Ovicidal, pupicidal, adulticidal, and repellent activity of Helicteres velutina K. Schum against Aedes aegypti L. (Diptera: Culicidae)

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Diegina Araújo Fernandes
Hyago Luiz Rique
Louise Helena Guimarães de Oliveira
Wilias Greison Silva Santos
Maria de Fátima Vanderlei de Souza
Fabiola da Cruz Nunes

Abstract

Aedes aegypti is a vector of emerging and neglected diseases, such as dengue, chikungunya, and Zika. Helicteres velutina, known as “pitó” in Brazil, is traditionally used as an insect repellent, and several studies have demonstrated its larvicidal activity. The aim of this study was to investigate this species and evaluate its potential ovicidal, pupicidal, adulticidal, and repellent activity. The viability of the eggs was evaluated using different concentrations of the test substances for 25 days. The hexane fraction killed 72.7% of the eggs, while dichloromethane killed 67.7%. The survival of the pupae and adults was verified after 72 h and 48 h, respectively. The LC50 for the hexane and dichloromethane fractions was 0.12 mg/mL and 8.85 mg/mL for pupae, 8.01 mg/mL and 0.74 mg/mL for adults (tarsal test), and 0.05 mg/mL and 0.23 mg/mL for adults (body test), respectively. Repellency was assessed for 240 min using neonatal Wistar rats on a Y-tube olfactometer. The hexane fraction attracted mosquitoes to the test chamber, while the dichloromethane fraction had a repellent action. The 7,4’-di-O-methyl-8-O-sulfate flavone provides greater repellency, and this finding is similar to the results of the in silico studies that have shown the potential of this substance against adult mosquitoes. This suggests that 7,4’-di-O-methyl-8-O-sulfate flavone may be one of the substances present in the extract from aerial parts of H. velutina that is responsible for the repellent activity mentioned in traditional medicine. These findings provide a better understanding of the insecticidal and repellent activity of the extract, fraction, and compounds isolated from H. velutina against Ae. aegypti, thereby revealing its potential in the development of a more effective botanical insecticide.

Article Details

How to Cite
Araújo Fernandes, D., Luiz Rique, H., Guimarães de Oliveira, L. H., Greison Silva Santos, W., Vanderlei de Souza, M. de F., & da Cruz Nunes, F. (2021). Ovicidal, pupicidal, adulticidal, and repellent activity of Helicteres velutina K. Schum against Aedes aegypti L. (Diptera: Culicidae). Brazilian Journal of Veterinary Medicine, 43(1), e102120. https://doi.org/10.29374/2527-2179.bjvm112120
Section
Scientific articles

References

Ajaegbu, E. E., Danga, S. P. Y., Chijoke, I. U., & Okoye, F. B. C. (2016). Mosquito adulticidal activity of the leaf extracts of Spondias mombin L. against Aedes aegypti L. and isolation of active principles. Journal of Vector Borne Diseases, 53(1), 17-22. PMid:27004574.

Amerasan, D., Murugan, K., Kovendan, K., Mahesh Kumar, P., Panneerselvam, C., Subramaniam, J., John William, S., & Hwang, J. S. (2012). Adulticidal and repelente properties of Cassia tora Linn. (Family: Caesalpinaceae) against Culex quinquefasciatus, Aedes aegypti, and Anopheles stephensi. Parasitology Research, 111(5), 1953-1964. http://dx.doi.org/10.1007/s00436-012-3042-3. PMid:22821231.

Castillo, R. M., Stashenko, E., & Duque, J. E. (2017). Insecticidal and repellent activity of several plant-derived essential oils against Aedes aegypti. Journal of the American Mosquito Control Association, 33(1), 25-35. http:// dx.doi.org/10.2987/16-6585.1. PMid:28388322.

