippe | Tounsi, S. | Frikha-Gargouri, O.
peer reviewed | The persistence of pathogenic Agrobacterium strains as soil-associated saprophytes may cause an inconsistency in the efficacy of the biocontrol inoculants under field condition. The study of the interaction occurring in the rhizosphere between the beneficial and the pathogenic microbes is thus interesting for the development of effective biopesticides for the management of crown gall disease. However, very little is still known about the influence of these complex interactions on the biocontrol determinants of beneficial bacteria, especially Bacillus strains. This study aimed to evaluate the effect of the soil borne pathogen Agrobacterium tumefaciens C58 on root colonization and lipopeptide production by Bacillus velezensis strain 32a during interaction with tomato plants. Results show that the presence of A. tumefaciens C58 positively impacted the root colonization level of the Bacillus strain. However, negative impact on surfactin production was observed in Agrobacterium-treated seedling, compared with control. Further investigation suggests that these modulations are due to a modified tomato root exudate composition during the tripartite interaction. Thus, this work contributes to enhance the knowledge on the impact of interspecies interaction on the ecological fitness of Bacillus cells living in the rhizosphere. © 2020, Springer-Verlag GmbH Germany, part of Springer Nature.
Show more [+] Less [-]Two low-toxic Klebsiella pneumoniae strains from gut of black soldier fly Hermetia illucens are multi-resistance to sulfonamides and cadmium Full text
2022
Shi, Zhihui | Zhang, Jie | Jiang, Yijie | Wen, Yiting | Gao, Zhenghui | Deng, Wenhui | Yin, Yumeng | Zhu, Fen
In recent years, pollution of antibiotics and heavy metal has often been reported in organic wastes. Saprophytic insects have been recorded as biological control agents in organic waste management. During organic waste conversion, the intestinal bacteria of the saprophytic insects play an important role in digestion, physiology, immunity and prevention of pathogen colonization. Black soldier fly (BSF) Hermetia illucens has been widely used as saprophytic insects and showed tolerance to sulfonamides (SAs) and cadmium (Cd). Diversity and changes in gut microbiota of black soldier fly larvae (BSFL) were evaluated through 16S rRNA high-throughput sequencing, and a decrease in diversity of gut microbiota along with an increase in SAs stress was recorded. Major members identified were Actinomycetaceae, Enterobacteriaceae, and Enterococcaceae. And fourteen multi-resistance Klebsiella pneumoniae strains were isolated. Two strains BSFL7-B-5 (from middle midgut of 7-day BSFL) and BSFL11-C-1 (from posterior midgut of 11-day BSFL) were found to be low-toxic and multi-resistance. The adsorption rate of SAs in 5 mg/kg solutions by these two strains reached 65.2% and 61.6%, respectively. Adsorption rate of Cd in 20 mg/L solutions was 77.2% for BSFL7-B-5. The strain BSFL11-C-1 showed higher than 70% adsorption rates of Cd in 20, 30 and 40 mg/L solutions. This study revealed that the presence of multi-resistance bacterial strains in the gut of BSFL helped the larvae against SAs or Cd stress. After determining how and where they are used, selected BSFL gut bacterial strains might be utilized in managing SAs or Cd contamination at suitable concentrations in the future.
Show more [+] Less [-]ZnO nanoparticles interfere with top-down effect of the protozoan paramecium on removing microcystis Full text
2022
Zhang, Lu | Yin, Wei | Shen, Siyi | Feng, Yuyun | Xu, Wenjie | Sun, Yunfei | Yang, Zhou
Under intensive human activity, sewage discharge causes eutrophication-driven cyanobacteria blooms as well as nanomaterial pollution. In biological control of harmful cyanobacteria, top-down effect of protozoan has great potentials for removing cyanobacterial populations, degrading cyanotoxins, and improving phytoplankton community. ZnO nanoparticles as a kind of emerging contaminants have attracted increasing attention because of wide application and their high bio-toxicity effects on reducing the ingestion of aquatic animals including Paramecium, thereby possibly disturbing top-down control of cyanobacteria. Therefore, this study investigated the effects of ZnO nanoparticles at environmental-relevant concentrations on the protozoan Paramecium removing toxic Microcystis. Results showed Paramecium effectively eliminated all the Microcystis, despite exposure to ZnO nanoparticles. However, their ingestion rate was significantly reduced at more than 0.1 mg L⁻¹ ZnO nanoparticles, thereby delaying Microcystis removal. Nevertheless, at 0.1 mg L⁻¹ ZnO nanoparticles, the time to Microcystis extinction decreased compared to the group without ZnO nanoparticles, because Microcystis populations were reduced under this circumstance, while ingestion rate of Paramecium was unaffected. Furthermore, ZnO nanoparticles obviously accumulated in food vacuoles of Paramecium, and the size of nanoparticles aggregates and zinc concentrations in Paramecium were increased with ZnO nanoparticles concentrations. At the end of experiment, these food vacuoles were not dissipated. Overall, these findings suggest that ZnO nanoparticles impair protozoan top-down effects through reducing Microcystis and ingestion rate as well as disturbing functions of their digestive organelles, and highlight the need to consider the interfering effects of environmental pollutants on cyanobacterial removal efficiency by protozoans in natural waters.
