Abstract
Mosquitoes are responsible for serious public health problems worldwide, and as such, Aedes aegypti and Aedes albopictus are important vectors in the transmission of dengue, chikungunya, and Zika in Brazil and other countries of the world. Due to growing resistance to chemical insecticides among populations of vectors, environmentally friendly strategies for vector management are receiving ever more attention. Essential oils (EOs) extracted from plants have activities against insects with multiple mechanisms of action. These mechanisms hinder the development of resistance, and have the advantages of being less toxicity and biodegradable. Thus, the present study aimed to evaluate the chemical composition of the EOs obtained from Piper capitarianum Yunck, as well as evaluating their insecticidal potential against Aedes aegypti and A. albopictus, and their toxicity in relation to Artemia salina. The yields of the EOs extracted from the leaves, stems, and inflorescences of P. capitarianum were 1.2%, 0.9%, and 0.6%, respectively, and their main constituents were trans-caryophyllene (20.0%), α-humulene (10.2%), β-myrcene (10.5%), α-selinene (7.2%), and linalool (6.0%). The EO from the inflorescences was the most active against A. aegypti and A. albopictus, and exhibited the respective larvicidal (LC50 = 87.6 μg/mL and 76.1 μg/mL) and adulticide activities (LC50 = 126.2 μg/mL and 124.5 μg/mL). This EO was also the most active in the inhibition of AChE, since it presented an IC50 value of 14.2 μg/mL. Its larvicidal effect was observed under optical and scanning electron microscopy. Additionally, non-toxic effects against A. salina were observed. Docking modeling of trans-caryophyllene and α-humulene on sterol carrier protein-2 (SCP-2) suggests that both molecules have affinity with the active site of the enzyme, which indicates a possible mechanism of action. Therefore, the essential oil of P. capitarianum may be used in the development of new insecticide targets for the control of A. aegypti and A. albopictus in the Amazonian environment.
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References
Abbots WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267. https://doi.org/10.1093/jee/18.2.265a
Achee NL, Grieco JP, Vatandoost H, Seixas G, Pinto J, Ching-Ng L, David JP (2019) Alternative strategies for mosquito-borne arbovirus control. Plos Neglect Trop D 131:1935–2727. https://doi.org/10.1371/journal.pntd.0006822
Adams PR (2009) Identification of essential oil components by Gas gas chromatography/mass spectrometry. Allured Books, South Carol, USA
Almeida RR, Souto RN, Bastos CN, Silva MH, Maia JG (2009) Chemical variation in Piper aduncum and biological properties of its dillapiole-rich essential oil. ChemBioChem 6:1427–1434. https://doi.org/10.1002/cbdv.200800212
Alphey L, Benedict M, Bellini R, Clark GG, Dame DA, Service MW, Dobson SL (2010) Sterile-insect methods for control of mosquito-borne diseases: an analysis. Vector Borne Zoonotic Dis 10:295–311. https://doi.org/10.1089/vbz.2009.0014
Alves SN, Serrao JE, Melo AL (2010) Alterations in the fat body and midgut of Culex quinquefasciatus larvae following exposure to different insecticides. Micron 41:592–597. https://doi.org/10.1016/j.micron.2010.04.004
Andrade Ochoa S, Correa Basurto J, Rodríguez Valdez LM, Sánchez Torres LE, Nogueda Torres B, Nevárez Moorillón GV (2018) In vitro and in silico studies of terpenes, terpenoids and related compounds with larvicidal and pupaecidal activity against Culex quinquefasciatus Say (Diptera: Culicidae). Chem Cent J 53:12–53. https://doi.org/10.1186/s13065-018-0425-2
