The Laboratory and Semi-Field Larvicidal Effects of Essential Oil Extracted from <i>Feronia limonia</i> against <i>Anopheles arabiensis</i> Patton

Kweka, Eliningaya J.; Mdoe, France P.; Lowassari, Norah N.; Venkatesalu, Venugopalan; Senthilkumar, Annadurai

doi:https://doi.org/10.1155/2023/5907603

Journal of Parasitology Research

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Abstract Introduction Methods Results Discussion Conclusion Data Availability Ethical Approval Conflicts of Interest Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2023 | Article ID 5907603 | https://doi.org/10.1155/2023/5907603

The Laboratory and Semi-Field Larvicidal Effects of Essential Oil Extracted from Feronia limonia against Anopheles arabiensis Patton

Eliningaya J. Kweka,^1,2France P. Mdoe,³Norah N. Lowassari,²Venugopalan Venkatesalu,⁴and Annadurai Senthilkumar⁴

Academic Editor: Lizandra Guidi Magalhães

Received17 Jan 2022

Revised13 Sept 2022

Accepted03 Feb 2023

Published22 Feb 2023

Abstract

This study intended to evaluate the larvicidal activity of Feronia limonia leaf essential oil against the wild population of Anopheles arabiensis Patton larvae in laboratory and semi-field environments. Larvae mortality was observed after 12, 24, 48, and 72 hours of exposure. In laboratory condition, the essential oil showed good larvicidal activity against An. arabiensis (LC₅₀ = 85.61 and LC₉₅ = 138.03 ppm (after 12 hours); LC₅₀ = 65.53 and LC₉₅ = 117.95 ppm (after 24 hours); LC₅₀ = 32.18 and LC₉₅ = 84.59 ppm (after 48 hours); LC₅₀ = 8.03 and LC₉₅ = 60.45 ppm (after 72 hours), while in semi-field experiments, larvicidal activity was (LC₅₀ = 91.89 and LC₉₅ = 134.93 ppm (after 12 hours); LC₅₀ = 83.34 and LC₉₅ = 109.81 ppm (after 24 hours); LC₅₀ = 66.78 and LC₉₅ = 109.81 (after 28 hours); LC₅₀ = 47.64 and 90.67 ppm (after 72 hours). These results give an insight on the future use of F. limonia essential oils for mosquitoes control.

1. Introduction

Mosquito control in recent past has been challenged by the wide spread of insecticide resistance among the vector populations [1, 2]. The decline of efficacy of currently used vector control tools (long-lasting insecticidal nets and indoor residual spray) have threatened the achieved efforts across Sub-Saharan Africa [1, 2]. The search for alternative insecticides with different mode of action is of paramount importance. The targeting of breeding habitats has shown a great impact on larvae and subsequently reduction of adult mosquitoes and disease incidences [3]. The search of the natural products to overcome the resistance by targeting the aquatic stages of mosquitoes has shown an effect in laboratory and semi-field evaluation [3]. The use of botanical extracts for pests control has shown to have no side effect on environment and non-targeted organisms [4, 5]. Previous studies have shown that the essential oil from plants displayed a great impact on larvicidal, adulticidal, and repellent effects [6]. To date, the plant extracts resistance by vectors has not been reported [6]. The aim of this study was to assess the larvicidal activities of Feronia limonia leaf essential oil against An. arabiensis.

2. Material and Methods

2.1. Plant Collection and Essential Oil Extraction

The leaves of F. limonia were collected from Keerapalayam [11°26;03 N, 079°39;02 E], Cuddalore District, Tamil Nadu, India, and the voucher specimen (AUBOT# 209) is deposited at the Herbarium, Department of Botany, AU. The fresh leaves were subjected to hydro-distillation using Clevenger-type apparatus for 4 hours. The essential oil was dried over anhydrous sodium sulphate, and the purified essential oil was stored at +4°C for mosquito larvicidal activity.

The essential oil volatile constituents were determined by Gas chromatography–mass spectrometry (GC-MS) by using Varian 3800 Gas Chromatography equipped with Varian 1200 L single quadrupole mass spectrometer. The mass spectrometer was operated in the electron impact (IE) mode at 70 eV. Ion source and transfer line temperature were kept at 250°C. The mass spectra were obtained by centroid scan of the mass range from 40 to 1000 amu. The compounds were identified based on the comparison of their retention indices (RI), retention time (RT), and data bank mass spectra of Wiley library (Table 1).

2.2. Mosquito Larvae Rearing

The An. arabiensis Patton eggs were obtained from wild gravid mosquitoes collected from cowsheds in Lower Moshi near rice irrigation schemes. The wild population of Anopheles gambiae s.l. in this area has been confirmed to be composed of 100% An. arabiensis [7]. The larvae room was maintained at the temperature of °C and relative humidity of %. The larvae were fed with 0.003 g of Tetra mine per larva as shown in previous study [8]. The An. arabiensis larvae were reared until when they were stage three instars and used for screening as per WHO guidelines.