Chellappandian, M., Thanigaivel, A., Vasantha-Srinivasan, P., Edward-Sam, E., Ponsankar, A., Selin-Rani, S., Kalaivani, K., Senthil-Nathan, S., & Benelli, G. (2018). Toxicological effects of Sphaeranthus indicus Linn. (Asteraceae) leaf essential oil against human disease vectors, Culex quinquefasciatus Say and Aedes aegypti Linn., and impacts on a beneficial mosquito predator. Environmental Science and Pollutuin Research, 25(11), 10294-10306. http://dx.doi.org/10.1007/s11356-017-8952-2.

Fernandes, D. A., Assis, E. B., Souza, M. S. R., & Souza, M. F. V. (2020a). Helicteres L. species (Malvaceae sensu lato) as source of new drugs: A review. Quimica Nova, 43(6), 787-803. http://dx.doi.org/10.21577/0100-4042.20170533.

Fernandes, D. A., Barros, R. P. C., Teles, Y. C. F., Oliveira, L. H. G., Lima, J. B., Scotti, M. T., Nunes, F. C., Conceição, A. S., & Vanderlei de Souza, M. F. (2019). Larvicidal Compounds Extracted from Helicteres velutina K. Schum (Sterculiaceae) Evaluated against Aedes aegypti L. Molecules (Basel, Switzerland), 24(12), 2315. http://dx.doi. org/10.3390/molecules24122315. PMid:31234501.

Fernandes, D. A., Oliveira, L. H. G., Rique, H. L., Souza, M. F. V., & Nunes, F. C. (2020b). Insights on tha larvicidal mechanism of action of fractions and compounds from aerial parts of Helicteres velutina K. Schum against Aedes aegypti L. Molecules (Basel, Switzerland), 25(13), 3015. http://dx.doi.org/10.3390/molecules25133015. PMid:32630318.

Fernandes, D. A., Souza, M. S. R., Teles, Y. C. F., Oliveira, L. H. G., Lima, J. B., Conceição, A. S., Nunes, F. C., Silva, T. M. S., & Souza, M. F. V. (2018). New sulphated flavonoids and larvicidal activity of Helicteres velutina K. Schum (Sterculiaceae). Molecules (Basel, Switzerland), 23(11), 2784. http://dx.doi.org/10.3390/molecules23112784. PMid:30373225.

Govindarajan, M. (2011). Mosquito larvicidal and ovicidal activity of Cardiospermum halicacabum Linn. (Family: Sapindaceae) leaf extract against Culex quinquefasciatus (Say) and Aedes aegypti (Linn.) (Diptera: Culicidae). European Review for Medical and Pharmacological Sciences, 15(7), 787-794. PMid:21780548.

Govindarajan, M., & Rajeswary, M. (2015). Ovicidal and adulticidal potential of leaf and seed extract of Albizia lebbeck (L.) Benth. (Family: Fabaceae) against Culex quinquefasciatus, Aedes aegypti, and Anopheles stephensi (Diptera: Culicidae). Parasitology Research, 114(5), 1949-1961. http://dx.doi.org/10.1007/s00436-015-4384-4. PMid:25681143.

Govindarajan, M., & Sivakumar, R. (2012). Adulticidal and repelente properties of indigenous plant extracts against Culex quinquefasciatus and Aedes aegypti (Diptera: Culicidae). Parasitology Research, 110(5), 1607-1620. http://dx.doi.org/10.1007/s00436-011-2669-9. PMid:22009267.

Govindarajan, M., & Sivakumar, R. (2014). Larvicidal, ovicidal and adulticidal efficacy of Erythrina indica (Lam.) (Family: Fabaceae) against Anopheles stephensi, Aedes aegypti, ans Culex quinquefasciatus (Diptera: Culicidae). Parasitology Research, 113(2), 777-791. http://dx.doi.org/10.1007/s00436-013-3709-4. PMid:24322290.

Imam, H., Zarnigar, Sofi, G., & Seikh, A. (2014). The basic rules and methods of mosquito rearing (Aedes aegypti). Tropical Parasitology, 4(1), 53-55. http://dx.doi.org/10.4103/2229-5070.129167. PMid:24754030.