Araújo TVB, Ximenes RA, Barros MFD, Souza WV, Montarroyos UR, Melo APL, Vazquez E (2018) Association between microcephaly, Zika virus infection, and other risk factors in Brazil: final report of a case-control study. Lancet Infect Dis 18:328–336. https://doi.org/10.1016/S1473-3099(17)30727-2
Attela GC, Majerowicz D, Gondim KC (2012) Tópicos Avançados em Entomologia Molecular. Metabolismo em Lipídeos – Cap. 6. Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular - INCT-EM, São Paulo
Autran ES, Neves IA, Silva CSB, Santos GKN, Câmara CAG, Navarro DMAF (2009) Chemical composition, oviposition deterrent and larvicidal activities against Aedes aegypti of essential oils from Piper marginatum Jacq. (Piperaceae). Bioresour Technol 100:2284–2288. https://doi.org/10.1016/j.biortech.2008.10.055
Balasubramani S, Sabapathi G, Moola AK, Solomon RV, Venuvanalingam P, Diana RKB (2018) Evaluation of the leaf essential oil from Artemisia vulgaris and its larvicidal and repellent activity against dengue fever vector Aedes aegypt - an experimental and molecular docking investigation. A C S Omega 3:15657–15665. https://doi.org/10.1021/acsomega.8b01597
Benelli G, Beier JC (2017) Current vector control challenges in the fight against malaria. Acta Trop 174:91–96. https://doi.org/10.1016/j.actatropica.2017.06.028
Benelli G, Iacono AL, Canale A, Mehlhorn H (2016a) Mosquito vectors and the spread of cancer: an overlooked connection? Parasitol Res 115:2131–2137. https://doi.org/10.1007/s00436-016-5037-y
Benelli G, Jeffries CL, Walker T (2016b) Biological control of mosquito vectors: past, present, and future. Insects 7:1–18. https://doi.org/10.3390/insects7040052
Benelli G, Govindarajan M, Rajeswar M, Senthilmurugan S, Vijayan P, Alharbi NS, Khaled JM (2017a) Larvicidal activity of Blumea eriantha essential oil and its components against six mosquito species, including Zika virus vectors: the promising potential of (4E, 6Z)-allo-ocimene, carvotanacetone and dodecyl acetate. Parasitol Res 116:1175–1188. https://doi.org/10.1007/s00436-017-5395-0
Benelli G, Pavela R, Canale A, Cianfaglione K, Ciaschetti G, Conti F, Maggi F (2017b) Acute larvicidal toxicity of five essential oils (Pinus nigra, Hyssopus officinalis, Satureja montana, Aloysia citrodora and Pelargonium graveolens) against the filariasis vector Culex quinquefasciatus: Synergistic and antagonistic effects. Parasitol Int 66:166–171. https://doi.org/10.1016/j.parint.2017.01.012
Benelli G, Rajeswary M, Govindarajan M (2018) Towards green oviposition deterrents? Effectiveness of Syzygium lanceolatum (Myrtaceae) essential oil against six mosquito vectors and impact on four aquatic biological control agents. Environ Sci Pollut Res 25:10218–10227. https://doi.org/10.1007/s11356-016-8146-3
Benitez NP, León EMM, Stashenko EE (2009) Essential oil composition from two species of Piperaceae family grown in Colombia. J Chromatogr Sci 47:804–807. https://doi.org/10.1093/chromsci/47.9.804
Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak JR (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81:3684–3690. https://doi.org/10.1063/1.448118
Bezerra JWA, Costa AR, Silva MAP, Rocha MI, Boligon AA, Rocha JBT, Kamdem JP (2017) Chemical composition and toxicological evaluation of Hyptis suaveolens (L.) Poiteau (LAMIACEAE) in Drosophila melanogaster and Artemia salina. S Afr J Bot 113:437–442. https://doi.org/10.1016/j.sajb.2017.10.003
Borrero MA, Jonny E, Duque SC, Mendez S (2019) Insecticide design using in silico and in vivo analysis of different pharmacological targets in Aedes aegypti. Comp Biochem Phys A 229:108–664. https://doi.org/10.1016/j.cbpc.2019.108664
Botas G, Cruz R, Almeida F, Duarte J, Araújo R, Souto R, Fernandes C (2017) Baccharis reticularia DC. and limonene nanoemulsions: promising larvicidal agents for Aedes aegypti (Diptera: Culicidae) Control. Molecules 22:1990. https://doi.org/10.3390/molecules22111990