Show more [+] Less [-]Neonicotinoids from coated seeds toxic for honeydew-feeding biological control agents Full text
2021
Calvo-Agudo, Miguel | Dregni, Jonathan | González-Cabrera, Joel | Dicke, Marcel | Heimpel, George E. | Tena, Alejandro
Neonicotinoids from coated seeds toxic for honeydew-feeding biological control agents Full text
2021
Calvo-Agudo, Miguel | Dregni, Jonathan | González-Cabrera, Joel | Dicke, Marcel | Heimpel, George E. | Tena, Alejandro
Seed coating (‘seed treatment’) is the leading delivery method of neonicotinoid insecticides in major crops such as soybean, wheat, cotton and maize. However, this prophylactic use of neonicotinoids is widely discussed from the standpoint of environmental costs. Growing soybean plants from neonicotinoid-coated seeds in field, we demonstrate that soybean aphids (Aphis glycines) survived the treatment, and excreted honeydew containing neonicotinoids. Biochemical analyses demonstrated that honeydew excreted by the soybean aphid contained substantial concentrations of neonicotinoids even one month after sowing of the crop. Consuming this honeydew reduced the longevity of two biological control agents of the soybean aphid, the predatory midge Aphidoletes aphidimyza and the parasitic wasp Aphelinus certus. These results have important environmental and economic implications because honeydew is the main carbohydrate source for many beneficial insects in agricultural landscapes.
Show more [+] Less [-]Neonicotinoids from coated seeds toxic for honeydew-feeding biological control agents Full text
2021
Calvo-Agudo, Miguel | Dregni, Jonathan | González-Cabrera, Joel | Dicke, Marcel | Heimpel, George E. | Tena, Alejandro
Seed coating (‘seed treatment’) is the leading delivery method of neonicotinoid insecticides in major crops such as soybean, wheat, cotton and maize. However, this prophylactic use of neonicotinoids is widely discussed from the standpoint of environmental costs. Growing soybean plants from neonicotinoid-coated seeds in field, we demonstrate that soybean aphids (Aphis glycines) survived the treatment, and excreted honeydew containing neonicotinoids. Biochemical analyses demonstrated that honeydew excreted by the soybean aphid contained substantial concentrations of neonicotinoids even one month after sowing of the crop. Consuming this honeydew reduced the longevity of two biological control agents of the soybean aphid, the predatory midge Aphidoletes aphidimyza and the parasitic wasp Aphelinus certus. These results have important environmental and economic implications because honeydew is the main carbohydrate source for many beneficial insects in agricultural landscapes.
Show more [+] Less [-]Neonicotinoids from coated seeds toxic for honeydew-feeding biological control agents Full text
2021
Calvo-Agudo, Miguel | Dregni, Jonathan | González-Cabrera, Joel | Dicke, Marcel | Heimpel, George E. | Tena, Alejandro
Seed coating (‘seed treatment’) is the leading delivery method of neonicotinoid insecticides in major crops such as soybean, wheat, cotton and maize. However, this prophylactic use of neonicotinoids is widely discussed from the standpoint of environmental costs. Growing soybean plants from neonicotinoid-coated seeds in field, we demonstrate that soybean aphids (Aphis glycines) survived the treatment, and excreted honeydew containing neonicotinoids. Biochemical analyses demonstrated that honeydew excreted by the soybean aphid contained substantial concentrations of neonicotinoids even one month after sowing of the crop. Consuming this honeydew reduced the longevity of two biological control agents of the soybean aphid, the predatory midge Aphidoletes aphidimyza and the parasitic wasp Aphelinus certus. These results have important environmental and economic implications because honeydew is the main carbohydrate source for many beneficial insects in agricultural landscapes.
