Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-17T19:53:02.742Z Has data issue: false hasContentIssue false

The main component of the scent of Senecio madagascariensis flowers is an attractant for Aedes aegypti (L.) (Diptera: Culicidae) mosquitoes

Published online by Cambridge University Press:  06 July 2022

G. A. Kashiwagi*
Affiliation:
Centro de Investigaciones de Plagas e Insecticidas (CONICET-CITEDEF), Juan Bautista de La Salle 4397, B1603ALO Villa Martelli, Provincia de Buenos Aires, Argentina
S. von Oppen
Affiliation:
Centro de Investigaciones de Plagas e Insecticidas (CONICET-CITEDEF), Juan Bautista de La Salle 4397, B1603ALO Villa Martelli, Provincia de Buenos Aires, Argentina
L. Harburguer
Affiliation:
Centro de Investigaciones de Plagas e Insecticidas (CONICET-CITEDEF), Juan Bautista de La Salle 4397, B1603ALO Villa Martelli, Provincia de Buenos Aires, Argentina
P. González-Audino
Affiliation:
Centro de Investigaciones de Plagas e Insecticidas (CONICET-CITEDEF), Juan Bautista de La Salle 4397, B1603ALO Villa Martelli, Provincia de Buenos Aires, Argentina
*
Author for correspondence: G. A. Kashiwagi, Email: gustavokashiwagi@gmail.com

Abstract

Aedes aegypti (L.) (Diptera: Culicidae) is one of the main vectors of arboviruses, including dengue, Zika, and chikungunya. It almost exclusively inhabits urban areas. Both sexes feed on plant carbohydrates, although for males, this is their only food source. In the case of floral nectars, mosquitoes locate plant sugar sources assisted by volatile compounds. In this work, we found that the floral scent of Senecio madagascariensis elicited a behavioral response in males; therefore, we focused on identifying the volatiles emitted by these flowers. The terpenes (±)-α-pinene, β-pinene, sabinene, and phellandrene and 1-alkenes 1-undecene, and 1-nonene were identified. To determine which compounds are bioactive, pure synthetic lures were assessed using an olfactometer. Only the main compound 1-nonene was an attractant for males. Since our goal was the introduction of synthetic floral-based attractants in toxic sugar-baited traps, we formulated 1-nonene in solid paraffin and stearin matrices to obtain a controlled release system. The bioassay with a toxicological end point showed that the incorporation of a feeding attractant to the toxic sugar trap increased overall mortality. These results suggest that it is possible to use plant volatile compounds or flower cuttings as male Ae. aegypti attractants to improve the efficacy of baited traps.

Type
Research Paper
Copyright
Copyright © CONICET-UNIDEF, 2022. Published by Cambridge University Press.

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Both authors contributed equally.