Brogdon W, Chan A (2010) Guideline for evaluating insecticide resistance in vectors using the CDC bottle bioassay, 2nd edn. Center for Global Health, Division of Parasitic Diseases and Malaria, Atlanta, p 30 https://www.fdacs.gov/content/download/71564/file/CDC_Bioassay.pdf. Accessed 21 September 2020
Bussi G, Donadio D, Parrinello M (2007) Canonical sampling through velocity rescaling. J Chem Phys 126:014–101. https://doi.org/10.1063/1.2408420
Cansian RL, Vanin AB, Orlando T, Piazza SP, Puton BMS, Cardoso RI, Oliveira D (2017) Toxicity of clove essential oil and its ester eugenyl acetate against Artemia salina. J Biol Sci 77:155–161. https://doi.org/10.1590/1519-6984.12215
Carvalho D, McKemey A, Garziera L, Lacroix R, Donnelly CA, Alphey L, Capurro ML (2015) Suppression of a field population of Aedes aegypti in Brazil by sustained release of transgenic male mosquitoes. Plos Neglect Trop D 9:3864. https://doi.org/10.1371/journal.pntd.0003864
Castillo RM, Stashenko E, Duque JE (2017) Insecticidal and repellent activity of several plant-derived essential oils against Aedes aegypti. J Am Mosquito Contr 33:25–35. https://doi.org/10.2987/16-6585.1
Chaithong U, Choochote W, Kamsuk K, Jitpakdi A, Tippawangkosol P, Chaiyasit D, Pitasawat B (2006) Larvicidal effect of pepper plants on Aedes aegypti (L.) (Diptera: Culicidae). J Vector Ecol 31:138–144. https://doi.org/10.3376/1081-1710(2006)31[138:leoppo]2.0.co;2
Chaiyasit D, Choochote W, Rattanachanpichai E, Chaithong U, Chaiwong P, Jitpakdi A, Pitasawat B (2006) Essential oils as potential adulticides against two populations of Aedes aegypti, the laboratory and natural field strains, in Chiang Mai Province, northern Thail. Parasitol Res 99:715. https://doi.org/10.1007/s00436-006-0232-x
Chellappandian M, Thanigaivel A, Vasantha-Srinivasan P, Edwin ES, Ponsankar A, Selin-Rani S, Benelli G (2018a) 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. Environ Sci Pollut Res 25:10294–10306. https://doi.org/10.1007/s11356-017-8952-2
Chellappandian M, Vasantha-Srinivasan P, Senthil-Nathan S, Karthi S, Thanigaivel A, Ponsankar A, Hunter WB (2018b) Botanical essential oils and uses as mosquitocides and repellents against dengue. Environ Int 113:214–230. https://doi.org/10.1016/j.envint.2017.12.038
Cruz RCD, Silva SLCE, Souza IA, Gualberto SA, Carvalho KS, Santos FR, Carvalho MG (2017) Toxicological evaluation of essential oil from the leaves of Croton argyrophyllus (Euphorbiaceae) on Aedes aegypti (Diptera: Culicidae) and Mus musculus (Rodentia: Muridae). J Med Entomol 54:985–993. https://doi.org/10.1093/jme/tjw239
Dias CN, Moraes DFC (2014) Essential oils and their compounds as Aedes aegypti L. (Diptera: Culicidae) larvicides. Parasitol Res 113:565–592. https://doi.org/10.1007/s00436-013-3687-6
Ding F, Fu J, Jiang D, Hao M, Lin G (2018) Mapping the spatial distribution of Aedes aegypti and Aedes albopictus. Acta Trop 178:155–162. https://doi.org/10.1016/j.actatropica.2017.11.020
Dunford CJ, Falconer A, Leite NL, Robert AW, Brogdon WA (2016) Determination of insecticidal effect (LC50 and LC90) of organic fatty acids mixture (C89101Silicone) against Aedes aegypti and Aedes albopictus (Diptera: Culicidae). J Med Entomol 53:699–702. https://doi.org/10.1093/jme/tjv239
Dyer DH, Lovell S, Thoden JB, Holden HM, Rayment I, Lan Q (2003) The structural determination of an insect sterol carrier protein-2 with a ligand-bound C16 fatty acid at 1.35-Å resolution. J Biol Chem 278:39085–39091. https://doi.org/10.1074/jbc.M306214200
Ellman KD, Courtney V, Andres JR, Featrrstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. https://doi.org/10.1016/0006-2952(61)90145-9
Essmann U, Perera L, Berkowitz ML (1995) A smooth particle mesh Ewald method. J Chem Phys 103:8577–8593. https://doi.org/10.1063/1.470117
