Insecticidal activity and restoration of piriproxifen action by monoterpenes on Aedes aegypti (Diptera: Culicidae)

Atividade inseticida e restauração da ação do piriproxifeno por monoterpenos sobre o Aedes aegypti (Diptera: Culicidae)

Abstract

The aim was to evaluate the insecticidal action and restoration of piriproxifen (PP) activity through the monoterpenes carveol and β-citronellol on Aedes aegypti. Eggs were placed to incubate in trays with distilled water and fish food to obtain larvae at the third instar (L3). Monoterpenes were used individually in four repetitions at doses of 6.2; 12.5; 25 and 50 µL. For activity restoration, three doses of 5.0; 6.2 and 8.0 µL were used, as well as PP dissolved in distilled water. Ae. aegypti larvae were evaluated at 24, 48, and 72 h after exposure. It was found that both carveol and β-citronellol showed insecticidal activities against Ae. aegypti. Regarding modulation, the two monoterpenes potentiated the activity of PP. In this sense, studies are needed to elucidate the molecular targets of these bioactive molecules, as well as to explore them in synergy with other compounds.

Keywords:
biological activities; vector control; secondary metabolites; dengue mosquito

Resumo

O objetivo foi avaliar a ação inseticida e restauração da atividade do piriproxifeno (PP) através dos monoterpenos carveol e β-citronelol sobre Aedes aegypti. Os ovos foram colocados para incubar em bandejas com água destilada e ração para peixes para obtenção de larvas de terceiro ínstar (L3). Os monoterpenos foram utilizados individualmente em quatro repetições nas doses de 6,2; 12,5; 25 e 50 µL. Na restauração da atividade foram utilizados três dosagens de 5,0, 6,2 e 8,0 µL, bem como, PP dissolvido em água destilada. As larvas de A. aegypti foram avaliadas em 24, 48 e 72 h após exposição. Verificou-se que tanto o carveol quanto o β-citronelol apresentaram atividades inseticidas contra Ae. aegypti. Quanto à modulação, os dois monoterpenos potencializaram a atividade do PP. Nesse sentido, são necessários estudos que elucidem os alvos moleculares dessas moléculas bioativas, bem como explorá-las em sinergia com outros compostos.

Palavras-chave:
atividades biológicas; controle de vetores; metabólitos secundários; mosquito da dengue

1. Introduction

Vector-borne diseases are currently considered one of the main contributors to the global disease burden, accounting for over 1 billion infections annually (Iwamura et al., 2020). Due to the high incidence of cases, there is a growing interest in innovating methods to prevent pathogen transmission (Li et al., 2020).

Among the main vectors responsible for the high rate of infections, Aedes aegypti (Linneaus, 1762) stands out, given its immense epidemiological importance as the primary vector for several arboviruses, including dengue, Zika, chikungunya, and yellow fever. It is a synanthropic and anthropophilic species, with a preference for and ease of proliferation in densely populated urban environments (Cavalli et al., 2019; Li et al., 2020).

The life cycle of Ae. aegypti comprises two main phases: aquatic and aerial, with all immature forms in water and adults being winged, undergoing complete metamorphosis (Lima et al., 2021). Its cycle is influenced by ambient temperature, food availability, and larval quantity in breeding sites (Silvério et al., 2020). As there are no specific treatments available for the arboviruses transmitted by it in government public health programs, reducing the population density of this vector has a significant impact on interrupting the transmission chain (Adhikari et al., 2022).

In Brazil, arboviruses are responsible for high rates of morbidity and mortality, the magnitude of which is a matter of global concern (Lima et al., 2021). This adversity poses a public health problem, both due to its incidence and prevalence and its potential complications (Nunes et al., 2022). As vector-borne infections, there has been an expansion of investments in vector control, but the measures used so far have limitations (Takagi et al., 2020).

Factors such as unplanned urban growth, along with its repercussions on infrastructure conditions, correlated with favorable climatic conditions and human mobility, favor mosquito proliferation while complicating efforts for confrontation, prevention, and control (Vanlerberghe et al., 2018).

In an attempt to prevent the spread of Ae. aegypti, the main method used for vector control is chemical, through the use of insecticides. However, excessive, constant, and prolonged use of insecticides in a certain mosquito population can have consequences, such as vector resistance, which is passed on to future generations. Thus, eradicating diseases transmitted by this vector proves to be quite difficult (Vargas et al., 2022; Azevedo et al., 2023; Cruz et al., 2024).