References

Abbott, WS (1925) A method of computing the effectiveness of an insecticide. Journal of Economic Entomology 18, 265267.CrossRefGoogle Scholar
Abdel-Malek, AA (1964) Study of the feeding habits of male Anopheles sergenti. Theo. at Siwa Oasis using radiophosphorus. Bulletin of WHO 30, 137.Google ScholarPubMed
Abdel-Malek, AA and Baldwin, WF (1961) Specificity of plant feeding in mosquitoes as determined by radioactive phosphorus. Nature 192, 178179.CrossRefGoogle ScholarPubMed
Allan, SA (2011) Susceptibility of adult mosquitoes to insecticides in aqueous sucrose baits. Journal of Vector Ecology 36, 5967.CrossRefGoogle ScholarPubMed
Antonio-Arreola, GE, López-BelloI, R, Romero-Moreno, DK and Sánchez, D (2011) Laboratory and field evaluation of the effects of the neonicotinoid imidacloprid on the oviposition response of Aedes (Stegomyia) aegypti Linnaeus (Diptera: Culicidae). Memorias do Instituto Oswaldo Cruz 106, 9971001.CrossRefGoogle ScholarPubMed
Braks, MA, Honório, NA, Lourenço-De-Oliveira, R, Juliano, SA and Lounibos, LP (2003) Convergent habitat segregation of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in southeastern Brazil and Florida. Journal of Medical Entomology 40, 785794.CrossRefGoogle ScholarPubMed
Bruce, TJA and Pickett, JA (2011) Perception of plant volatile blends by herbivorous insects – finding the right mix. Phytochemistry 72, 16051611.CrossRefGoogle ScholarPubMed
Fikrig, K, Johnson, J, Fish, D and Ritchie, SA (2017) Assessment of synthetic oral-based attractants and sugar baits to capture male and female Aedes aegypti (Diptera: Culicidae). Parasites & Vectors 10, 32.CrossRefGoogle Scholar
Foster, WA (1995) Mosquito sugar feeding and reproductive energetics. Annual Review of Entomology 40, 443.CrossRefGoogle ScholarPubMed
Foster, WA and Hancock, RG (1994) Nectar-related olfactory and visual attractants for mosquitoes. Journal of the American Mosquito Control Association 10, 288296.Google ScholarPubMed
Galili, A (2017) Attractive Toxic Baited Traps. Conference in Bringing Innovation to the Frontline: Tools to Advance the Global Response to Vector-Borne Diseases. Madrid: Fundación Ramón Areces. Available at https://www.fundacionareces.tv/ciencias-de-la-vida-y-de-la-materia/new-tools-to-advance-the-global-response-to-vector-borne-dis/amir-galili-attractive-toxic-baited-traps/ (Accessed 30 December 2020).Google Scholar
Gardner, DR, Thorne, MS, Molyneux, RJ, Pfister, JA and Seawright, AA (2006) Pyrrolizidine alkaloids in Senecio madagascariensis from Australia and Hawaii and assessment of possible livestock poisoning. Biochemical Systematics and Ecology 34, 736744.CrossRefGoogle Scholar
Gary, RE and Foster, WA (2004) Anopheles gambiae feeding and survival on honeydew and extra-oral nectar of peridomestic plants. Medical and Veterinary Entomology 18, 102107.CrossRefGoogle Scholar
Geier, M and Broeckh, J (1999) A new Y-tube olfactometer for mosquitoes to measure the attractiveness of host odours. Entomologia Experimentalis et Applicata 92, 919.CrossRefGoogle Scholar
Haddouchi, F, Chaouche, TM, Zaouali, Y, Ksouri, R, Attou, A and Benmansour, A (2013) Chemical composition and antimicrobial activity of the essential oils from four Ruta species growing in Algeria. Food Chemistry 141, 253258.CrossRefGoogle ScholarPubMed
Jardine, KL, Abrell, L, Kurc, SA, Huxman, T, Ortega, J and Guenther, A (2010) Volatile organic compound emissions from Larrea tridentata (creosotebush). Atmospheric Chemistry and Physics 10, 1219112206.CrossRefGoogle Scholar
Jepson, PC and Healy, TP (1988) The location of oral nectar sources by mosquitoes: an advanced bioassay for volatile plant odours and initial studies with Aedes aegypti (L.) (Diptera: Culicidae). Bulletin of Entomological Research 78, 641650.CrossRefGoogle Scholar
Jhumur, US, Dötterl, S and Jürgens, A (2007) Electrophysiological and behavioural responses of mosquitoes to volatiles of Sileneotites (Caryophyllaceae). Arthropod–Plant Interactions 1, 245254.CrossRefGoogle Scholar
Joseph, SR (1970) Fruit feeding of mosquitoes in nature. Proceedings of the New Jersey Mosquito Extermination Association 57, 125131.Google Scholar