Show more [+] Less [-]Transgenic insect-resistant Bt cotton expressing Cry1Ac/CpTI does not affect the mirid bug Apolygus lucorum Full text
2020
Niu, Lin | Liu, Fang | Zhang, Shuai | Luo, Junyu | Zhang, Lijuan | Ji, Jichao | Gao, Xueke | Ma, Weihua | Cui, Jinjie
Common varieties of genetically modified (GM) cotton increasingly display insect-resistant properties via expression of bacterial-derived toxins from Bacillus thuringiensis (Bt). This necessitates a deeper understanding of the possible effects of these crops on non-target insects. The mirid bug Apolygus lucorum is a major pest in cotton production in China, however, the effect of GM cotton on this non-target species is currently virtually unknown. This insect is exposed to these transgenic plants by consuming genetically modified (GM) leaves. In this study, laboratory experiments were conducted to assess the toxicity of CCRI41 and CCRI45, (genetically modified cotton varieties which express the toxins Cry1Ac and CpTI (Cowpea Trypsin Inhibitor)) on nymphs and adults of A. lucorum. There was no detectable increase in mortality after A. lucorum fed on GM cotton leaves for 20 days. While we detected trace amounts of Cry1Ac proteins in both A. lucorum nymphs and adults (<10 ng/g fresh weight), the expression of genes related to detoxification did not detectably differ from those feeding on non-GM cotton. Our binding assays did not show Cry1Ac binding to receptors on the midgut brush border membrane from either A. lucorum nymphs or adults. Our findings collectively indicate that feeding on leaves of the GM cotton varieties CCRI41 and CCRI45 have few toxic effects on A. lucorum.
Show more [+] Less [-]IPM-recommended insecticides harm beneficial insects through contaminated honeydew Full text
2020
Calvo-Agudo, Miguel | González-Cabrera, Joel | Sadutto, Daniele | Picó, Yolanda | Urbaneja, Alberto | Dicke, Marcel | Tena, Alejandro
IPM-recommended insecticides harm beneficial insects through contaminated honeydew Full text
2020
Calvo-Agudo, Miguel | González-Cabrera, Joel | Sadutto, Daniele | Picó, Yolanda | Urbaneja, Alberto | Dicke, Marcel | Tena, Alejandro
The use of some systemic insecticides has been banned in Europe because they are toxic to beneficial insects when these feed on nectar. A recent study shows that systemic insecticides can also kill beneficial insects when they feed on honeydew. Honeydew is the sugar-rich excretion of hemipterans and is the most abundant carbohydrate source for beneficial insects such as pollinators and biological control agents in agroecosystems. Here, we investigated whether the toxicity of contaminated honeydew depends on i) the hemipteran species that excretes the honeydew; ii) the active ingredient, and iii) the beneficial insect that feeds on it. HPLC-MS/MS analyses demonstrated that the systemic insecticides pymetrozine and flonicamid, which are commonly used in Integrated Pest Management programs, were present in honeydew excreted by the mealybug Planococcus citri. However, only pymetrozine was detected in honeydew excreted by the whitefly Aleurothixus floccosus. Toxicological studies demonstrated that honeydew excreted by mealybugs feeding on trees treated either with flonicamid or pymetrozine increased the mortality of the hoverfly Sphaerophoria rueppellii, but did not affect the parasitic wasp Anagyrusvladimiri. Honeydew contaminated with flonicamid was more toxic for the hoverfly than that contaminated with pymetrozine. Collectively, our data demonstrate that systemic insecticides commonly used in IPM programs can contaminate honeydew and kill beneficial insects that feed on it, with their toxicity being dependent on the active ingredient and hemipteran species that excretes the honeydew.