In this context, a rational strategy for chemical control should be implemented, based on detailed knowledge of the territorial distribution of the vector, associated with its susceptibility to different compounds belonging to distinct classes of insecticides, as well as the mechanisms involved in resistance selection, only then will it be possible to reduce vector infestation levels (Campos et al., 2020).

Discussions about the high levels of resistance of Ae. aegypti to the main classes of insecticides used in vector control have been widely disseminated, as this occurs through various molecular and genetic mechanisms. Therefore, it is important to reinforce the need for new alternative investments aimed at controlling the vector through other methods and action mechanisms that target more than one molecular target (Marques, 2020; Chiele et al., 2023).

Thus, the use of botanical insecticides has been expanded due to their promising potential based on their phytochemical composition and broad spectrum of action. They possess toxic properties against the various developmental stages of the Ae. aegypti life cycle (Leite and Bertotti, 2020). It is also worth mentioning that plant secondary metabolites have potent action regarding substance modulation, which stimulates research development in this field (Ferreira et al., 2019).

Among the substances with potential bioinsecticidal properties, the class of monoterpenes stands out, which has already shown significant results on Ae. aegypti with high mortality rates depending on the dosage and stage of the insect's life cycle (Khaleel et al., 2018; Silva et al., 2018a). However, specifically regarding the monoterpenes carveol and β-citronellol, there are no studies available in the scientific literature measuring their insecticidal activity on this vector, nor their ability to modulate substances, thus, there is a lack of knowledge about these phytochemicals.

In this context, the aim was to evaluate the insecticidal action and restoration of piriproxifen (PP) activity, a growth regulator, through the monoterpenes carveol and β-citronellol on Ae. Aegypti.

2. Materials and Methods

2.1. Egg acquisition

The eggs used in the experimental studies were donated by the dipteran breeding facility at the Laboratory of Chemical Ecology, Department of Fundamental Chemistry, Federal University of Pernambuco (UFPE).

2.2. Location of experimental studies

The research was conducted at the Entomology Laboratory (LEN), located at the Center for Agricultural Sciences and Biodiversity (CCAB) of the Federal University of Cariri (UFCA), Crato campus, Ceará, Brazil.

2.3. Obtaining Ae. Aegypti Larvae

Ae. aegypti eggs were placed to incubate in trays with distilled water and fish food to obtain larvae at the third instar (L3) in a Biochemical Oxygen Demand (B.O.D.) type climatic chamber for three days, with a temperature of (25 ± 2°C), relative air humidity (70 ± 10%), and a 12-hour photoperiod.

2.4. Insecticidal activity of monoterpenes on Ae. aegypti

Disposable cups were used, adding 25 mL of Dimethyl Sulfoxide (DMSO), 25 mL of distilled water, as well as the monoterpenes carveol and β-citronellol individually in four repetitions at doses of 6.2, 12.5, 25, and 50 µL. In each replication, 20 Ae. aegypti L3 larvae were added and incubated at a temperature of (25 ± 2°C), with a relative air humidity of (70 ± 10%) and a 12-hour photoperiod, in a B.O.D. type climatic chamber. Ae. aegypti larvae were evaluated at 24, 48, and 72 hours after exposure to the doses. During this specific period, mortality was assessed by the larvae's reaction to mechanical stimulation from a fine brush.

Negative control tests were also conducted, using distilled water, and positive control tests with the insecticide piriproxifen at a commercial dose of 0.001 g/L. All experiments were conducted in four repetitions to obtain greater confidence and precision in the results.

2.5. Restoration of piriproxifen action by monoterpenes

Disposable cups were used, adding 14.5 mL of distilled water, 14.5 mL of piriproxifen dissolved in distilled water at a dose of 0.0005 g/L, as well as the monoterpenes in three volumes: 5.0, 6.2, and 8.0 µL. These concentrations were selected considering that when used alone on Ae. aegypti, they had little or no efficiency in larval mortality.

In each replication, 20 Ae. aegypti L3 larvae were added and incubated at a temperature of (25 ± 2°C), with a relative air humidity of (70 ± 10%) and a 12-hour photoperiod, in a B.O.D. type climatic chamber. Ae. aegypti larvae were evaluated at 24, 48, and 72 hours after exposure to the substances. During this specific period, mortality was assessed by the larvae's reaction to mechanical stimulation from a fine brush. Positive and negative controls were conducted as described in the previous procedure, as well as the number of replications performed.

