Abstract
Sextonia rubra is an Amazonian tree known for the larvicide activity of its wood extracts against Aedes aegypti. However, the lipophilic character of this extract presents an obstacle to the development of vector management products. The purpose of this study was to assess the feasibility, efficacy, and selectivity of a water-soluble formulation based on a S. rubra wood extract characterized by its larvicidal compounds rubrenolide and rubrynolide. Using reference and wild strains, larval mortality, oviposition behavior, hatching response, and fitness of mosquitoes exposed to the extract were evaluated. Laboratory eco- and cytotoxicity bioassays were performed concurrently. The extract showed larvicidal efficacy and no repulsive effect on oviposition, thus supporting its use in the treatment of breeding sites. The formulation exhibited strong acute toxicity, leading to 100% larval mortality in 2–4 days in either the dry or rainy season at a test dose of 102 µg/ml under semi-operational conditions, with residual activity maintained during the 5 weeks of testing. The formulation allowed for a noticeable gain in selectivity compared with the extract, with lower immobilization rates for Daphnia magna and Chironomus riparius, and no significant toxicity towards human cell lines (IC50 > 100 µg/ml). These results highlight the potential of the S. rubra-based formulation for the management of Ae. aegypti larvae, including strains showing resistance to conventional insecticides.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and analyzed during the current study are available from the corresponding author on reasonable request.
References
Agrawal AA, Weber MG (2015) On the study of plant defence and herbivory using comparative approaches: how important are secondary plant compounds. Ecol Lett 18:985–991. https://doi.org/10.1111/ele.12482
Amer A, Mehlhorn H (2006) Persistency of larvicidal effects of plant oil extracts under different storage conditions. Parasitol Res 99:473–477. https://doi.org/10.1007/s00436-006-0183-2
Awouafack MD, McGaw LJ, Gottfried S et al (2013) Antimicrobial activity and cytotoxicity of the ethanol extract, fractions and eight compounds isolated from Eriosema robustum (Fabaceae). BMC Complement Altern Med 13:289–297. https://doi.org/10.1186/1472-6882-13-289
Bailly S, Rousset D, Fritzell C et al (2021) Spatial distribution and burden of emerging arboviruses in French Guiana. Viruses 13:1299. https://doi.org/10.3390/v13071299
Benelli G (2015) Research in mosquito control: current challenges for a brighter future. Parasitol Res 114:2801–2805. https://doi.org/10.1007/s00436-015-4586-9
Benelli G (2020) On a magical mystery tour of green insecticide research: current issues and challenges. Molecules 25:5014. https://doi.org/10.3390/molecules25215014
Benelli G, Mehlhorn H (2016) Declining malaria, rising of dengue and Zika virus: insights for mosquito vector control. Parasitol Res 115:1747–1754. https://doi.org/10.1007/s00436-016-4971-z
Borges JCM, Haddi K, Oliveira EE et al (2019) Mosquiticidal and repellent potential of formulations containing wood residue extracts of a Neotropical plant, Tabebuia heptaphylla. Ind Crops Prod 129:424–433. https://doi.org/10.1016/j.indcrop.2018.12.022
Carvalho FD, Moreira LA (2017) Why is Aedes aegypti Linnaeus so successful as a species? Neotrop Entomol 46:243–255. https://doi.org/10.1007/s13744-017-0520-4
Clervil E, Bossu J, Duchemin JB et al (2023) Sextonia rubra (Mez.) van der Werff sawmills residues as a valuable resource for the production of larvicidal extracts against Ae. aegypti Linnaeus (Diptera: Culicidae). Ind Crops Prod 193:116162. https://doi.org/10.1016/j.indcrop.2022.116162
Cos P, Vlietinck AJ, Vanden BD, Maes L (2006) Anti-infective potential of natural products: how to develop a stronger in vitro “proof-of-concept.” J Ethnopharmacol 106:290–302. https://doi.org/10.1016/j.jep.2006.04.003