Ferreira SAF, Simões RC, Ferreira RL, Alencar J, Scarpassa VM, Tadei WP (2019) Scanning electron microscopy and geometric contour morphometry for identifying eggs of three amazonian species of Mansonia (Diptera: Culicidae). J Med Entomol 10:1–10. https://doi.org/10.1093/jme/tjz240
Finney DJ (1971) Probit analysis. Cambridge University, London, pp 68–78. https://doi.org/10.1002/jps.2600600940
Flora do Brasil (2020) Jardim Botânico do Rio de Janeiro. Available on-line: http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB86578. Accessed 22 September 2020
Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Petersson GA, Nakatsuji H (2019) Gaussian 09:512. https://doi.org/10.12691/wjoc-5-1-2
Fujiwara GM, Annies V, Oliveira CF, Lara RA, Gabriel MM, Betim FCM, Zanin SMW (2017) Evaluation of larvicidal activity and ecotoxicity of linalool, methyl cinnamate and methyl cinnamate/linalool in combination against Aedes aegypti. Ecotox Environ Safe 139:238–244. https://doi.org/10.1016/j.ecoenv.2017.01.046
Gould E, Pettersson J, Higgs S, Charrel R, Lamballerie X (2017) Emerging arboviruses: why today? One Health 4:1–13. https://doi.org/10.1016/j.onehlt.2017.06.001
GROMACS (2019) Groningen University. Available online: http://www.gromacs.org. Accessed 26 March 2020
Guimarães EF, Carvalho-Silva M, Monteiro D, Medeiros ES, Queiroz GA (2015). Piperaceae in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. Available on-line: http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB86578. Accessed 30 March 2020
Gupta RC (2006) Classification and uses of Organophosphates and Carbamates. Toxicol Organophosphate Carbamate Compd:5–24. https://doi.org/10.1016/b978-012088523-7/50003-x
Hematpoor A, Liew SY, Azirun MS, Awang K (2017) Insecticidal activity and the mechanism of action of three phenylpropanoids isolated from the roots of Piper sarmentosum. Sci Rep 7:1–13. https://doi.org/10.1038/s41598-017-12898-z
Hess B, Bekker H, Berendsen HJ, Fraaije JG (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18:1463–1472. https://doi.org/10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H
Huang J, MacKerell AD (2013) CHARMM36 all-atom additive protein force field: validation based on comparison to NMR data. J Comput Chem 34:2135–2145. https://doi.org/10.1002/jcc.23354
Huang YJ, Higgs S, Vanlandingham D (2017) Biological control strategies for mosquito vectors of arboviruses. Insect 8:21. https://doi.org/10.3390/insects8010021
Jankowska M, Rogalska J, Wyszkowska J, Stankiewicz M (2018) Molecular targets for components of essential oils in the insect nervous system—a review. Molecules 23:34. https://doi.org/10.3390/molecules23010034
Kirchmair J, Markt P, Distinto S, Wolber G, Langer T (2008) Evaluation of the performance of 3D virtual screening protocols: RMSD comparisons, enrichment assessments, and decoy selection—what can we learn from earlier mistakes? J Comput Aided Mol Des 22:213–228. https://doi.org/10.1007/s10822-007-9163-6
Klimovich PV, Shirts MR, Mobley DL (2015) Guidelines for the analysis of free energy calculations. J Comput Aided Mol Des 29:397–411. https://doi.org/10.1007/s10822-015-9840-9
Kraemer MU, Sinka ME, Duda KA, Mylne AQ, Shearer FM, Barker CM, Hendrickx G (2015) The global distribution of the arbovirus vectors Aedes aegypti and Aedes albopictus. eLife 4:08–347. https://doi.org/10.7554/eLife.08347
Kumar R, Shanmugapriya B, Thiyagesan K, Kumar S, Xavier S (2010) A search for mosquito larvicidal compounds by blocking the sterol carrying protein, AeSCP-2, through computational screening and docking strategies. Pharm Res 2:247. https://doi.org/10.4103/0974-8490.69126