3. Results and Discussion

3.1. Insecticidal activity of monoterpenes

From the analysis of the data, it was evident that both studied monoterpenes exhibited insecticidal activity against Ae. aegypti, depending on the concentration and exposure period to the substances. These findings are in line with information available in the scientific literature. Furthermore, according to Silva et al. (2018b), the toxicity of different monoterpenes and behavioral changes in response to them also depend on the stage of the insect's life cycle, and they may prove to be efficient in all phases.

As observed in Table 1, it is possible to see that β-citronellol exhibits lower toxicity compared to carveol, as higher concentrations are required to achieve the same effect. This finding was evident both in the LC₅₀ and LC₉₀, and it may be associated with a greater efficiency of the latter in Ae. aegypti populations.

Table 1
Lethal concentration of monoterpenes on Ae. aegypti.

Lethal concentration	Carveol	β-citronellol
LC10	5.5 µL	4.5 µL
LC50	6.1 µL	7.6 µL
LC90	6.8 µL	12.9 µL
95% Confidence Interval

Specifically regarding carveol, it was observed that at concentrations of 6.2 and 12.5 µL, the efficiency of mortality increased as the exposure period to the treatments progressed. At this first concentration, even at the end of the 72-hour exposure, there was not 100% mortality. However, at the second mentioned concentration, 100% efficiency was achieved already at 48 hours of exposure. In contrast, at concentrations of 25 and 50 µL, 100% mortality was observed within 24 hours of exposure, demonstrating potent insecticidal activity even in a short exposure period (Figure 1).

Figure 1
Insecticidal activity of carveol against Ae. aegypti.

With regard to the action of carveol on Ae. aegypti, nothing was found in the scientific literature. However, its larvicidal activity, as well as in the present study, was also evidenced by Lee et al. (1997) when investigating it through a soil laboratory bioassay using Diabrotica virgifera virgifera Le Conte, known as the western corn rootworm. The research evaluated the efficiency of 34 monoterpenes and found that alcoholic and phenolic monoterpenoids such as carveol, citronellol, and thymol showed significantly more toxic effects than ketones and those with other functional groups.

Based on this principle, the structure-activity relationship of monoterpenes has been investigated to identify structural characteristics responsible for insecticidal activity. Pandey et al. (2013) describe that acetylation of the hydroxyl group, present even in carveol, generally increases the activity of monoterpenes. Thus, by identifying bioactive functional groups, it is possible to contribute to the improvement of the properties of these phytochemicals, as well as to favor the development of environmentally friendly compounds.

The literature also highlights that the presence of certain chemical groups in the carbon chain of monoterpenes can favor or impair their activity. Thus, conjugated double bonds and the presence of lipophilic groups potentiate their larvicidal activity against Ae. aegypti. On the other hand, the presence of heteroatoms in the basic hydrocarbon structure, as well as hydroxyl groups in the cyclic structure, result in a decrease in potency, probably due to increased polarity (Santos et al., 2011).

Another mechanism of action that may be related to the insecticidal activity of carveol concerns the inhibition of the enzyme acetylcholinesterase (AChE). In the study by Hung et al. (2022), for example, it was identified that the trans-carveol diastereoisomer presented such an effect when investigating the inhibitory activity of AChE of some essential oils from the genera Callicarpa, Premna, and Karomia present in Vietnam. This mechanism of action consists of the major larvicidal action among phytochemicals, where there is interference in the Central Nervous System (CNS) via cutaneous or respiratory absorption resulting in death by intoxication, similar to the effect of organophosphate and carbamate insecticides (Moyes et al., 2017; Wuillda et al., 2019).

Regarding the insecticidal activity of β-citronellol, it was also evidenced that mortality varied according to concentration and exposure period. However, its efficiency at concentrations of 6.2 and 12.5 µL was lower compared to carveol in the 24- and 48-hour exposure periods. In the treatments of 25 and 50 µL, the results showed 100% mortality from the first 24 hours of exposure (Figure 2).

Figure 2
Insecticidal activity of β-citronellol against Ae. aegypti.

As discussed by Silva et al. (2020), the behavior and activity of the positive and negative isomers of β-citronellol may vary according to their dosage, and similar to the findings of the present study, the activity of this compound is more significant at higher concentrations. Thus, the higher the concentrations of this phytoconstituent, the shorter the time required to achieve the desired effect.

