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Revista Colombiana de Ciencias Hortícolas

versión impresa ISSN 2011-2173

rev.colomb.cienc.hortic. vol.18 no.2 Bogotá mayo/ago. 2024  Epub 31-Jul-2024

https://doi.org/10.17584/rcch.2024v18i2.17363 

Section of aromatic and medicinal herbs

Acaricidal and larvicidal activity of Piper marginatum and Piper tuberculatum essential oils from Ecuador

Actividad acaricida y larvicida de los aceites esenciales de Piper marginatum y Piper tuberculatum de Ecuador

SHIRLEY MADELEINE MONCAYO-BAÑO1  2  4 
http://orcid.org/0000-0003-2374-497X

MARÍA EUGENIA RONDÓN-RIVAS2 
http://orcid.org/0000-0003-2393-751X

FRANCISCO XAVIER CORNEJO-SOTOMAYOR3 
http://orcid.org/0000-0002-4081-4047

1 Universidad Agraria del Ecuador, Facultad de Ciencias Agrarias, Carrera Agroindustria, Guayaquil (Ecuador).

2 Universidad de Los Andes, Facultad de Farmacia y Bioanálisis, Cátedra de Farmacognosia, Merida (Venezuela).

3 Universidad de Guayaquil, Facultad de Ciencias Naturales, Herbario GUAY, Guayaquil (Ecuador).


ABSTRACT

Piper marginatum and Piper tuberculatum are species used for their insecticidal properties by local indigenous people in eastern Ecuador. This study aimed to determine the acaricidal and larvicidal activity of the essential oil of these species. The essential oils were obtained by hydrodistillation. The acaricidal activity was evaluated with the contact toxicity method against larvae of the tick Rhipicephalus microplus. Larvicidal activity was evaluated against Aedes aegypti mosquito larvae following WHO recommended guidelines. The essential oils of P. marginatum and P. tuberculatum showed an acaricidal potential with LC50 of 0.90 and 0.73 µL mL-1,respectively. In addition, excellent larvicidal activity was obtained with LC50 of 11.87 µL mL-1 (P. marginatum) and 8.42 µL mL-1 (P. tuberculatum) at 48 hours of evaluation. This is the first report of the acaricidal activity of P. marginatum and P. tuberculatum essential oils against R. microplus tick larvae. The results indicate that essential oils could serve as a natural alternative for controlling these pests, with ethnobotanical applications as a lice and tick repellent.

Additional key words: Piper; larvae; Rhipicephalus microplus; Aedes aegypti; ethnobotanical

RESUMEN

Piper marginatum y Piper tuberculatum son especies utilizadas por sus propiedades insecticidas por indígenas locales del este de Ecuador. Este estudio tuvo como objetivo determinar la actividad acaricida y larvicida del aceite esencial de estas especies. Los aceites esenciales se obtuvieron por hidrodestilación. La actividad acaricida se evaluó con el método de toxicidad por contacto frente a larvas de la garrapata Rhipicephalus microplus. Se evaluó la actividad larvicida contra larvas del mosquito Aedes aegypti siguiendo los lineamientos recomendados por la OMS. Los aceites esenciales de P. marginatum y P. tuberculatum mostraron un potencial acaricida con CL50 de 0.90 y 0.73 µL mL-1,respectivamente. Además, se obtuvo una excelente actividad larvicida con CL50 de 11.87 µL mL-1 (P. marginatum) y 8.42 µL mL-1 (P. tuberculatum) a las 48 horas de evaluación. Este es el primer reporte de la actividad acaricida de los aceites esenciales de P. marginatum y P. tuberculatum frente a las larvas de la garrapata R. microplus. Los resultados indican que los aceites esenciales podrían servir como una alternativa natural para el control de estas plagas, con aplicaciones etnobotánicas como repelente de piojos y garrapatas.