Keziah, E. A., Nukenine, E. N., Danga, S. P. Y., Younoussa, L., & Esimone, C. O. (2015). Creams formulated with Ocimum gratissimum L. and Lantana camara L. crude extracts and fractions as mosquito repellents against Aedes aegypti L. (Diptera: Culicidae). Journal of Insect Science, 15(1), 1-5. http://dx.doi.org/10.1093/jisesa/iev025. PMid:25881633.

Kovendan, K., Murugan, K., Mahesh Kumar, P., Thiyagarajan, P., & John William, S. (2013). Ovicidal, repellent, adulticidal and field evaluations of plant extract against dengue, malaria and filarial vectors. Parasitology Research, 112(3), 1205-1219. http://dx.doi.org/10.1007/s00436-012-3252-8. PMid:23271569.

Kraemer, M. U., Sinka, M. E., Duda, K. A., Mylne, A. Q., Shearer, F. M., Barker, C. M., Moore, C. G., Carvalho, R. G., Coelho, G. E., Van Bortel, W., Hendrickx, G., Schaffner, F., Elyazar, I. R., Teng, H. J., Brady, O. J., Messina, J. P., Pigott, D. M., Scott, T. W., Smith, D. L., Wint, G. R., Golding, N., & Hay, S. I. (2015). The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus. eLife, 4, e08347. http://dx.doi.org/10.7554/eLife.08347. PMid:26126267.

Kovendan, K., Murugan, K., Kumar, P.M., Thiyagarajan, P., William, S.J. (2013). Ovicidal, repellent, adulticidal and field evaluations of plant extract against dengue, malaria and filarial vectors. Parasitology Research, 112(3),1205-1219. http://dx.doi.org/10.1007/s00436-012-3252-8. PMid: 23271569

Kumar, D., Kumar, G., & Agrawal, V. (2018). Green synthesis of silver nanoparticles using Holarrhena antidysenterica (L.) Wall. Bark extract and their larvicidal activity against dengue and filariasis vectors. Parasitology Research, 117(2), 377-389. http://dx.doi.org/10.1007/s00436-017-5711-8. PMid:29250727.

Kumar, N. P., Suresh, A., Vanamail, P., Sabesan, S., Krishnamoorthy, K. G., Mathew, J., Jose, V. T., & Jambulingam, P. (2011). Chikungunya vírus outbreak in Kerala, India, 2007: A seroprevalence study. Memorias do Instituto Oswaldo Cruz, 106(8), 912-916. http://dx.doi.org/10.1590/S0074-02762011000800003. PMid:22241110.

Kumar, P. M., Murugan, K., Kalimuthu, K., Panneerselvam, C., Kumar, K. P., Amerasan, D., Subramaniam, J., Kalimuthu, K., & Natarai, T. (2012). Mosquitocidal activity of Solanum xanthocarpum fruit extract and copepod Mesocyclops thermocyclopoides for the control of dengue vector Aedes aegypti. Parasitology Research, 111(2), 609-618. http://dx.doi.org/10.1007/s00436-012-2876-z. PMid:22398832.

Lalthazuali, & Mathew, N. (2017). Mosquito repelente activity of volatile oils from selected aromatic plants. Parasitology Research, 116(2), 821-825. http://dx.doi.org/10.1007/s00436-016-5351-4. PMid:28013374.

Leta, S., Beyene, T. J., De Clercq, E. M., Amenu, K., Kraemer, M. U. G., & Revie, C. W. (2018). Global risk mapping for major diseases transmited by Aedes aegypti and Aedes albopictus. International Journal of Infectious Diseases, 67, 25-35. http://dx.doi.org/10.1016/j.ijid.2017.11.026. PMid:29196275.

Mukandiwa, L., Eloff, J. N., & Naidoo, V. (2016). Larvicidal activity of leaf extracts and seselin from Clausena anisata (Rutaceae) against Aedes aegypti. South African Journal of Botany, 100, 169-173. http://dx.doi.org/10.1016/j. sajb.2015.05.016.