Darriet F, Marcombe S, Etienne M et al (2010) Field evaluation of pyriproxyfen and spinosad mixture for the control of insecticide resistant Aedes aegypti in Martinique (French West Indies). Parasit Vectors 3:1–8. https://doi.org/10.1186/1756-3305-3-88
de Oliveira JL, Campos EVR, Bakshi M et al (2014) Application of nanotechnology for the encapsulation of botanical insecticides for sustainable agriculture: prospects and promises. Biotechnol Adv 32:1550–1561. https://doi.org/10.1016/j.biotechadv.2014.10.010
de Thoisy B, Duron O, Epelboin L et al (2021) Ecology, evolution, and epidemiology of zoonotic and vector-borne infectious diseases in French Guiana: transdisciplinarity does matter to tackle new emerging threats. Infect Genet Evol 93:104916. https://doi.org/10.1016/j.meegid.2021.104916
Dusfour I, Zorrilla P, Guidez A et al (2015) Deltamethrin resistance mechanisms in Aedes aegypti populations from three French overseas territories worldwide. PLoS Negl Trop Dis 9:1–17. https://doi.org/10.1371/journal.pntd.0004226
ECHA (2022a) Fatty acids, rape-oil, Me esters. https://echa.europa.eu/fr/registration-dossier/-/registered-dossier/16753. Accessed 11 Mar 2022
ECHA (2022b) Alkyl Polyglycosides (APG). https://echa.europa.eu/fr/registration-dossier/-/registered-dossier/14407/12. Accessed 11 Mar 2022
Egito E, Amaral-Machado L, Alencar E, Oliveira A (2020) Microemulsion systems: from the design and architecture to the building of a new delivery system for multiple—route drug delivery. Drug Deliv Transl Res. https://doi.org/10.1007/s13346-020-00872-8
El Maghrbi AA, Hosni MM (2014) Influence of some plant extracts on the ovi-position behavior of Aedes fluviatilis and Culex quinquifasciatus. Int J Vet Sci Med 2:95–98. https://doi.org/10.1016/j.ijvsm.2014.04.003
Epelboin Y, Chaney SC, Guidez A et al (2018) Successes and failures of sixty years of vector control in French Guiana: What is the next step? Mem Inst Oswaldo Cruz 113:e170398. https://doi.org/10.1590/0074-02760170398
Epelboin Y, Wang L, Gianetto QG et al (2021) CYP450 core involvement in multiple resistance strains of Aedes aegypti from French Guiana highlighted by proteomics, molecular and biochemical studies. PLoS ONE 16:1–22. https://doi.org/10.1371/journal.pone.0243992
Falkowski M, Jahn-Oyac A, Ferrero E et al (2016) Assessment of a simple compound-saving method to study insecticidal activity of natural extracts and pure compounds against mosquito larvae. J Am Mosq Control Assoc 32:337–340. https://doi.org/10.2987/16-6613.1
Falkowski M, Jahn-Oyac A, Odonne G et al (2020) Towards the optimization of botanical insecticides research: Aedes aegypti larvicidal natural products in French Guiana. Acta Trop 201:105179. https://doi.org/10.1016/j.actatropica.2019.105179
Faucon F, Gaude T, Dusfour I et al (2017) In the hunt for genomic markers of metabolic resistance to pyrethroids in the mosquito Aedes aegypti: An integrated next-generation sequencing approach. PLoS Negl Trop Dis 11:1–20. https://doi.org/10.1371/journal.pntd.0005526
Faustino CG, de Medeiros FA, Galardo AKR et al (2020) Larvicide activity on Aedes aegypti of essential oil nanoemulsion from the Protium heptaphyllum resin. Molecules 25:5333. https://doi.org/10.3390/MOLECULES25225333
Fu T, Houël E, Amusant N et al (2019) Biosynthetic investigation of γ-lactones in Sextonia rubra wood using in situ TOF-SIMS MS/MS imaging to localize and characterize biosynthetic intermediates. Sci Rep 9:1928. https://doi.org/10.1038/s41598-018-37577-5
Geetha D, Tyagi R (2012) Alkyl poly glucosides (APGs) surfactants and their properties: a review. Tenside Surfactants Deterg 49:417–427. https://doi.org/10.3139/113.110212
George DR, Finn RD, Graham KM, Sparagano OA (2014) Present and future potential of plant-derived products to control arthropods of veterinary and medical significance. Parasit Vectors 7:1–12. https://doi.org/10.1186/1756-3305-7-28