Palabras clave adicionales: Piper; larvas; Rhipicephalus microplus; Aedes aegypti; etnobotánica

INTRODUCTION

The most significant tick in livestock worldwide is Rhipicephalus (Boophilus) microplus. This hematophagous ectoparasite is one of the main obstacles to the productivity of the livestock industry in areas where this species is endemic (Nicaretta et al., 2021). It causes a decrease in cattle weight gain, damage to hides, reduced meat and milk production, myiasis and transmission of zoonotic diseases (Polanco and Ríos, 2016). Due to its significance, it is the most studied species in acaricide trials (Adenubi et al., 2018). Aedes aegypti are vectors of arboviral pathogens that annually cause hundreds of millions of cases of Zika, dengue fever, yellow fever, and chikungunya. They thrive in urbanized areas where they are in close contact with people, making them an exceptionally successful vector. A. aegypti is extremely common in areas that lack piped water systems and rely heavily on stored water for breeding sites (Matthews, 2019; Zettel and Kaufman, 2019).

In the prevention of vector-borne diseases, there is a trend to develop alternative methods based on natural products to replace chemical pesticides and delay the development of resistance, a problem that causes millions of dollars in losses (Selles et al., 2021). Essential oils are metabolites formed by a complex mixture of several chemical compounds mainly terpenes and phenylpropanoids, which give plants their characteristic aroma and possess a wide range of biological properties, including antimicrobial, antifungal and insecticidal activities (De Souza et al., 2023). Studies conducted on the essential oils of Piper species (Piperaceae) highlight their great potential for pest control and the low environmental impact observed during the process (Pereira et al., 2021). Their efficacy against different species of mosquitoes and mites at low concentrations has been reported (Huong et al., 2019; Araújo et al., 2020).

Piper marginatum Jacq. and Piper tuberculatum Jacq. are native neotropical species that stand out for their pharmacological potential and are widely used in folk medicine for their healing properties (Salehi et al., 2019). P. marginatum is known in Ecuador as cordoncillo blanco, Santa María and "Anotede" in Tsa'fiki language (De la Torre, 2008). Its essential oils have shown antibacterial, antioxidant, antiparasitic and larvicidal activities (Ayres et al., 2021). P. tuberculatum is used in Ecuador to combat pediculosis problems (De la Torre et al., 2008). Previous studies have shown that its essential oils have antimicrobial, insecticidal and antiprotozoal effects (Da Silva et al., 2023).

This study reports the acaricidal and larvicidal activity of the essential oils of P. marginatum and P. tuberculatum against larvae of the tick R. microplus and the mosquito A. aegypti. These species cause serious damage to human and animal health and result in serious economic losses.

MATERIALS AND METHODS

Plant materials

Leaves, stems, and inflorescences of P. marginatum and P. tuberculatum were collected in Cumanda, Chimborazo province (2°12'12" S, 79°06'36" W) and on the El Triunfo - Bucay road, Guayas province (2°18'9" S, 79°14'16" W) from Ecuador. The identification of the botanical species was carried out in the GUAY Herbarium of the Faculty of Natural Sciences of the University of Guayaquil, Ecuador, where the vouchers of the specimens were deposited under the codes MER06 (P. marginatum) and MER07 (P. tuberculatum).

Hydrodistillation

The leaves, stems, and inflorescences of the species were subjected to hydrodistillation for 3 h, using a Clevenger-type apparatus. The oils, once obtained, were meticulously dried over anhydrous sodium sulfate and then stored in sealed vials. These vials were then placed in a controlled environment at 4°C in the dark to ensure the oils' stability and integrity until they were ready for analysis and testing.

Acaricidal activity

Acaricidal activity was analyzed using the contact toxicity technique described by Tabari et al. (2020) with minor modifications. Larvae between 14 and 21 d old of the tick R. microplus obtained from gravid females collected from infested cattle were used. The tick species was identified by Prof. Antonio Ascencão of the Laboratory of Biodiversity of Arthropods, Department of Biology, Faculty of Sciences, University of Los Andes, Venezuela. Serials of essential oil dilutions were prepared from 20.0 to 0.3 µL mL-1, in 2% Tween® 80 solution. A Tween® 80 solution was used as a negative control and a 20 µL mL-1 cypermethrin solution dissolved in Tween® 80 (2%), prepared from the commercial product CIPER-VEEX® (10% cypermethrin), was used as a positive control. Whatman® N°1 filter paper discs were impregnated with 1 mL of the test solutions. Tick larvae were transferred to two of the impregnated paper disks, placed inside a Petri dish. The plates were sealed and stored in a glass chamber at 27±2°C and 85±2% humidity. Assays were performed in duplicate. Mortality records were made after 48 h under a stereomicroscope.