Show more [+] Less [-]IPM-recommended insecticides harm beneficial insects through contaminated honeydew
2020
Calvo-Agudo, Miguel | González-Cabrera, Joel | Sadutto, Daniele | Picó, Yolanda | Urbaneja, Alberto | Dicke, Marcel | Tena, Alejandro
The use of some systemic insecticides has been banned in Europe because they are toxic to beneficial insects when these feed on nectar. A recent study shows that systemic insecticides can also kill beneficial insects when they feed on honeydew. Honeydew is the sugar-rich excretion of hemipterans and is the most abundant carbohydrate source for beneficial insects such as pollinators and biological control agents in agroecosystems. Here, we investigated whether the toxicity of contaminated honeydew depends on i) the hemipteran species that excretes the honeydew; ii) the active ingredient, and iii) the beneficial insect that feeds on it. HPLC-MS/MS analyses demonstrated that the systemic insecticides pymetrozine and flonicamid, which are commonly used in Integrated Pest Management programs, were present in honeydew excreted by the mealybug Planococcus citri. However, only pymetrozine was detected in honeydew excreted by the whitefly Aleurothixus floccosus. Toxicological studies demonstrated that honeydew excreted by mealybugs feeding on trees treated either with flonicamid or pymetrozine increased the mortality of the hoverfly Sphaerophoria rueppellii, but did not affect the parasitic wasp Anagyrus vladimiri. Honeydew contaminated with flonicamid was more toxic for the hoverfly than that contaminated with pymetrozine. Collectively, our data demonstrate that systemic insecticides commonly used in IPM programs can contaminate honeydew and kill beneficial insects that feed on it, with their toxicity being dependent on the active ingredient and hemipteran species that excretes the honeydew. Insecticides recommended in Integrated Pest Management programs reach honeydew and kill beneficial insects that feed on it.
Show more [+] Less [-]IPM-recommended insecticides harm beneficial insects through contaminated honeydew Full text
2020
Calvo-Agudo, Miguel | González-Cabrera, Joel | Sadutto, Daniele | Picó, Yolanda | Urbaneja, Alberto | Dicke, Marcel | Tena, Alejandro
The use of some systemic insecticides has been banned in Europe because they are toxic to beneficial insects when these feed on nectar. A recent study shows that systemic insecticides can also kill beneficial insects when they feed on honeydew. Honeydew is the sugar-rich excretion of hemipterans and is the most abundant carbohydrate source for beneficial insects such as pollinators and biological control agents in agroecosystems. Here, we investigated whether the toxicity of contaminated honeydew depends on i) the hemipteran species that excretes the honeydew; ii) the active ingredient, and iii) the beneficial insect that feeds on it. HPLC-MS/MS analyses demonstrated that the systemic insecticides pymetrozine and flonicamid, which are commonly used in Integrated Pest Management programs, were present in honeydew excreted by the mealybug Planococcus citri. However, only pymetrozine was detected in honeydew excreted by the whitefly Aleurothixus floccosus. Toxicological studies demonstrated that honeydew excreted by mealybugs feeding on trees treated either with flonicamid or pymetrozine increased the mortality of the hoverfly Sphaerophoria rueppellii, but did not affect the parasitic wasp Anagyrus vladimiri. Honeydew contaminated with flonicamid was more toxic for the hoverfly than that contaminated with pymetrozine. Collectively, our data demonstrate that systemic insecticides commonly used in IPM programs can contaminate honeydew and kill beneficial insects that feed on it, with their toxicity being dependent on the active ingredient and hemipteran species that excretes the honeydew.