The insecticidal activity of β-citronellol was also identified by Baranitharan et al. (2016) when investigating the larvicidal, ovicidal, and repellent activities of compounds present in the essential oil of Melissa officinalis L. (Lemon balm) against Anopheles stephensi L., an organism also studied by Dehghankar et al. (2021). In their research, larvicidal properties were evaluated using the essential oil of Pelargonium roseum (Andrews), and it was found that among the compounds identified, citronellol showed the highest larvicidal activity in both forms of A. stephensi studied.

According to Pavela (2015), some aromatic compounds can enhance the action of β-citronellol. In their study, it was possible to identify a synergistic effect on the larval mortality of Culex quinquefasciatus (Say, 1823) by associating β-citronellol and menthone. Differences in mortality were achieved through the binary proportions studied, indicating that the information obtained in the research could be used for the development of new botanical insecticides.

Similarly, the insectistatic property of this compound has also been evidenced against Ae. aegypti by evaluating its repellent activity through the protection period against mosquito bites, showing significant results (Eden et al., 2020). Corroborating these findings, Nerio et al. (2010) expose in their literature review study essential oils whose repellent activity has already been established, with β-citronellol being one of the main compounds with high repellent properties. The research also reiterates that compounds like this also have promising synergistic effects that should be further explored.

In summary, upon conducting a comparative analysis of the mortality efficiency of both studied monoterpenes, it is evident that after 72 hours of exposure, only the concentration of 6.2 µL failed to achieve 100% mortality (Table 2). In this specific concentration, a higher efficiency of carveol was observed compared to β-citronellol, with the standard deviation of repetitions showing similar results in both substances.

Table 2
Means (M) and standard deviations (SD) of the insecticidal activity of the monoterpenes.

Concentration (µL)	Monoterpene
	Carveol		β-citronellol
	M ± SD (%)		M ± SD (%)
50 µL	100	± 0	100	± 0
25 µL	100	± 0	100	± 0
12.5 µL	100	± 0	100	± 0
6.2 µL	73.35	± 5.03	48.75	± 5.31
Control +	0	± 0	0	± 0
Control -	0	± 0	0	± 0

Regarding the positive and negative control treatments, no mortality was observed in either of them.

In this context, based on the insecticidal activity of monoterpenes, formulations of bioactive molecules could be utilized in vector control programs as alternative methods, which are both environmentally friendly and biologically efficient. However, studies are also needed to evaluate the biosafety of these substances, expand the insecticidal evaluation of other monoterpenes, and elucidate their mechanisms of action (Ramzi et al., 2022). Therefore, this premise should also be extended to carveol and β-citronellol, as studies on their insecticidal activity and mechanism of action against Ae. aegypti are scarce in the literature.

3.2. Restoration of piriproxifen activity by monoterpenes

In the determination of modulation activity, it was evident that both carveol and β-citronellol exhibited such effect (Figure 3). Although the insecticidal efficiency of β-citronellol showed a lower performance than carveol, its efficiency in modulation with PP yielded more promising results, considering the mortality efficiency at the studied concentrations.

Figure 3
Restoration of pyriproxyfen by monoterpenes on Ae. aegypti.

The mortality of carveol 5 µL + PP in the first 24 hours of exposure was only 2.5%, while β-citronellol + PP showed 45% efficiency. In both cases, the mortality efficiency increased throughout the exposure period.

Regarding the second concentration studied, both compounds showed higher efficiency. However, β-citronellol 8 µL + PP presented better results in the exposure period of 24 and 48 hours, corresponding to 98.75% efficiency in both periods. Meanwhile, carveol 8 µL + PP progressed from 72.5 to 96.25% in the aforementioned periods.

At the end of the studied exposure period, none of the modulations at the concentration of 5 µL + PP reached 100% efficiency, corresponding to 77.5% (β-citronellol) and 53.75% (Carveol 5 µL + PP), with the standard deviation of β-citronellol higher than carveol. Regarding 8 µL + PP, both monoterpenes showed 100% mortality, with no standard deviation. Meanwhile, in the positive and negative control treatments, there was no mortality in either of them (Table 3).

Table 3
Means (M) and standard deviations (SD) of piriproxifen restoration.

Concentration (µL)	Monoterpene
	Carveol + PP		β-citronellol + PP
	M ± SD (%)		M ± SD (%)
5 µL	53.75	± 1.25	77.5	± 2.08
8 µL	100	± 0	100	± 0
Control +	0	± 0	0	± 0
Control -	0	± 0	0	± 0

The synergistic activity of terpenes evidenced in the present study was also observed by Sarma et al. (2019). In their research, the synthetic larvicide Temephos and the commercially used adulticide Malathion were tested individually and in binary combinations with terpenic compounds. The study revealed that the combination of Temephos and diallyl disulfide and the combination of Malathion and eudesmol had significant effects on Ae. aegypti larvae. Therefore, terpenic compounds can be used to reduce the dosages of insecticides commonly used against mosquitoes, so that synergistic combinations with efficiency are solutions to reduce the evolution of resistance in mosquitoes.