Larvicidal activity

Larvicidal activity was analyzed following the guidelines of the World Health Organization (WHO, 1981) for third and fourth instar larvae of wild A. aegypti, collected at the Faculty of Natural Sciences of the University of Guayaquil. The larvae were identified by the author using taxonomic guides. An aliquot of essential oils was solubilized in absolute ethanol until a stock solution was obtained, to prepare test solutions in serial dilutions of 3 to 1,000 µL mL-1. The final volume of the solutions was 50 mL. A total of 10 larvae were exposed to the test solutions. The negative control consisted of a 2% ethanol solution; the positive control consisted of a solution of the organophosphate insecticide malathion (1 µL mL-1). Each concentration was evaluated in triplicate. The assays were stored at 25±2ºC and relative humidity of 70±2%. Larval mortality readings were taken at 24 and 48 h.

Statistical analyses

The concentrations producing 50 and 95% mortality in the mite and larvae population (LC50) and (LC95) and their respective confidence limits (95 %) were determined by Probit analysis. To establish statistically significant differences between the assays, a one-way ANOVA analysis of variance was performed using the Fisher (LSD) method. Values of P<0.05 were considered significant. All the statistical analyses were carried out using Statgraphics Centurion XVI statistical software.

RESULTS AND DISCUSSION

Acaricidal activity

The mortality percentages of R. microplus larvae after 48 h of exposure to the essential oils of P. marginatum and P. tuberculatum are shown in tables 1 and 2. No mortality was reported in the negative control, while mortality with the positive control was 100%. The results indicate that the essential oil of P. tuberculatum was the most toxic, causing 100% mortality of R. microplus larvae at a concentration of 1 µL mL-1. The ANOVA comparison analysis found statistically significant differences between the lethal concentrations of the essential oils at 95 % significance level.

Table 1. Mortality percentage of Rhipicephalus microplus caused by different concentrations of Piper marginatum essential oil

Concentration (µL mL-1) 0.6 1.2 2.5 5.0 10.0 20.0
Mortality 11±2 86±1 92±3 100±0 100±0 100±0

Mean of n=3±standard deviation.

Table 2. Mortality percentage of larvae of Rhipicephalus microplus caused by different concentrations of Piper tuberculatum essential oil

Concentration (µL mL-1) 0.3 0.6 0.8 1.0 2.5
Mortality 6±1 23±2 49±1 100±0 100±0

Mean of n=3±standard deviation.

Table 3 summarizes the LC50 and LC90 values of P. marginatum and P. tuberculatum oils against R. microplus tick larvae. The most potent oil was that of P. tuberculatum, with a LC50 of 0.73 µL mL-1 while the oil of P. marginatum showed an LC50 of 0.90 µL mL-1.

Table 3. Lethal concentrations of the essential oils of Piper species on larvae of Rhipicephalus microplus

Essential oil LC50 LC95
P. marginatum 0.90 (0.75-1.02) 2.10 (1.86-2.47)
P. tuberculatum 0.73 (0.71-0.75) 1.06 (1.02-1.11)

(95% CI) = 95% confidence interval.

This groundbreaking report unveils the acaricidal activity of essential oils from Piper species against R. microplus larvae, a discovery of utmost significance as larvae are pivotal in tick control systems. Da Silva et al. (2017) suggest that essential oils from plants of the genus Piper, rich in phenylpropanoids and hydrocarbonated sesquiterpenes, as in this study, exhibit potent insecticidal and acaricidal activity.

The practical implications of this research are evident in the evaluation of the essential oil of P. marginatum and P. tuberculatum against the mite Tetranychus urticae, a crop pest from the family Tetranychidae. The obtained LC50 values of 0.90 and 0.50 µL mL-1, respectively (Ribeiro et al., 2016; Araújo et al., 2020) underscore the potential of these essential oils in pest control.

According to Selles et al. (2021), the acaricidal activity of essential oils is related to their hydrophobic nature, which is responsible for several mechanical effects, causing death by water stress or asphyxia due to alteration of cuticular waxes and blockage of respiratory stigmas. Essential oils have been shown to act on the motor function of R. microplus larvae, increasing catecholamine levels within the central nervous system (Salman et al., 2020) and inhibiting the action of acetylcholinesterase in this tick species (Cardoso et al., 2020).