Gerwick BC, Sparks TC (2014) Natural products for pest control: an analysis of their role, value and future. Pest Manag Sci 70:1169–1185. https://doi.org/10.1002/ps.3744
Gloria-Soria A, Kellner DA, Brown JE et al (2016) Temporal genetic stability of Stegomyia aegypti (= Aedes aegypti) populations. Med Vet Entomol 30:235–240. https://doi.org/10.1111/mve.12153
Guidez A, Pocquet N, Restrepo J et al (2020) Spatiotemporal multiple insecticide resistance in Aedes aegypti populations in French Guiana: need for alternative vector control. Mem Inst Oswaldo Cruz 115:1–9. https://doi.org/10.1590/0074-02760200313
Houël E, Gonzalez G, Bessière J-M et al (2015) Therapeutic switching: from antidermatophytic essential oils to new leishmanicidal products. Mem Inst Oswaldo Cruz 110:106–113. https://doi.org/10.1590/0074-02760140332
Indrayanto G, Putra GS, Suhud F (2021) Validation of in-vitro bioassay methods: application in herbal drug research. Profiles Drug Subst Excip Relat Methodol 46:273–307. https://doi.org/10.1016/bs.podrm.2020.07.005
Isman MB (2020) Botanical insecticides in the twenty-first century-fulfilling their promise? Annu Rev Entomol 65:233–249. https://doi.org/10.1146/annurev-ento-011019-025010
Isman MB, Grieneisen ML (2014) Botanical insecticide research: many publications, limited useful data. Trends Plant Sci 19:140–145. https://doi.org/10.1016/j.tplants.2013.11.005
Johansson I, Svensson M (2001) Surfactants based on fatty acids and other natural hydrophobes. Curr Opin Colloid Interface Sci 6:178–188. https://doi.org/10.1016/S1359-0294(01)00076-0
Jones RT, Ant TH, Cameron MM, Logan JG (2021) Novel control strategies for mosquito-borne diseases. Philos Trans R Soc b Biol Sci 376:20190802. https://doi.org/10.1098/rstb.2019.0802
Kanis LA, Prophiro JS, Da Silva VE et al (2012) Larvicidal activity of Copaifera sp. (Leguminosae) oleoresin microcapsules against Aedes aegypti (Diptera: Culicidae) larvae. Parasitol Res 110:1173–1178. https://doi.org/10.1007/s00436-011-2610-2
Kanis LA, Rabelo BD, Moterle D et al (2013) Standardized extract of Piper ovatum (Piperaceae) to control Aedes aegypti larvae (Diptera: Culicidae). Ind Crops Prod 50:816–820. https://doi.org/10.1016/j.indcrop.2013.08.034
Kanis LA, Rabelo BD, Moterle D et al (2018) Piper ovatum (Piperaceae) extract/starch-cellulose films to control Aedes aegypti (Diptera: Culicidae) larvae. Ind Crops Prod 122:148–155. https://doi.org/10.1016/j.indcrop.2018.05.055
Kumar PM, Murugan K, Kovendan K et al (2012) Mosquito larvicidal and pupicidal efficacy of Solanum xanthocarpum (Family: Solanaceae) leaf extract and bacterial insecticide, Bacillus thuringiensis, against Culex quinquefasciatus Say (Diptera: Culicidae). Parasitol Res 110:2541–2550. https://doi.org/10.1007/s00436-011-2797-2
Machado FP, Folly D, Salas Enriquez JJ et al (2023) Nanoemulsion of Ocotea indecora (Shott) Mez essential oil: Larvicidal effects against Aedes aegypti. Ind Crops Prod 192:116031. https://doi.org/10.1016/j.indcrop.2022.116031
Maia JD, La Corte R, Martinez J et al (2019) Improved activity of thyme essential oil (Thymus vulgaris) against Aedes aegypti larvae using a biodegradable controlled release system. Ind Crops Prod 136:110–120. https://doi.org/10.1016/j.indcrop.2019.03.040
Miresmailli S, Isman MB (2014) Botanical insecticides inspired by plant-herbivore chemical interactions. Trends Plant Sci 19:29–35. https://doi.org/10.1016/j.tplants.2013.10.002
Oliveira AEMFM, Duarte JL, Amado JRR et al (2016) Development of α larvicidal nanoemulsion with Pterodon emarginatus Vogel oil. PLoS ONE 11:1–16. https://doi.org/10.1371/journal.pone.0145835
Pavela R (2016) Encapsulation—a convenient way to extend the persistence of the effect of eco-friendly mosquito larvicides. Curr Org Chem 20:2674–2680. https://doi.org/10.2174/1385272820666151026231851