In addition to enhancing the action of other compounds, terpenes have also shown to positively interact with substances of the same class. In the study by Dhinakaran et al. (2019), the activity of the monoterpenes γ-terpinene (T), R-(+)-limonene (L), carvacrol (C), and trans-anethole (A) on Ae. aegypti larvae was evaluated, where larvicidal properties and synergistic interactions were observed based on the cytotoxicity factor. In all eight combinations studied, there was an additive effect, and none of the combinations showed antagonism, thus characterizing them as promising candidates for enhancing compounds.

4. Conclusion

Both carveol and β-citronellol exhibit insecticidal activity against Ae. aegypti, with carveol showing greater potency as mortality is higher at lower concentrations in the initial hours of exposure. As the exposure period or substance concentration increases, larval mortality also increases.

Both monoterpenes enhance the activity of piriproxifen; however, unlike their individual insecticidal activity, β-citronellol demonstrates greater efficiency at both concentrations studied compared to carveol.

Further studies are needed to elucidate the molecular targets of the studied substances and explore their synergy with other compounds, given the promising results obtained in this study.

References

• ADHIKARI, K., KHANIKOR, B. and SARMA, R., 2022. Persistent susceptibility of Aedes aegypti to eugenol. Scientific Reports, vol. 12, no. 1, pp. 2277. http://doi.org/10.1038/s41598-022-06302-8 PMid:35145175.
  » http://doi.org/10.1038/s41598-022-06302-8
• AZEVEDO, F.R., FERREIRA, R.C.A.B., LEANDRO, C.S., ARAÚJO, I.M. and TINTINO, S.R., 2023. Use of essential oils from plants of Araripe National Forest against Aedes aegypti (Diptera: culicidae). Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 83, pp. e275062. http://doi.org/10.1590/1519-6984.275062 PMid:38055504.
  » http://doi.org/10.1590/1519-6984.275062
• BARANITHARAN, M., DHANASEKARAN, S., MURUGAN, K., KOVENDAN, K. and GOKULAKRISHNAN, J., 2016. Chemical composition and laboratory investigation of Melissa officinalis essential oil against human malarial vector mosquito, Anopheles stephensi L (Diptera: culicidae). Journal of Coastal Life Medicine, vol. 4, no. 12, pp. 969-973. http://doi.org/10.12980/jclm.4.2016J6-174
  » http://doi.org/10.12980/jclm.4.2016J6-174
• CAMPOS, K.B., MARTINS, A.J., RODOVALHO, C.D.M., BELLINATO, D.F., DIAS, L.D.S., MACORIS, M.D.L.D.G. and OBARA, M.T., 2020. Assessment of the susceptibility status of Aedes aegypti (Diptera: Culicidae) populations to pyriproxyfen and malathion in a nation-wide monitoring of insecticide resistance performed in Brazil from 2017 to 2018. Parasites & Vectors, vol. 13, no. 1, pp. 1-18. http://doi.org/10.1186/s13071-020-04406-6 PMid:33109249.
  » http://doi.org/10.1186/s13071-020-04406-6
• CAVALLI, F. S., SEBEN, J. T., BUSATO, M. A., LUTINSKI, J. A. and ANDRIOLI, D. C., 2019. Controlling the Vector Aedes Aegypti and Handling Dengue Fever Bearing Patients.Revista de Pesquisa Cuidado é Fundamental Online, vol. 11, no. 5, pp. 1333-1339. https://doi.org/10.9789/2175-5361.2019.v11i5.1333-1339
  » https://doi.org/10.9789/2175-5361.2019.v11i5.1333-1339
• CHIELE, A.H., FLORENTINO, I.N.A., SCHULZ, R.G., FIGUEIREDO, E.F., LIBRELOTTO, C.S. and COLACITE, J., 2023. Estudo da variabilidade genética e análise de possíveis mutações kdr no gene codificador dos canais de sódio relacionados à resistência do Aedes aegypti a inseticidas.Research Social Development, vol. 12, no. 3, pp. e11312340474. http://doi.org/10.33448/rsd-v12i3.40474