Larson RT, Wessely V, Jiang Z (2008) Larvicidal activity of sterol carrier Protein-2 in four species of mosquitoes. J Med Entomol 45:439–444. https://doi.org/10.1603/0022-2585(2008)45[439:laoscp]2.0.co;2
Lavor PL, Santiago GMP, Gois RWS, Sousa LM, Bezerra GP, Romero NR, Arriaga AMC, Lemos TLG, Alves PB, Gomes PCS (2012) Larvicidal activity against Aedes aegypti of essential oils from northeast Brazil. Nat Prod Commun 7:10. https://doi.org/10.1007/s00436-013-3687-6
Leal SM, Pino N, Stashenko EE, Martínez JR, Escobar P (2013) Antiprotozoal activity of essential oils derived from Piper spp. grown in Colombia. J Essent Oil Res 25:512–519. https://doi.org/10.1080/10412905.2013.820669
Lee SJ, Kim JH, Lee SC (2018) Effects of oil-film layer and surfactant on the siphonal respiration and survivorship in the fourth instar larvae of Aedes togoi mosquito in laboratory conditions. Sci Rep 8:56–94. https://doi.org/10.1038/s41598-018-23980-5
Leta S, Beyene TJ, De Clercq EM, Amenu K, Kraemer MU, Revie CW (2018) Global risk mapping for major diseases transmitted by Aedes aegypti and Aedes albopictus. Int J Infect Dis 67:25–35. https://doi.org/10.1016/j.ijid.2017.11.026
Lipinski CA, Lombardo F, Dominy BW, Feeney PJ (1997) Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 23:3–25. https://doi.org/10.1016/S0169-409X(96)00423-1
MacKerell AD, Vanommeslaeghe K (2020). University of Maryland. https://cgenff.umaryland.edu/. Accessed 30 March 2020
Meyer BN, Ferrigini N, Putnam JE, Jacobsen LB, Nichols DE, McLaughlin JL (1982) Brine shrimp: a convenient general bioassay for active plant constituents. Planta Med 45:31–34. https://doi.org/10.1055/s-2007-971236
Monzote L, Scull R, Cos P, Setzer WN (2017) Essential oil from Piper aduncum: chemical analysis, antimicrobial assessment and literature review. Med 4:49. https://doi.org/10.3390/medicines4030049
Morais SM, Facundo VA, Bertini LM, Cavalcanti ESB, Anjos JF, Ferreira SA, Souza Neto MA (2007) Chemical composition and larvicidal activity of essential oils from Piper species. Biochem Syst Ecol 35:670–675. https://doi.org/10.1016/j.bse.2007.05.002
Nagori K, Singh MK, Alexander A, Kumar T, Dewangan D, Badwaik H, Tripathi DK (2011) Piper betle L.: a review on its ethnobotany, phytochemistry, pharmacological profile and profiling by new hyphenated technique DART-MS (Direct Analysis in Real Time Mass Spectrometry). J Pharm Res 4:2991–2997. https://doi.org/10.1177/1934578X1601100948
Nascimento JCD, Paula VFD, David JM, David JP (2012) Occurrence, biological activities and 13C NMR data of amides from Piper (Piperaceae). Quim Nova 35:2288–2311. https://doi.org/10.1590/S0100-40422012001100037
Nascimento JCD, David JM, Barbosa LC, Paula VF, Demuner AJ, David JP, Guimarães EF (2013) Larvicidal activities and chemical composition of essential oils from Piper klotzschianum (Kunth) C. DC.(Piperaceae). Pest Manag Sci 69:1267–1271. https://doi.org/10.1002/ps.3495
Navickiene HM, Morandim AD, Alécio AC, Regasini LO, Bergamo DC, Telascrea M, Cavalheiro AJ, Lopes MN, Bolzani VD, Furlan M (2006) Composition and antifungal activity of essential oils from Piper aduncum, Piper arboreum and Piper tuberculatum. Quim Nova 29:467–470. https://doi.org/10.1590/S0100-40422006000300012
Nawaz R, Rathor HR, Bilal H, Hassan SA, Khan IA (2011) Adulticidal activity of Olea vera, Linum usitatissimum and Piper nigera against Anopheles stephensi and Aedes aegypti under laboratory conditions. Iran J Arthropod Borne Dis 5:2–9 Available online:https://jad.tums.ac.ir/index.php/jad/article/view/86.Accessed 22 September 2020
NIST (2016) Standard reference data. Available online: http://webbook.nist.gov/ chemistry. Accessed 12 April 2020
Nunes FC, Leite JA, Oliveira LHG, Sousa PAPS, Menezes MC, Moraes JPS, Braga VA (2015) The larvicidal activity of Agave sisalana against L4 larvae of Aedes aegypti is mediated by internal necrosis and inhibition of nitric oxide production. Parasitol Res 114:543–549. https://doi.org/10.1007/s00436-014-4216-y