The acaricidal capacity observed in the extracts supports the ethnobotanical use of P. tuberculatum in Ecuador as a lice and tick repellent (De la Torre et al., 2008).

Larvicidal activity

The concentrations of the essential oils and their respective percentages of mortality after 24 and 48 h of exposure are shown in tables 4 and 5. A. aegypti larvae's mortality percentage was 100% from the concentration of 50 µL mL-1 in both oils evaluated. No mortality was reported in the negative control, while mortality with the positive control was 100%.

Table 4. Mortality percentage of Aedes aegypti larvae caused by different concentrations of Piper marginatum essential oil (µL mL -1 )

Exposure time (h) 3 6 12 16 20 25 50-250
24 10±0 27±6 30±0 53±6 73±6 83±6 100±0
48 17±6 30±6 43±6 67±6 87±15 90±0 100±0

Mean of n=3±standard deviation.

Table 5 Mortality percentage of Aedes aegypti larvae caused by different concentrations of Piper tuberculatum essential oil (µL mL -1 )

Exposure time (h) 3 6 12 25 30 40-250
24 17±6 30±10 33±6 60±0 70±10 100±0
48 30±10 57±6 60±10 70±0 80±10 100±0

Mean of n=3±standard deviation.

The lethal concentrations of the essential oils are shown in table 6. P. tuberculatum obtained the highest activity with LC50 of 8.42 µL mL-1 and LC95 of 51.38 µL mL-1 while P. marginatum obtained LC50 of 11.87 µL mL-1 and LC95 of 28.29 µL mL-1 at 48 h of exposure. The ANOVA comparison analysis found statistically significant differences between the lethal concentrations of the essential oils at 95% significance level.

Table 6. Lethal concentrations (LC) of the essential oils of Pirper marginatum and P. tuberculatum species on 3°- 4° instar larvae of the mosquito Aedes aegypti

Exposure time (h) LC P. marginatum P. tuberculatum
24 LC50 (CI) 14.65 (11.90-17.84) 19.70 (15.43-25.53)
LC95 (CI) 32.34 (26.95-42.53) 52.69 (41.40-78.73)
48 LC50 (CI) 11.87 (9.21-14.61) 8.42 (4.25-13.08)
LC95 (CI) 28.29 (23.63-36.83) 51.38 (37.76-94.06)

(95% CI) = 95% confidence interval.

The volatile compounds of Piper species are characterized by their great potential for pest control and the low environmental impact (Pereira et al., 2021). Previous larvicidal evaluations on the oils of P. marginatum and P. tuberculatum (Lavor et al., 2012; Pereira et al., 2021), reported LC50 of 39 and 106 µL mL-1, respectively. Essential oils from Ecuadorian species showed higher larvicidal activity, probably due to their different chemical composition and synergistic interactions between their compounds. The plant extracts used in the present study were previously characterized to identify their phytochemical composition by our research team. Compounds such as sesquiterpenes curzerene (22.44%) and atractylone (18.15%) were identified in P. marginatum, while in P. tuberculatum, the phenylpropanoid dilapiol (49.15%) was identified (Moncayo et al., 2021). Species with essential oils predominantly composed of these compounds have shown insecticidal properties against both adult and larvae stages of A. aegypti and Culex quinquefasciatus mosquitoes (Benelli et al., 2017; Hung et al., 2020; Pereira et al., 2021). Dilapiol, a potent inhibitor of cytochrome activity (P450 and CYP34A), reduces the ability to excrete xenobiotics causing the insect's death by accumulation of toxic substances in the digestive tract (Santos et al., 2021). In addition, its structure can amplify the effects of other chemicals (Durofil et al., 2021).

CONCLUSION

The present study demonstrated that the essential oils of P. marginatum and P. tuberculatum possess high acaricidal (R. microplus) and larvicidal (A. aegypti) activity and could serve as a natural alternative for the biocontrol of these dangerous disease vectors. This is the first report on the activity of P. marginatum and P. tuberculatum essential oils against R. microplus tick larvae.

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Received: March 17, 2024; Revised: April 28, 2024; Accepted: May 24, 2024

4 Corresponding author. smoncayo@uagraria.edu.ec

Conflict of interests:

The manuscript was prepared and reviewed with the participation of the authors, who declare that there is no conflict of interest that puts at risk the validity of the presented results.

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