  » http://doi.org/10.33448/rsd-v12i3.40474
• CRUZ, I.L.S.D., PIMENTEL, M.A.G., NASCIMENTO, T.A., ALVES, S.P., MALECK, M. and QUEIROZ, M.M.D.C., 2024. Larvicidal activity and chemical composition of four essential oils against Aedes aegypti (Diptera: culicidae). Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 84, pp. e283724. http://doi.org/10.1590/1519-6984.283724 PMid:39476032.
  » http://doi.org/10.1590/1519-6984.283724
• DEHGHANKAR, M., MALEKI-RAVASAN, N., TAHGHIGHI, A., KARIMIAN, F. and KARAMI, M., 2021. Bioactivities of rose-scented geranium nanoemulsions against the larvae of Anopheles stephensi and their gut bacteria. PLoS One, vol. 16, no. 2, pp. e0246470. http://doi.org/10.1371/journal.pone.0246470 PMid:33556110.
  » http://doi.org/10.1371/journal.pone.0246470
• DHINAKARAN, S.R., MATHEW, N. and MUNUSAMY, S., 2019. Synergistic terpene combinations as larvicides against the dengue vector Aedes aegypti Linn. Drug Development Research, vol. 80, no. 6, pp. 791-799. http://doi.org/10.1002/ddr.21560 PMid:31241777.
  » http://doi.org/10.1002/ddr.21560
• EDEN, W. T., ALIGHIRI, D., SUPARDI, K. I. and CAHYONO, E., 2020. The mosquito repellent activity of the active component of air freshener gel from Java Citronella oil (Cymbopogon winterianus).Journal of parasitology research, vol. 2020, no. 1, pp. 9053741. https://doi.org/10.1155/2020/9053741
  » https://doi.org/10.1155/2020/9053741
• FERREIRA, J. A., DE SOUSA JÚNIOR, D. L., MARQUES, A. E. F. and De CARVALHO MENDES, R., 2019. Prospecção Fitoquímica e Análise da Atividade Antimicrobiana e Moduladora in Vitro do Extrato Hidroalcoólico das Folhas de Senna spectabilisEnsaios e Ciência C Biológicas Agrárias e da Saúde, vol. 23, no. 3, pp. 262-267. https://doi.org/10.17921/1415-6938.2019v23n3p262-267
  » https://doi.org/10.17921/1415-6938.2019v23n3p262-267
• HUNG, N.H., QUAN, P.M., SATYAL, P., DAI, D.N., HOA, V.V., HUY, N.G. and SETZER, W.N., 2022. Acetylcholinesterase inhibitory activities of essential oils from Vietnamese traditional medicinal plants. Molecules (Basel, Switzerland), vol. 27, no. 20, pp. 7092. http://doi.org/10.3390/molecules27207092 PMid:36296686.
  » http://doi.org/10.3390/molecules27207092
• IWAMURA, T., GUZMAN-HOLST, A. and MURRAY, K.A., 2020. Accelerating invasion potential of disease vector Aedes aegypti under climate change. Nature Communications, vol. 11, no. 1, pp. 2130. http://doi.org/10.1038/s41467-020-16010-4 PMid:32358588.
  » http://doi.org/10.1038/s41467-020-16010-4
• KHALEEL, C., TABANCA, N. and BUCHBAUER, G., 2018. α-Terpineol, a natural monoterpene: a review of its biological properties. Open Chemistry, vol. 16, no. 1, pp. 349-361. http://doi.org/10.1515/chem-2018-0040
  » http://doi.org/10.1515/chem-2018-0040
• LEE, S., TSAO, R., PETERSON, C. and COATS, J.R., 1997. Insecticidal activity of monoterpenoids to western corn rootworm (Coleoptera: Chrysomelidae), twospotted spider mite (Acari: Tetranychidae), and house fly (Diptera: Muscidae). Journal of Economic Entomology, vol. 90, no. 4, pp. 883-892. http://doi.org/10.1093/jee/90.4.883 PMid:9260540.
  » http://doi.org/10.1093/jee/90.4.883
• LEITE, T.V.P. and BERTOTTI, D.L., 2020. Efeito dos inseticidas botânicos aplicados no manejo agroecológico de pragas na cultura do milho doce.Revista Brasiliense de Agroambiente e Desenvolvimento Sustentável, vol. 1, no. 1, pp. 12-20.