Oliveira PV, Ferreira JC, Moura FS, Lima GS, Oliveira FM, Oliveira PES, Lemos RPL (2010) Larvicidal activity of 94 extracts from ten plant species of northeastern of Brazil against Aedes aegypti L.(Diptera: Culicidae). Parasitol Res 107:403–407. https://doi.org/10.1007/s00436-010-1880-4
Oliveira AEMFM, Duarte JL, Cruz RAS, Souto RNP, Ferreira MAF, Peniche T, Conceição EC, Oliveira LAR, Faustino SMM, Florentino AC, Carvalho JCT, Fernandes CP (2017) Pterodon emarginatus oleoresin-based nanoemulsion as a promising tool for Culex quinquefasciatus (Diptera: Culicidae) control. J Nanobiotechnol 15:9–11. https://doi.org/10.1186/s12951-016-0234-5
Pacheco FV, Paula AR, Alvarenga IC, Bertolucci SK, Alvarenga AA, Pinto JE (2016) Essential oil of monkey-pepper (Piper aduncum L.) cultivated under different light environments. Ind Crop Prod 85:251–257. https://doi.org/10.1016/j.indcrop.2016.03.016
Pavela R (2015) Essential oils for the development of eco-friendly mosquito larvicides: a review. Ind Crop Prod 76:174–187. https://doi.org/10.1016/j.indcrop.2015.06.050
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
Peng R, Fu Q, Hong H, Schwaegler T, Lan Q (2012) THAP and ATF-2 regulated sterol carrier Protein-2 promoter activities in the larval midgut of the yellow fever mosquito, Aedes aegypti. PLoS One 7:e46948. https://doi.org/10.1371/journal.pone.0046948
Perera H, Wijerathna T (2019) Sterol carrier protein inhibition-based control of mosquito vectors: current knowledge and future perspectives. Can J Infect Dis Med Microbiol:10:1–10:6. https://doi.org/10.1155/2019/7240356
Pino JA, Marbot R, Bello A, Urquiola A (2004) Composition of the essential oil of Piper hispidum Sw. from Cuba. J Essent Oil Res 16:459–460. https://doi.org/10.1080/10412905.2004.9698771
Pinto ACS, Nogueira KL, Chaves FCM, Silva LVS, Tadei WP, Pohlit AM (2012) Adulticidal activity of dillapiol and semi-synthetic derivatives of dillapiol against adults of Aedes aegypti (L.) (Culicidae). Int J Mosq Res 2:1–7. https://doi.org/10.5376/jmr.2012.01.0001
Pohlit AM, Quinard ELJ, Nunomura SM, Tadei WP, Hidalgo AF, Pinto ACS, Alecrim AM (2004) Screening of plants found in the State of Amazonas, Brazil for activity against Aedes aegypti larvae. Acta Amaz 34:97–105. https://doi.org/10.1590/S0044-59672004000100012
Procópio TF, Fernandes KM, Pontual EV, Ximenes RM, Oliveira ARC, Souza CS, Melo AMMA, Navarro DMAF, Paiva PMG, Martins GF, Napoleão TH (2015) Schinus terebinthifolius leaf extract causes midgut damage, interfering with survival and development of Aedes aegypti larvae. PLoS One 10:0126612. https://doi.org/10.1371/journal.pone.0126612
Radek JT, Dyer DH, Lah Q (2010) Effects of mutations in Aedes aegypti sterol carrier Protein-2 on the biological function of the protein. BioChem 49:7532–7541. https://doi.org/10.1021/bi902026v
Rattan RS (2010) Mechanism of action of insecticidal secondary metabolites of plant origin. J Crop Prot 29:913–920. https://doi.org/10.1016/j.cropro.2010.05.008
Riesna M, Hamid PH (2019) Larvicidal, adulticidal, and oviposition-deterrent activity of Piper betle L. essential oil to Aedes aegypti. Vet World 12:367–371. https://doi.org/10.14202/vetworld.2019.367-371
Rizvi SAH, Ling S, Tian F, Xie F, Zeng X (2018) Toxicity and enzyme inhibition activities of the essential oil and dominant constituents derived from Artemisia absinthium L. against adult Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Psyllidae). Ind Crops Prod 121: 468–475. https://doi.org/10.1016/j.indcrop.2018.05.031
Robertson JL, Savin NE, Preisler HK (2007) Bioassays with arthropods, 2nd edn. CRC Press, Boca Raton, p 224