Munusamy, R. G., Appadurai, D. R., Kuppusamy, S., Michael, G. P., & Savarimuthu, I. (2016). Ovicidal and larvicidal activities of some plant extracts against Aedes aegypti L. and Culex quinquefasciatus Say (Diptera: Culicidae). Asian Pacific Journal of Tropical Disease, 6(6), 468-471. http://dx.doi.org/10.1016/S2222-1808(16)61070-8.

Murugan, K., Mahesh Kumar, P., Kovendan, K., Amerasan, D., Subrmaniam, J., & Hwang, J. S. (2012). Larvicidal, pupicidal, repelente and adulticidal activity of Citrus sinensis orange peel extracts against Anopheles stephensi, Aedes aegypti and Culex quinquefasciatus (Diptera: Culicidae). Parasitology Research, 111(4), 1757-1769. http:// dx.doi.org/10.1007/s00436-012-3021-8. PMid:22797605.

Nunes, F. C., Leite, J. A., Oliveira, L. H. G., Sousa, P. A. P. S., Menezes, M. C., Moraes, J. P. S., Mascarenhas, S. R., & Braga, V. A. (2015). The larvicidal activity of Agave sisalana against L4 larvae of Aedes aegypti is mediated by internal necrosis and inhibition of nitric oxide production. Parasitology Research, 114(2), 543-549. http:// dx.doi.org/10.1007/s00436-014-4216-y. PMid:25395257.

Nunes, F. C., Oliveira, L. H. G., Sousa, P. A. P. S., & Rique, H. L. (2019a). Biotecnologia no controle de mosquitos transmissores de arboviroses bioensaios para avaliação da atividade inseticida em mosquitos adultos. In N. A. Cardoso, R. R. Rocha & M. V. Laurindo (Orgs.), As Ciências Biológicas e da Saúde na Contemporaneidade 2 (pp. 94-102, cap., 10). Atena Editora. http://dx.doi.org/10.22533/at.ed.16619280310.

Nunes, F. C., Souza, M. F. V., Fernandes, D. A., Ferreira, M. D. L., Oliveira, L. H. G., Figueiredo, G., & Rique, H. L. (2019b). Bioensaio para avaliação da atividade repelente em mosquitos adultos. In R. M. Freitas (Org.), Ciências Biológicas: Campo Promissor em Pesquisa (pp. 72-84, cap. 9 ). Ponta Grossa. http://dx.doi.org/10.22533/at.ed.8191913119.

Pluempanupat, S., Kumrungsee, N., Pluempanupat, W., Ngamkitpinyo, K., Chavasiri, W., Bullangpoti, V., & Koul, O. (2013). Laboratory evaluation of Dalbergia oliveri (Fabaceae: Fabales) extracts and isolated isoflavonoids on Aedes aegypti (Diptera: Culicidae) mosquitoes. Industrial Crops and Products, 44, 653-658. http://dx.doi. org/10.1016/j.indcrop.2012.09.006.

Ravindran, J., Samuel, T., Alex, E., & William, J. (2012). Adulticidal activity of Ageratum houstonianum Mill. (Asteraceae) leaf extracts against three vector mosquito species (Diptera: Culcidae). Asian Pacific Journal of Tropical Disease, 2(3), 177-179. http://dx.doi.org/10.1016/S2222-1808(12)60042-5.

Reegan, A. D., Gandhi, M. R., Paulraj, M. G., & Ignacimuthu, S. (2015). Ovicidal and oviposition deterrent activities of medicinal plant extracts against Aedes aegypti L. and Culex quinquefasciatus Say Mosquitoes (Diptera: Culicidae). Osong Public Health and Research Perspectives, 6(1), 64-69. http://dx.doi.org/10.1016/j. phrp.2014.08.009. PMid:25737834.