2.3. Mosquito Larvicidal Assay

The F. limonia essential oil was dissolved in 1 ml of acetone. Then, serial dilution was made from this stoke solution into six concentrations 3.125, 6.25, 12.5, 25, 50, and 100 ppm with distilled water as per WHO guidelines. Each concentration had six replicates, each with twenty-third instar larvae of An. arabiensis. There were two controls: one control (C1) contained distilled water, while the other (C2) contained 1 ml aqueous solution of acetone. During these assays, food was provided to the larvae after 24 hours. The mortality of larvae was monitored after 12, 24, 48, and 72 hours of exposure period in both treatments and controls. The dead and moribund larvae were both considered dead. Experiments were set in both laboratory and semi-field conditions as described elsewhere [9].

2.4. Data Analysis

Data were entered into excel sheet and transferred into IBM SPSS Version 26 (IMB Corp., Armonk, NY, USA) for analysis. The lethal concentrations LC₅₀ and LC₉₅ and their 95% confidence limit of upper and lower confidence levels were calculated by probit analysis [10]. The comparison of larvae mortality among treatments, between treatments and control, and between laboratory and semi-field environment were conducted using Chi-square test.

3. Results

3.1. Chemical Composition

The GC-MS chemical analysis of the F. limonia leaf essential oil revealed 51 chemical compounds with estragole as the highest abundant compound with 34.69%, while cis-dihydro-β-terpineol and ρ-Cymene were revealed to have the least amount of 0.03% each. The other 48 compounds occurred in different percentage compositions (Table 1).

3.2. Mortality Effect of the Essential Oils

The mortality of the larvae of An. arabiensis from 12 to 72 hours of observation in both laboratory and semi-field environment was found to be dosage dependent (Figure 1), and the proportion of larvae that died between laboratory and semi-field environments was found to have statistically significant difference (Table 2). The observed mortality rate was higher in the laboratory environment as compared to semi-field environment, it ranged between 20.83% in 3.125 ppm and 91.88% in 100 ppm (Table 2). Also, the mortality effect was found to be exposure time dependent, with percentage mortality significant different revealed in some time intervals (Table 3).

3.3. Lethal Dose

The lethal dose enough to kill 50% (LC₅₀) and 95% (LC₉₅) of the larvae exposed varied with exposure time in both laboratory and semi-field environments (Table 4). In both LC₅₀ and LC₉₅, the lowest values were found in laboratory than in the semi-field conditions (Table 4). The proportions of lethal dose comparison were found to differ significantly between laboratory and semi-field experiments (Table 4).

4. Discussion

The findings of this study have highlighted the impact of F. limonia essential oil against An. arabiensis larvae. The mortality of the larvae in both laboratory and semi-field was found to be dosage dependent with higher mortality observed in laboratory. These findings are similar to the previous study conducted using larvae of Aedes aegypti, Anopheles stephensi, Culex quinquefasciatus, and An. gambiae s.s. having more mortality in laboratory than semi-field [11]. This mortality decreases in semi-field compared to the laboratory and it might have been attributed to the exposure of the essential oil to the sunlight, which might cause compound degradation into secondary metabolites with low toxicity [12]. To maintain the effectiveness of the botanical larvicides, repeated application is needed frequently [13]. The modification of the plant-based biolarvicides is of paramount importance to extend its longevity in environment by making it in slow-release technology. This technology has been practical to Bacillus thuringiensis israelensis (Bti), which in application lasts for 5–7 days [14, 15], but with improved slow-release technology, it has lasted active against larvae for 6 months with no effects to non-targeted organisms [3, 16].

In recent years, the non-particle technologies have enhanced natural products to be more stable and effective. The recent nanoparticles incorporated in natural products have seen to be effective for public health and agriculture pests [17].

The larval source management currently is mostly done with frequent application of organophosphate [15] and insect growth regulators [18, 19]. So, taking up plant- and fungal-based natural product in improved synthesis in small-scale trials can be paving a way to manage insecticide resistance and reduce vector abundance. The findings of this study have shown that the essential oils of F. limonia have impact on mosquito mortality, but in semi-field environment has to be modified to maintain the laboratory observed mortality results.