• LI, M., YANG, T., KANDUL, N.P., BUI, M., GAMEZ, S., RABAN, R. and AKBARI, O.S., 2020. Development of a confinable gene drive system in the human disease vector Aedes aegypti. eLife, vol. 9, pp. e51701. http://doi.org/10.7554/eLife.51701 PMid:31960794.
  » http://doi.org/10.7554/eLife.51701
• LIMA, É.O., RODRIGUES, F.A.C., BUTAKKA, C.M., MIYAZAKI, R.D., DE MIRANDA CERQUEIRA, L.L. and MARIOTTO, S., 2021. Avaliação do polimorfismo na enzima esterase em populações naturais de Aedes aegypti em Chapada de Guimarães, Mato Grosso. Brazilian Journal of Development, vol. 7, no. 2, pp. 18539-18552. http://doi.org/10.34117/bjdv7n2-477
  » http://doi.org/10.34117/bjdv7n2-477
• MARQUES, C. S., 2020.Mecanismos moleculares da resistência a inseticidas químicos na população de Aedes aegypti (Linnaeus, 1762) da cidade do Funchal, Ilha da Madeira Lisboa: Instituto de Higiene e Medicina Tropical, 106 p. Dissertação de Mestrado em Ciências Biomédicas.
• MOYES, C.L., VONTAS, J., MARTINS, A.J., NG, L.C., KOOU, S.Y., DUSFOUR, I. and WEETMAN, D., 2017. Contemporary status of insecticide resistance in the major Aedes vectors of arboviruses infecting humans. PLoS Neglected Tropical Diseases, vol. 11, no. 7, pp. e0005625. http://doi.org/10.1371/journal.pntd.0005625 PMid:28727779.
  » http://doi.org/10.1371/journal.pntd.0005625
• NERIO, L.S., OLIVERO-VERBEL, J. and STASHENKO, E., 2010. Repellent activity of essential oils: a review. Bioresource Technology, vol. 101, no. 1, pp. 372-378. http://doi.org/10.1016/j.biortech.2009.07.048 PMid:19729299.
  » http://doi.org/10.1016/j.biortech.2009.07.048
• NUNES, J.S., DE SOUZA, E.M., AMORIM JÚNIOR, A.C., LORENZO, V.P., COSTA, E.C. and CUNHA JÚNIOR, J.A.N., 2022. Bioatividade do extrato aquoso de folhas de Vitis vinifera sobre larvas do mosquito Aedes aegypti. Revista Semiárido De Visu, vol. 10, no. 3, pp. 247-259. http://doi.org/10.31416/rsdv.v10i3.384
  » http://doi.org/10.31416/rsdv.v10i3.384
• PANDEY, S.K., TANDON, S., AHMAD, A., SINGH, A.K. and TRIPATHI, A.K., 2013. Structure–activity relationships of monoterpenes and acetyl derivatives against Aedes aegypti (Diptera: Culicidae) larvae. Pest Management Science, vol. 69, no. 11, pp. 1235-1238. http://doi.org/10.1002/ps.3488 PMid:23908002.
  » http://doi.org/10.1002/ps.3488
• PAVELA, R., 2015. Acute toxicity and synergistic and antagonistic effects of the aromatic compounds of some essential oils against Culex quinquefasciatus Say larvae. Parasitology Research, vol. 114, no. 10, pp. 3835-3853. http://doi.org/10.1007/s00436-015-4614-9 PMid:26149532.
  » http://doi.org/10.1007/s00436-015-4614-9
• RAMZI, A., EL OUALI LALAMI, A., ANNEMER, S., EZ ZOUBI, Y., ASSOUGUEM, A., ALMUTAIRI, M.H. and FARAH, A., 2022. Synergistic effect of bioactive monoterpenes against the mosquito, Culex pipiens (Diptera: culicidae). Molecules (Basel, Switzerland), vol. 27, no. 13, pp. 4182. http://doi.org/10.3390/molecules27134182 PMid:35807427.
  » http://doi.org/10.3390/molecules27134182
• SANTOS, S.R., MELO, M.A., CARDOSO, A.V., SANTOS, R.L., DE SOUSA, D.P. and CAVALCANTI, S.C., 2011. Structure–activity relationships of larvicidal monoterpenes and derivatives against Aedes aegypti Linn. Chemosphere, vol. 84, no. 1, pp. 150-153. http://doi.org/10.1016/j.chemosphere.2011.02.018 PMid:21376365.
  » http://doi.org/10.1016/j.chemosphere.2011.02.018