Reegan, A. D., Gandhi, M. R., Paulraj, M. G., Balakrishna, K., & Ignacimuthu, S. (2014). Effect of niloticin, a protolimonoid isolated from Limonia acidissima L. (Rutaceae) on the immature stages of dengue vector Aedes aegypti L. (Diptera: Culicidae). Acta Tropica, 139, 67-76. http://dx.doi.org/10.1016/j.actatropica.2014.07.002. PMid:25019220.

Rodriguez, S. D., Drake, L. L., Price, D. P., Hammond, J. I., & Hansen, I. A. (2015). The efficacy of some commercially available insect repellents for Aedes aegypti (Diptera: Culicidae) and Aedes albopictus (Diptera: Culicidae). Journal of Insect Sciense, 15(1), 140. http://dx.doi.org/1093/jisesa/iev125.

Rojas-Pinzón, P. A., Silva-Fernández, J. J., & Dussán, J. (2018). Laboratory and simulated-field bioassays for assessing mixed cultures of Lysinibacillus sphaericus against Aedes aegypti (Diptera: Culicidae) larvae resistant to temephos. Applied Entomology and Zoology, 53(2), 183-191. http://dx.doi.org/10.1007/s13355-017-0534-8.

Santos, E. A., Carvalho, C. M., Costa, A. L. S., Conceição, A. S., Moura, F. B. P., & Santana, A. E. G. (2012). Bioactivity evaluation of plant extracts used in indigenous medicine against the Snail, Biomphalaria glabrata, and the Larvae of Aedes aegypti. Evidence-Based Complementary and Alternative Medicine, 2012, 846583. http://dx.doi.org/10.1155/2012/846583. PMid:22194773

Silva, S. L. C., Gualberto, S. A., Carvalho, K. S., & Fries, D. D. (2014). Avaliação da atividade larvicida de extratos obtidos do caule de Croton linearifolius Mull. Arg. (Euphorbiaceae) sobre larvas de Aedes aegypti (Linnaes, 1762) (Diptera: Culicidae). Biotemas, 27(2), 79-85. http://dx.doi.org/10.5007/2175-7925.2014v27n2p79.

Simmonds, M. S. J. (2001). Importance of flavonoids in insect-plany interactions: Feeding and oviposition. Phytochemistry, 56(3), 245-252. http://dx.doi.org/10.1016/S0031-9422(00)00453-2. PMid:11243451.

Torres, R. C., Garbo, A. G., & Walde, R. Z. M. L. (2015). Larvicidal activity of Garcinia mangostana fruit wastes against dengue vector Aedes aegypti. Journal of Animal and Plant Sciences, 25(4), 1187-1190.

Vivekanandhan, P., Senthil-Nathan, S., & Shivakumar, M. S. (2018). Larvicidal, pupicidal and adult smoke toxic effects of Acanthospermum hispidum (DC) leaf crude extracts against mosquito vectors. Physiological and Molecular Plant Pathology, 101, 156-162. http://dx.doi.org/10.1016/j.pmpp.2017.05.005.

Wang, Y. H., Chang, M. M., Wang, X. L., Zheng, A. H., & Zou, Z. (2018). The immune strategies of mosquito Aedes aegypti against microbial infection. Developmental and Comparative Immunology, 83, 12-21. http://dx.doi.org/10.1016/j.dci.2017.12.001. PMid:29217264.

World Health Organization – WHO. (2005). Guidelines for laboratory and field testing of mosquito larvicides (pp. 1-41). WHO. https://apps.who.int/iris/handle/10665/69101

World Health Organization – WHO. (2013). Guidelines for efficacy testing of Spatial repellents: Control of neglected tropical diseases who pesticide evaluation scheme (pp. 1-58). WHO. https://apps.who.int/iris/bitstream/handle /10665/78142/9789241505024_eng.pdf

Yu, K. X., Wong, C. L., Ahmad, R., & Jantan, I. (2015). Mosquitocidal and oviposition repellent activities of the extracts of seaweed Bryopsis pennata on Aedes aegypti and Aedes albopictus. Molecules (Basel, Switzerland), 20(8), 14082-14102. http://dx.doi.org/10.3390/molecules200814082. PMid:26247928.