Pavela R, Maggi F, Iannarelli R, Benelli G (2019) Plant extracts for developing mosquito larvicides: from laboratory to the field, with insights on the modes of action. Acta Trop 193:236–271. https://doi.org/10.1016/j.actatropica.2019.01.019
Pavela R, Pavoni L, Bonacucina G et al (2004) (2021) Encapsulation of Carlina acaulis essential oil and carlina oxide to develop long - lasting mosquito larvicides: microemulsions versus nanoemulsions. J Pest Sci 94:899–915
Peña-Morán OA, Villarreal ML, Álvarez-Berber L et al (2016) Cytotoxicity, post-treatment recovery, and selectivity analysis of naturally occurring podophyllotoxins from Bursera fagaroides var. fagaroides on breast cancer cell lines. Molecules 21:1013–1024. https://doi.org/10.3390/molecules21081013
Peng Y, Xiao D, Yu G et al (2019) Effect of an eco-friendly o/w emulsion stabilized with amphiphilic sodium alginate derivatives on lambda-cyhalothrin adsorption–desorption on natural soil minerals. J Environ Sci 78:230–238. https://doi.org/10.1016/j.jes.2018.09.025
Renkin M, Fleurackers S, Szwach I, Hreczuch W (2005) Rapeseed methyl ester ethoxylates: a new class of surfactants of environmental and commercial interest. Tenside Surfactants Deterg 42:280–287. https://doi.org/10.3139/113.100269
Richards LA, Dyer LA, Forister ML et al (2015) Phytochemical diversity drives plant–insect community diversity. Proc Natl Acad Sci USA 112:10973–10978. https://doi.org/10.1073/pnas.1504977112
Rodrigues A, Theodoro PNET, Eparvier V et al (2010) Search for antifungal compounds from the wood of durable tropical trees. J Nat Prod 73:1706–1707. https://doi.org/10.1021/np1001412
Rodrigues ABL, Martins RL, de Rabelo É, M, et al (2021) Development of nano-emulsions based on Ayapana triplinervis essential oil for the control of Aedes aegypti larvae. PLoS ONE 16:1–23. https://doi.org/10.1371/journal.pone.0254225
Salazar D, Lokvam J, Mesones I et al (2018) Origin and maintenance of chemical diversity in a species-rich tropical tree lineage. Nat Ecol Evol 2:983–990. https://doi.org/10.1038/s41559-018-0552-0
Salimon J, Salih N, Yousif E (2012) Industrial development and applications of plant oils and their biobased oleochemicals. Arab J Chem 5:135–145. https://doi.org/10.1016/j.arabjc.2010.08.007
Satho T, Dieng H, Ahmad MHI et al (2015) Coffee and its waste repel gravid Aedes albopictus females and inhibit the development of their embryos. Parasit Vectors 8:272–286. https://doi.org/10.1186/s13071-015-0874-6
Seenivasagan T, Sharma A, Yadav R et al (2019) Plant infusions mediate oviposition of malaria, dengue and filariasis vectors: push-pull approach for vector surveillance and control. J Biopestic 12:95–103
Senthil-Nathan S (2020) A Review of resistance mechanisms of synthetic insecticides and botanicals, phytochemicals, and essential oils as alternative larvicidal agents against mosquitoes. Front Physiol 10:1591. https://doi.org/10.3389/fphys.2019.01591
Silva LLS, Fernandes KM, Miranda FR et al (2019) Exposure of mosquito (Aedes aegypti) larvae to the water extract and lectin-rich fraction of Moringa oleifera seeds impairs their development and future fecundity. Ecotoxicol Environ Saf 183:109583. https://doi.org/10.1016/j.ecoenv.2019.109583
Silvério MRS, Espindola LS, Lopes NP, Vieira PC (2020) Plant natural products for the control of Aedes aegypti: the main vector of important arboviruses. Molecules 25:3484. https://doi.org/10.3390/molecules25153484
Soulères O (2021) L’aménagement des forêts de Guyane française. In: Lanly JP, Soulères O (eds) Travailler au service des forêts tropicales, regards croisés de forestiers. L’Harmattan, Paris, pp 37–57
Spafford H, Jardine A, Carver S et al (2007) Laboratory determination of efficacy of a Santalum spicatum extract for mosquito control. J Am Mosq Control Assoc 23:304–311. https://doi.org/10.2987/8756-971X(2007)23[304:LDOEOA]2.0.CO;2