• SARMA, R., ADHIKARI, K., MAHANTA, S. and KHANIKOR, B., 2019. Combinations of plant essential oil based terpene compounds as larvicidal and adulticidal agent against Aedes aegypti (Diptera: culicidae). Scientific Reports, vol. 9, no. 1, pp. 9471. http://doi.org/10.1038/s41598-019-45908-3 PMid:31263222.
  » http://doi.org/10.1038/s41598-019-45908-3
• SILVA, D., DINIZ-NETO, H., CORDEIRO, L., SILVA-NETA, M., SILVA, S., ANDRADE-JÚNIOR, F. and LIMA, E., 2020. (R)-(+)-β-Citronellol and (S)-(−)-β-Citronellol in Combination with Amphotericin B against Candida Spp. International Journal of Molecular Sciences, vol. 21, no. 5, pp. 1785. http://doi.org/10.3390/ijms21051785 PMid:32150884.
  » http://doi.org/10.3390/ijms21051785
• SILVA, E.R., DE CARVALHO, F.O., TEIXEIRA, L.G., SANTOS, N.G.L., FELIPE, F.A., SANTANA, H.S.R. and NUNES, P.S., 2018a. Pharmacological effects of carvacrol in in vitro studies: A review. Current Pharmaceutical Design, vol. 24, no. 29, pp. 3454-3465. http://doi.org/10.2174/1381612824666181003123400 PMid:30280662.
  » http://doi.org/10.2174/1381612824666181003123400
• SILVA, I.M., MARTINS, G.F., MELO, C.R., SANTANA, A.S., FARO, R.R., BLANK, A.F. and BACCI, L., 2018b. Alternative control of Aedes aegypti resistant to pyrethroids: lethal and sublethal effects of monoterpene bioinsecticides. Pest Management Science, vol. 74, no. 4, pp. 1001-1012. http://doi.org/10.1002/ps.4801 PMid:29160036.
  » http://doi.org/10.1002/ps.4801
• SILVÉRIO, M.R.S., ESPINDOLA, L.S., LOPES, N.P. and VIEIRA, P.C., 2020. Plant natural products for the control of Aedes aegypti: the main vector of important arboviruses. Molecules (Basel, Switzerland), vol. 25, no. 15, pp. 3484. http://doi.org/10.3390/molecules25153484 PMid:32751878.
  » http://doi.org/10.3390/molecules25153484
• TAKAGI, B.A., DE SOUZA, T.G.B., DE OLIVEIRA, M.D., BERNARDES, L.G., ODA, J.Y., MACHADO, A.R.D.S.R. and MACHADO, A.M., 2020. Efeito larvicida e ovocida de extratos de Crotalaria pallida sobre o vetor Aedes aegypti. Brazilian Journal of Development, vol. 6, no. 5, pp. 23060-23074. http://doi.org/10.34117/bjdv6n5-019
  » http://doi.org/10.34117/bjdv6n5-019
• VANLERBERGHE, V., GÓMEZ-DANTÉS, H., VAZQUEZ-PROKOPEC, G., ALEXANDER, N., MANRIQUE-SAIDE, P., COELHO, G. and STUYFT, P.V.D., 2018. Changing paradigms in Aedes control: considering the spatial heterogeneity of dengue transmission. Revista Panamericana de Salud Pública, vol. 41, pp. e16. http://doi.org/10.26633/RPSP.2017.16 PMid:31391815.
  » http://doi.org/10.26633/RPSP.2017.16
• VARGAS, L.D.L., FERREIRA, S.M.B., SOUZA, M.D., DA SILVA, C.A.L. and SHIMOYA-BITTENCOURT, W., 2022. Resistência Das Populações de Aedes (Stegomyia) aegypti (Linnaeus, 1762) (Insecta, Diptera, Culicidae) Aos Inseticidas Utilizados Para o Controle.Revista de Ciências Médicas e Biológicas, vol. 21, pp. 98-116. http://doi.org/10.9771/cmbio.v21i1.44458
  » http://doi.org/10.9771/cmbio.v21i1.44458
• WUILLDA, A. C. J. S., MARTINS, R. C. C. and COSTA, F. D. N., 2019. Larvicidal activity of secondary plant metabolites in aedes aegypti control: an overview of the previous 6 years.Natural Product Communications, vol. 14, no. 7, pp. 1934578X19862893. https://doi.org/10.1177/1934578X19862893
  » https://doi.org/10.1177/1934578X19862893

Publication Dates

• Publication in this collection
  17 Mar 2025
• Date of issue
  2025

History

• Received
  07 July 2024
• Accepted
  29 Jan 2025