Roiz D, Wilson AL, Scott TW, Fonseca DM, Jourdain F, Müller P, Corbel V (2018) Integrated Aedes management for the control of Aedes-borne diseases. PLoS Neglect Trop D 12:45–68. https://doi.org/10.1371/journal.pntd.0006845
Salinas JL, Walteros DM Styczynski A, Garzón F, Quijada H, Bravo E, Chaparro P, Madero J, Reyes JA, Ledermann J, Arteta Z, Borland E, Burns P, Gonzalez M, Powers AM, Mercado M, solan A, Sejvar JJ, Ospina ML (2017) Zika virus disease-associated Guillain-Barré syndrome—Barranquilla, Colombia 2015–2016. J Neurol Sci 381:272–277. https://doi.org/10.1016/j.jns.2017.09.001
Santana H, Trindade F, Stabeli R, Silva A, Militão J, Facundo V (2015) Essential oils of leaves of Piper species display larvicidal activity against the dengue vector, Aedes aegypti (Diptera: Culicidae). Rev Bras Planta Med 17:105–111. https://doi.org/10.1590/1983-084X/13_052
Setzer WN, Park G, Agius BR, Stokes SL, Walker TM, Haber WA (2008) Chemical compositions and biological activities of leaf essential oils of twelve species of Piper from Monteverde, Costa Rica. Nat Prod Commun 3:1367–1374. https://doi.org/10.1177/1934578X0800300823
Shirts MR, Chodera JD (2008) Statistically optimal analysis of samples from multiple equilibrium states. Int J Chem Phys 129:24–105. https://doi.org/10.1063/1.2978177
Silva JK, Silva NN, Santana JF, Andrade EH, Maia JG, Setzer WN (2016) Phenylpropanoid-rich essential oils of Piper species from the Amazon and their antifungal and anti-cholinesterase activities. Nat Prod Commun 11:1907–1911. https://doi.org/10.1177/1934578X1601101233
Silva J, Trindade R, Alves N, Figueiredo P, Maia J, Setzer W (2017) Essential oils from Neotropical Piper species and their biological activities. Int J Mol Sci 18:25–71. https://doi.org/10.3390/ijms18122571
Silva LS, Mar JM, Azevedo SG, Rabelo MS, Bezerra JA, Campelo PH, Machado MB, Trovati G, Santos AL, Fonseca Filho HD, Souza T, Sanches EA (2018) Encapsulation of Piper aduncum and Piper hispidinervum essential oils in gelatin nanoparticles: a possible sustainable control tool of Aedes aegypti, Tetranychus urticae and Cerataphis lataniae. J Sci Food Agric 12:1–11. https://doi.org/10.1002/jsfa.9233
Simeone MLF, Mikich SB, Côcco LC, Hansel FA, Bianconi GV (2011) Chemical composition of essential oils from ripe and unripe fruits of Piper amalago L. var. medium (Jacq.)Yunck and Piper hispidum Sw. J Essent Oil Res 23:54–58. https://doi.org/10.1080/10412905.2011.9700483
Soonwera M, Phasomkusolsil S (2017) Adulticidal, larvicidal, pupicidal and oviposition deterrent activities of essential oil from Zanthoxylum limonella Alston (Rutaceae) against Aedes aegypti (L.) and Culex quinquefasciatus (Say). Asian Pac J Trop Biomed 7:967–978. https://doi.org/10.1016/j.apjtb.2017.09.019
Sutiningsih D, Mustofa M, Satoto TBT, Martono E (2018) Morphological and histological effects of bruceine a on the larvae of Aedes aegypti Linnaeus (Diptera: Culicidae). Asian J Pharm Clin Res 11:422–427. https://doi.org/10.22159/ajpcr.2018.v11i10.27315
Takeara R, Gonçalves R, Ayres VFS, Guimarães AC (2017) Biological properties of essential oils from the Piper species of Brazil: a review. Arom Med Pl B Nat 2:81–93. https://doi.org/10.5772/66508
Thanigaivel A, Senthil NS, Vasantha SP, Murugan K (2017) Chemicals isolated from Justicia adhatoda Linn reduce fitness of the mosquito, Aedes aegypti L. Arch Insect Biochem 1:1–14. https://doi.org/10.1002/arch.21384
Thomas MB (2018) Biological control of human disease vectors: a perspective on challenges and opportunities. BioControl 63:61–69. https://doi.org/10.1007/s10526-017-9815-y
World Health Organization - WHO (2005) Guidelines for laboratory and field testing of mosquito larvicides world health organization communicable disease control, prevention and eradication who pesticide. 5a. edition, Geneva 1:25 WHO/CDS/WHOPES/GCDPP/2005.13. https://apps.who.int/iris/handle/10665/69101. Accessed 10 February 2019