Show more [+] Less [-]IPM-recommended insecticides harm beneficial insects through contaminated honeydew Full text
2020
Calvo-Agudo, Miguel | González-Cabrera, Joel | Sadutto, D. | Picó, Yolanda | Urbaneja, Alberto | Dicke, Marcel | Tena, Alejandro | CSIC - Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA) | Generalitat Valenciana | Ministerio de Economía y Competitividad (España)
The use of some systemic insecticides has been banned in Europe because they are toxic to beneficial insects when these feed on nectar. A recent study shows that systemic insecticides can also kill beneficial insects when they feed on honeydew. Honeydew is the sugar-rich excretion of hemipterans and is the most abundant carbohydrate source for beneficial insects such as pollinators and biological control agents in agroecosystems. Here, we investigated whether the toxicity of contaminated honeydew depends on i) the hemipteran species that excretes the honeydew; ii) the active ingredient, and iii) the beneficial insect that feeds on it. HPLC-MS/MS analyses demonstrated that the systemic insecticides pymetrozine and flonicamid, which are commonly used in Integrated Pest Management programs, were present in honeydew excreted by the mealybug Planococcus citri. However, only pymetrozine was detected in honeydew excreted by the whitefly Aleurothixus floccosus. Toxicological studies demonstrated that honeydew excreted by mealybugs feeding on trees treated either with flonicamid or pymetrozine increased the mortality of the hoverfly Sphaerophoria rueppellii, but did not affect the parasitic wasp Anagyrus vladimiri. Honeydew contaminated with flonicamid was more toxic for the hoverfly than that contaminated with pymetrozine. Collectively, our data demonstrate that systemic insecticides commonly used in IPM programs can contaminate honeydew and kill beneficial insects that feed on it, with their toxicity being dependent on the active ingredient and hemipteran species that excretes the honeydew. | This research was partially funded by an Instituto Nacional de Investigaciones Agrarias (INIA) (Project RTA2017-00095) and the Conselleria d’Agricultura, Pesca i Alimentació de la Generalitat Valenciana. J.G.C was supported by the Spanish Ministry of Economy and Competitiveness, Ramón y Cajal Program (RYC-2013-13834) and M.C.A was recipient of grant from INIA (CPD2016-0085).
Show more [+] Less [-]IPM-recommended insecticides harm beneficial insects through contaminated honeydew Full text
2020
Calvo-Agudo, Miguel | González-Cabrera, Joel | Sadutto, Daniele | Picó, Yolanda | Urbaneja, Alberto | Dicke, Marcel | Tena, Alejandro
The use of some systemic insecticides has been banned in Europe because they are toxic to beneficial insects when these feed on nectar. A recent study shows that systemic insecticides can also kill beneficial insects when they feed on honeydew. Honeydew is the sugar-rich excretion of hemipterans and is the most abundant carbohydrate source for beneficial insects such as pollinators and biological control agents in agroecosystems. Here, we investigated whether the toxicity of contaminated honeydew depends on i) the hemipteran species that excretes the honeydew; ii) the active ingredient, and iii) the beneficial insect that feeds on it. HPLC-MS/MS analyses demonstrated that the systemic insecticides pymetrozine and flonicamid, which are commonly used in Integrated Pest Management programs, were present in honeydew excreted by the mealybug Planococcus citri. However, only pymetrozine was detected in honeydew excreted by the whitefly Aleurothixus floccosus. Toxicological studies demonstrated that honeydew excreted by mealybugs feeding on trees treated either with flonicamid or pymetrozine increased the mortality of the hoverfly Sphaerophoria rueppellii, but did not affect the parasitic wasp Anagyrus vladimiri. Honeydew contaminated with flonicamid was more toxic for the hoverfly than that contaminated with pymetrozine. Collectively, our data demonstrate that systemic insecticides commonly used in IPM programs can contaminate honeydew and kill beneficial insects that feed on it, with their toxicity being dependent on the active ingredient and hemipteran species that excretes the honeydew. Insecticides recommended in Integrated Pest Management programs reach honeydew and kill beneficial insects that feed on it.
Show more [+] Less [-]Plant and fungal biodiversity from metal mine wastes under remediation at Zimapan, Hidalgo, Mexico Full text
2010
Pilar Ortega-Larrocea, María del | Xoconostle-Cázares, Beatriz | Maldonado-Mendoza, Egnacio E. | Carrillo González, Rogelio | Hernández-Hernández, Jani | Díaz Garduño, Margarita | López-Meyer, Melina | Gómez-Flores, Lydia | González-Chávez, Ma. del Carmen A.
Plant establishment, presence of arbuscular mycorrhizal fungi (AMF) and other rhizospheric fungi were studied in mine wastes from Zimapan, Hidalgo state, Mexico, using a holistic approach. Two long-term afforested and three non-afforested mine tailings were included in this research. Fifty-six plant species belonging to 29 families were successfully established on the afforested sites, while unmanaged tailings had only a few native plant species colonizing the surrounding soils. Almost all plant roots collected were associated to AMF in these sites. The genus Glomus was the most abundant AMF species found in their rhizosphere; however, the Acaulospora genus was also observed. Other rhizospheric fungi were identified by 18S rDNA sequencing analysis. Their role in these substrates, i.e. biocontrol, pollutant- and organic matter-degradation, and aides that increase plant metal tolerance is discussed. Our results advance the understanding of fungal diversity in sites polluted with metals and present alternative plants for remediation use.