The larvicidal mortality seen in this study might have been caused by the occurrence of β-pinene and estragole (methyl chavicol). Estragole is a common chemical constituent in plants’ essential oils [20]. Essential oils with methyl chavicol from different have shown high mortality against mosquito larvae. Also, this compound has shown to exhibit fumigant and contact toxicity against Ceratitis capitata, Bactrocera dorsalis, Bactrocera cucurbitae [21], and other storage post-harvest pests [22, 23]. In F. Limonia, β-pinene occurrence was higher and past studies have shown high mortality effect of larvae [24]. The β-pinene-rich in essential oil has shown to impact mortality of Aedes aegypti fourth instar Ae. aegypti larvae. Also, there might be an impact of elements considered to be minor components of the essential oils in larvicidal activity of essential oils [25]. In Ocimum suave essential oils, the linalool among the least occurring ingredient was found to be a major source of mortality [26]. In this case, the natural products from plants have shown to be the major alternative of synthetic pesticides if well moderated and composed.

5. Conclusion

The findings of this study have shown that the essential oils of F. limonia have impact on mosquito mortality, but in semi-field environment has to be modified to maintain the laboratory observed mortality results.

Data Availability

All data generated in this study have been provided in the manuscript.

Ethical Approval

This study did not require ethical clearance.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

Authors wish to thank insectary staff, Mr. Adrian Massawe and Ibrahim Sungi for rearing mosquitoes throughout, Ms. Grace Jayombo for a continuous support during experimental setup, and TPRI for availing its infrastructure to support this study.