World Health Organization - WHO (2006) Guidelines for testing mosquito adulticides for indoor residual spraying and treatment of mosquito nets. 6a. edition, Geneva 1:114 WHO/CDS/NTD/WHOPES/GCDPP/2006. https://apps.who.int/iris/handle/10665/69296. Accessed 10 February 2019
World Health Organization - WHO (2019a) Chikungunya. Disease outbreak News. https://www.who.int/chikungunya/epidemiology. Accessed 10 Fev 2019
World Health Organization - WHO (2019b) Countries and territories with current or previous Zika virus transmission. Disease outbreak News https://www.who.int/emergencies/diseases/zika. Accessed 10 Fev 2019
World Health Organization - WHO (2019c) Dengue control: epidemiology. Disease outbreak News. https://www.who.int/denguecontrol/epidemiology. Accessed 10 Fev 2019
World Health Organization - WHO (2019d) Yellow fever—Brazil. Disease outbreak News. https://www.who.int/yellowfever/epidemiology. Accessed 15 February 2019
Xiang CP, Han JX, Li XC, Li YH, Zhang Y, Chen L, Xu M (2017) Chemical composition and acetylcholinesterase inhibitory activity of essential oils from Piper Species. J Sci Food Agric 65:3702–3710. https://doi.org/10.1021/acs.jafc.7b01350
Yu KX, Wong CL, Ahmad R, Jantan I (2015) Mosquitocidal and oviposition repellent activities of the extracts of seaweed Bryopsis pennata on Aedes aegypti and Aedes albopictus. Molecules 20:14082–14102. https://doi.org/10.3390/molecules200814082
Zahid K, Shakoor S, Sajid HA, Afzal S, Ali L, Amin I, Idrees M (2020) Advancements in developing an effective and preventive dengue vaccine. Futur Virol 15:127–138. https://doi.org/10.2217/fvl-2019-0080
Zdobnov EM, von Mering C, Letunic I, Torrents D, Suyama M, Copley RR, Christophides GK, Thomasova D, Holt RA, Subramanian GM, Mueller HM, Dimopoulos G, Law JH, Wells MA, Birney E, Charlab R, Halpern AL, Kokoza E, Kraft CL, Lai Z, Lewis S, Louis C, Barillas-Mury C, Nusskern D, Rubin GM, Salzberg SL, Sutton GG, Topalis P, Wides R, Wincker P, Yandell M, Collins FH, Ribeiro J, Gelbart WM, Kafatos FC, Bork P (2002) Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster. Science 298:149–159. https://doi.org/10.1126/science.1077061
Zou X, Sun Y, Kuntz ID (1999) Inclusion of solvation in ligand binding free energy calculations using generalized-Born model. J Am Chem Soc 121:8033–8043. https://doi.org/10.1021/ja984102p
Acknowledgments
L.P.F. thanks fellowship from CAPES.
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This research was financially supported by Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM) (Edital N. 006/2019—Universal Amazonas Program and Edital No. 005/2019—PAPAC Program); PROEP 407856/2017-0-CNPq; Universidade Federal do Amazonas (UFAM) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).
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Conceptualization and fund acquisition: JRAS and ACFA. Investigation: LPF, KMTO, ESA, ADSB, JNS, NGS, and GAB. Data curation: ASR, FCMC, WPT, JLPF, JRAS, and ACFA. Literature search, data analysis, and writing (original draft preparation): LPF, ACBM, ASR, JLPF, JRAS, and ACFA. Writing (review & editing): ACFA, ASR, JLPF, and JRAS. Project administration and supervision: JRAS and ACFA.
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França, L.P., Amaral, A.C.F., Ramos, A.d.S. et al. Piper capitarianum essential oil: a promising insecticidal agent for the management of Aedes aegypti and Aedes albopictus. Environ Sci Pollut Res 28, 9760–9776 (2021). https://doi.org/10.1007/s11356-020-11148-6
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DOI: https://doi.org/10.1007/s11356-020-11148-6