Szwach I, Lukosek M (2017) Comparative evaluation of environmental impact of selected ethoxylate fatty alcohols and ethoxylate fatty acid methyl esters as nonionic surfactants. Pol J Environ Stud 26:1245–1250. https://doi.org/10.15244/pjoes/67748
Tan S, Saad J, Wong L et al (2013) A formulated solvent composition for pesticide. WO 2013/05
Taranta C, Mansour P, Bourgogne M, Henriet M (2002) Oil-in-water emulsion formulation of insecticides. US 2002/00
Tófoli D, Martins L, Matos M et al (2016) Antiproliferative Butyrolactones from Mezilaurus crassiramea. Planta Med Lett 3:e14–e16. https://doi.org/10.1055/s-0035-1568355
Touré S, Nirma C, Falkowski M et al (2017) Aedes aegypti larvicidal sesquiterpene alkaloids from Maytenus oblongata. J Nat Prod 80:384–390. https://doi.org/10.1021/acs.jnatprod.6b00850
Turchen LM, Cosme-Júnior L, Guedes RNC (2020) Plant-derived insecticides under meta-analyses: status, biases, and knowledge gaps. InSects 11:1–13. https://doi.org/10.3390/insects11080532
Villaverde JJ, Sevilla-Morán B, Sandín-España P et al (2014) Biopesticides in the framework of the European Pesticide Regulation (EC) No. 1107/2009. Pest Manag Sci 70:2–5. https://doi.org/10.1002/ps.3663
Von RW, Hill K (1998) Alkyl polyglycosides-properties and applications of a new class of surfactants. Angew Chem Int Ed Engl 37:1328–1345. https://doi.org/10.1002/(SICI)1521-3773(19980605)37:10%3c1328::AID-ANIE1328%3e3.0.CO;2-9
World Health Organisation W (2005) Guidelines for laboratory and field testing of mosquito larvicides
Zhang F, Gu W, Xu P et al (2011) Effects of alkyl polyglycoside (APG) on composting of agricultural wastes. Waste Manag 31:1333–1338. https://doi.org/10.1016/j.wasman.2011.02.002
Funding
The SextoniAedes project (Valorization of molecules from Sextonia rubra wood wastes for the formulation of larvicidal products against the Aedes aegypti mosquito: effectiveness and selectivity) was funded by the European Regional Development Funds (FEDER) for French Guiana (ERDF OP, Agreement No. FEDER/2017/N°65). This work benefited from an “Investissement d'Avenir” Grant managed by Agence Nationale de la Recherche (Infrastructure Nationale en Biologie Santé “ANAEE-France” ANR-11-INBS-0001) through the use of the U3E INRA1036 PEARL platform. This work has benefited from an "Investissement d’Avenir" grant managed by Agence Nationale de la Recherche (CEBA, ref. ANR-10-LABX-25-01).
Author information
Authors and Affiliations
Contributions
EH, ID and JBD conceived and designed research. EH and NA collected the wood samples and conducted the extractions and chemical analysis. EC conducted the laboratory and semi-field larvicidal assays and the mosquito fitness study. EW conceived the formulation. DA, MC and DH designed and conducted the ecotoxicity assays. RLG and HS designed and conducted the cytotoxicity assays. EH, EC, ID and JBD analyzed the data and wrote the manuscript. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors have no relevant financial or non-financial interests to disclose.
Ethical statements
Wood material was accessed according to French regulations concerning genetic resources access and benefit-sharing (French Ministry of Ecological Transition and Solidarity permit No. TREL1820249A/80), and obtained the required certificate of compliance delivered by the international Access and Benefit-Sharing Clearing House (UID: ABSCH-IRCC-FR-246958-1).
Additional information
Communicated by Orlando Campolo.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Clervil, E., Duchemin, JB., Amusant, N. et al. Efficacy and selectivity of Sextonia rubra wood extracts and formulation in the control of Aedes aegypti strains. J Pest Sci (2024). https://doi.org/10.1007/s10340-024-01747-4
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10340-024-01747-4