References

R. Pwalia, J. Joannides, A. Iddrisu et al., “High insecticide resistance intensity of Anopheles gambiae (s.l.) and low efficacy of pyrethroid LLINs in Accra, Ghana,” Parasites & Vectors, vol. 12, no. 1, p. 299, 2019.
View at: Publisher Site | Google Scholar
WHO, World malaria report, 20 Years of Global Progress and Challenges, World Health Organization, Geneva, 2020.
S. C. Kahindi, S. Muriu, Y. A. Derua et al., “Efficacy and persistence of long-lasting microbial larvicides against malaria vectors in western Kenya highlands,” Parasites & Vectors, vol. 11, no. 1, p. 438, 2018.
View at: Publisher Site | Google Scholar
P. Vivekanandhan, S. Deepa, E. J. Kweka, and M. S. Shivakumar, “Toxicity of fusarium oxysporum-VKFO-01 derived silver nanoparticles as potential inseciticide against three mosquito vector species (Diptera: Culicidae),” Journal of Cluster Science, vol. 29, no. 6, pp. 1139–1149, 2018.
View at: Publisher Site | Google Scholar
P. Vivekanandhan, K. Swathy, D. Kalaimurugan et al., “Larvicidal toxicity of Metarhizium anisopliae metabolites against three mosquito species and non-targeting organisms,” PLoS One, vol. 15, no. 5, article e0232172, 2020.
View at: Publisher Site | Google Scholar
K. Kannathasan, A. Senthilkumar, and V. Venkatesalu, “Mosquito larvicidal activity of methyl-p-hydroxybenzoate isolated from the leaves of Vitex trifolia Linn,” Acta Tropica, vol. 120, no. 1–2, pp. 115–118, 2011.
View at: Publisher Site | Google Scholar
J. N. Ijumba, F. Mosha, and S. Lindsay, “Malaria transmission risk variations derived from different agricultural practices in an irrigated area of northern Tanzania,” Medical and Veterinary Entomology, vol. 16, no. 1, pp. 28–38, 2002.
View at: Publisher Site | Google Scholar
H. S. Kivuyo, P. H. Mbazi, D. S. Kisika et al., “Performance of five food regimes on Anopheles gambiae Senso Stricto larval rearing to adult emergence in insectary,” PLoS One, vol. 9, no. 10, p. e110671, 2014.
View at: Publisher Site | Google Scholar
F. P. Mdoe, G. Nkwengulila, M. Chobu et al., “Larvicidal effect of disinfectant soap on Anopheles gambiae s.s (Diptera: Culicidae) in laboratory and semifield environs,” Parasites & Vectors, vol. 7, no. 1, p. 211, 2014.
View at: Publisher Site | Google Scholar
D. J. Finney, Probit Analysis: A Statistical Treatment of the Sigmoid Response Curve, Cambridge University Press, Cambridge, 1952.
T. Veni, T. Pushpanathan, and J. Mohanraj, “Larvicidal and ovicidal activity of Terminalia chebula Retz. (family: Combretaceae) medicinal plant extracts against Anopheles stephensi, Aedes aegypti and Culex quinquefasciatus,” Journal of Parasitic Diseases, vol. 41, no. 3, pp. 693–702, 2017.
View at: Publisher Site | Google Scholar
E. J. Kweka, M. Nyindo, F. Mosha, and A. G. Silva, “Insecticidal activity of the essential oil from fruits and seeds of Schinus terebinthifolia Raddi against African malaria vectors,” Parasites & Vectors, vol. 4, no. 1, pp. 129–129, 2011.
View at: Publisher Site | Google Scholar
Y. C. Yang, S. G. Lee, H. K. Lee, M. K. Kim, S. H. Lee, and H. S. Lee, “A piperidine amide extracted from Piper longum L. fruit shows activity against Aedes aegypti mosquito larvae,” Journal of Agricultural and Food Chemistry, vol. 50, no. 13, pp. 3765–3767, 2002.
View at: Publisher Site | Google Scholar
H. D. Mazigo, L. E. G. Mboera, S. F. Rumisha, and E. J. Kweka, “Malaria mosquito control in rice paddy farms using biolarvicide mixed with fertilizer in Tanzania: semi-field experiments,” Malaria Journal, vol. 18, no. 1, p. 226, 2019.
View at: Publisher Site | Google Scholar
N. Berlin Rubin, L. E. Mboera, A. Lesser, M. L. Miranda, and R. Kramer, “Process evaluation of a community-based microbial larviciding intervention for malaria control in rural Tanzania,” International Journal of Environmental Research, vol. 17, no. 19, p. 7309, 2020.
View at: Google Scholar
Y. A. Derua, S. C. Kahindi, F. W. Mosha et al., “Microbial larvicides for mosquito control: impact of long lasting formulations of Bacillus thuringiensis var. israelensis and Bacillus sphaericus on non-target organisms in western Kenya highlands,” Ecology and Evolution, vol. 8, no. 15, pp. 7563–7573, 2018.
View at: Publisher Site | Google Scholar
V. Rajkumar, C. Gunasekaran, C. A. Paul, and J. Dharmaraj, “Development of encapsulated peppermint essential oil in chitosan nanoparticles: characterization and biological efficacy against stored-grain pest control,” Pesticide Biochemistry and Physiology, vol. 170, p. 104679, 2020.
View at: Publisher Site | Google Scholar
P. V. Gonzalez and L. Harburguer, “Lufenuron can be transferred by gravid Aedes aegypti females to breeding sites and can affect their fertility, fecundity and blood intake capacity,” Parasites & Vectors, vol. 13, no. 1, p. 257, 2020.
View at: Publisher Site | Google Scholar
N. Gunathilaka, T. Ranathunga, D. Hettiarachchi, L. Udayanga, and W. Abeyewickreme, “Field-based evaluation of novaluron EC10 insect growth regulator, a chitin synthesis inhibitor against dengue vector breeding in leaf axils of pineapple plantations in Gampaha District, Sri Lanka,” Parasites & Vectors, vol. 13, no. 1, p. 228, 2020.
View at: Publisher Site | Google Scholar
A. Senthilkumar, M. Jayaraman, and V. Venkatesalu, “Chemical constituents and larvicidal potential of Feronia limonia leaf essential oil against Anopheles stephensi, Aedes aegypti and Culex quinquefasciatus,” Parasitology Research, vol. 112, no. 3, pp. 1337–1342, 2013.
View at: Publisher Site | Google Scholar
C. Ling Chang, I. Kyu Cho, and Q. X. Li, “Insecticidal activity of basil oil, trans-anethole, estragole, and linalool to adult fruit flies of Ceratitis capitata, Bactrocera dorsalis, and Bactrocera cucurbitae,” Journal of Economic Entomology, vol. 102, no. 1, pp. 203–209, 2009.
View at: Publisher Site | Google Scholar
D. H. Kim and Y. J. Ahn, “Contact and fumigant activities of constituents of Foeniculum vulgare fruit against three coleopteran stored-product insects,” Pest Management Science: Formerly Pesticide Science, vol. 57, no. 3, pp. 301–306, 2001.
View at: Publisher Site | Google Scholar
C. F. Wang, K. Yang, H. M. Zhang et al., “Components and insecticidal activity against the maize weevils of Zanthoxylum schinifolium fruits and leaves,” Molecules, vol. 16, no. 4, pp. 3077–3088, 2011.
View at: Publisher Site | Google Scholar
B. Conti, A. Canale, A. Bertoli, F. Gozzini, and L. Pistelli, “Essential oil composition and larvicidal activity of six Mediterranean aromatic plants against the mosquito Aedes albopictus (Diptera: Culicidae),” Parasitology Research, vol. 107, no. 6, pp. 1455–1461, 2010.
View at: Publisher Site | Google Scholar
W. Silva, G. Dória, R. Maia et al., “Effects of essential oils on Aedes aegypti larvae: alternatives to environmentally safe insecticides,” Bioresource Technology, vol. 99, no. 8, pp. 3251–3255, 2008.
View at: Publisher Site | Google Scholar
E. Shaaya, U. Ravid, N. Paster, B. Juven, U. Zisman, and V. Pissarev, “Fumigant toxicity of essential oils against four major stored-product insects,” Journal of Chemical Ecology, vol. 17, no. 3, pp. 499–504, 1991.
View at: Publisher Site | Google Scholar

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Copyright © 2023 Eliningaya J. Kweka et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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