Show more [+] Less [-]Bio-activation of soil with beneficial microbes after soil fumigation reduces soil-borne pathogens and increases tomato yield Full text
2021
Cheng, Hongyan | Zhang, Daqi | Ren, Lirui | Song, Zhaoxin | Li, Qingjie | Wu, Jiajia | Fang, Wensheng | Huang, Bin | Yan, Dongdong | Li, Yuan | Wang, Qiuxia | Cao, Aocheng
Soil-borne diseases have become increasingly problematic for farmers producing crops intensively under protected agriculture. Although soil fumigants are convenient and effective for minimizing the impact of soil-borne disease, they are most often detrimental to beneficial soil microorganisms. Previous research showed that bio-activation of soil using biological control agents present in biofertilizers or organic fertilizers offered promise as a strategy for controlling soil-borne pathogens when the soil was bio-activated after fumigation. Our research sought to determine how bio-activation can selectively inhibit pathogens while promoting the recovery of beneficial microbes. We monitored changes in the soil’s physicochemical properties, its microbial community and reductions in soil-borne pathogens. We found that the population density of Fusarium and Phytophthora were significantly reduced and tomato yield was significantly increased when the soil was bio-activated. Soil pH and soil catalase activity were significantly increased, and the soil’s microbial community structure was changed, which may have enhanced the soil’s ability to reduce Fusarium and Phytophthora. Our results showed that soil microbial diversity and relative abundance of beneficial microorganisms (such as Sphingomonas, Bacillus, Mortierella and Trichoderma) increased shortly after bio-activation of the soil, and were significantly and positively correlated with pathogen suppression. The reduction in pathogens may have been due to a combination of fumigation-fertilizer that reduced pathogens directly, or the indirect effect of an optimized soil microbiome that improved the soil’s non-biological factors (such as soil pH, fertility structure), enhanced the soil’s functional properties and increased tomato yield.
Show more [+] Less [-]Essential oil from Negramina (Siparuna guianensis) plants controls aphids without impairing survival and predatory abilities of non-target ladybeetles Full text
2019
Toledo, Pedro F.S. | Ferreira, Taciano P. | Bastos, Isabela M.A.S. | Resende, Sarah M. | Viteri Jumbo, Luis O. | Didonet, Julcemar | Andrade, Bruno S. | Melo, Tarcisio S. | Smagghe, Guy | Oliveira, Eugênio E. | Aguiar, Raimundo W.S.
Plant essential oils are regarded as interesting alternative tools to be integrated into the management of pest insects. However, as they generally consist of mixtures of numerous molecules, the physiological basis for their action is unresolved. Here, we evaluated the effects of essential oil of the Neotropical plant Siparuna guianensis Aubl., commonly known as Negramina, against an important pest insect: the green peach aphid Myzus persicae (Sulzer), and also in two non-target natural enemies: the ladybeetle predators Coleomegilla maculata (DeGeer) and Eriopis connexa (Germar). In addition, we conducted a computational docking analysis for predicting the physical interactions between the two Negramina essential oil major constituents: β-myrcene and 2-undocanone, and the transient receptor potential (TRP) channels as potential binding receptors in the aphid and ladybeetles. As the most important results, Negramina essential oil caused mortality in M. persicae aphids with an LC95 = 1.08 mg/cm2, and also significantly repelled the aphids at concentrations as low as 0.14 mg/cm2. Our computational docking analysis reinforced such selectivity actions as the Negramina essential oil major compounds (i.e., β-myrcene and 2-undocanone) bound to the TRP channels of M. persicae but not to ladybeetle-related TRP channels. Interestingly, the exposure to the Negramina essential oil did not affect the predatory abilities of C. maculata but increased the abilities of E. connexa to prey upon M. persicae. Collectively, our findings provided a physiological basis for the insecticidal and selectivity potential of Negramina essential oil, reinforcing its potential as a tool to be used in integrated pest control programs.
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