Kegge, W, Weldegergis, BT, Soler, R, Eijk, MV, Dicke, M, Voesenek, LA and Pierik, R (2013) Canopy light cues affect emission of constitutive and methyl jasmonate induced volatile organic compounds in Arabidopsis thaliana. New Phytologist 200, 861874.CrossRefGoogle ScholarPubMed
Lacroix, R, McKemey, AR, Raduan, N, Wee LK, Ming WH, Ney TG, Rahidah AA, Salman S, Subramaniam S, Nordin O, Hanum AT, Angamuthu C, Mansor SM, Lees RS, Nash N, Scaife S, Gray P, Labbé G, Beech C, Nimmo D, Alphey L, Vasan SS, Lim LH, Wasi AN and Murad S (2012) Open field release of genetically engineered sterile male Aedes aegypti in Malaysia. PLoS One 7, e42771.CrossRefGoogle ScholarPubMed
Lucia, A, Zerba, EN and Masuh, HM (2013) Knockdown and larvicidal activity of six monoterpenes against Aedes aegypti (Diptera: Culicidae) and their structure–activity relationships. Parasitology Research 112, 42674272.CrossRefGoogle ScholarPubMed
Lwande, W, McDowell, PG, Amiani, H and Amoke, P (1989) Analysis of airborne volatiles of cowpea. Phytochemistry 28, 421423.CrossRefGoogle Scholar
Magnarelli, LA (1977) Nectar feeding by Aedes sollicitans and its relation to gonotrophic activity. Environmental Entomology 6, 237242.CrossRefGoogle Scholar
Mathew, N, Ayyanar, E, Shanmugavelu, S and Muthuswamy, K (2013) Mosquito attractant blends to trap host seeking Aedes aegypti. Parasitology Research 112, 1305.CrossRefGoogle ScholarPubMed
Müller, G and Schlein, Y (2006) Sugar questing mosquitoes in arid areas gather on scarce blossoms that can be used for control. International Journal for Parasitology 36, 10771080.CrossRefGoogle ScholarPubMed
Müller, GC, Kravchenko, VD and Schlein, Y (2008) Decline of Anopheles sergentii and Aedes caspius populations following presentation of attractive toxic (spinosad) sugar bait stations in an oasis. Journal of the American Mosquito Control Association 24, 147149.CrossRefGoogle Scholar
Müller, GC, Junnila, A and Schlein, Y (2010) Effective control of adult Culex pipiens by spraying an attractive toxic sugar bait solution in the vegetation near larval habitats. Journal of Medical Entomology 47, 6366.CrossRefGoogle ScholarPubMed
Patterson, RS, Smittle, BJ and DeNeve, RT (1969) Feeding habits of male southern house mosquitoes on 32P-labeled and unlabeled plants. Journal of Economic Entomology 62, 14551458.CrossRefGoogle ScholarPubMed
Qualls, WA, Naranjo, DP, Subía, MA, Ramon, G, Cevallos, V, Grijalva, I, Gómez, E, Arheart, KL, Fuller, DO and Beier, JC (2016) Movement of Aedes aegypti following a sugar meal and its implication in the development of control strategies in Durán, Ecuador. Journal of Vector Ecology 41, 224231.CrossRefGoogle ScholarPubMed
Raguso, R (2004) Why are some floral nectars scented? Ecology 85, 14861494. Retrieved December 30, 2020, from http://www.jstor.org/stable/3450568.CrossRefGoogle Scholar
Revay, EE, Müller, GC, Qualls, WA, Kline, DL, Naranjo, DP, Arheart, KL, Kravchenko, VD, Yefremova, Z, Hausmann, A, Beier, JC, Schlein, Y and Xue, RD (2014) Control of Aedes albopictus with attractive toxic sugar baits (ATSB) and potential impact on non-target organisms in St. Augustine, Florida. Parasitology Research 113, 7379.CrossRefGoogle Scholar
Seccacini, E, Masuh, H, Licastro, SA and Zerba, EN (2006) Laboratory and scaled up evaluation of cis-permethrin applied as a new ultra-low volume formulation against Aedes aegypti (Diptera: Culicidae). Acta Tropica 97, 14.CrossRefGoogle ScholarPubMed
Smith, L, Kasai, S and Scott, JG (2016) Pyrethroid resistance in Aedes aegypti and Aedes albopictus: important mosquito vectors of human diseases. Pesticide Biochemistry and Physiology 133, 112.CrossRefGoogle ScholarPubMed
Stone, C and Foster, WA (2013) Plant-sugar feeding and vectorial capacity. In Ecology of Parasite–Vector Interactions. Chapter: 3. Ecology and control of vector-borne diseases, vol. 3. Wageningen: Wageningen Academic Publishers, pp. 35–79. Available at https://doi.org/10.3920/978-90-8686-744-8_3.Google Scholar
Tsuda, Y, Suwonkerd, W, Chawprom, S, Prajakwong, S and Takagi, M (2006) Different spatial distribution of Aedes aegypti and Aedes albopictus along an urban rural gradient and the relating environmental factors examined in three villages in northern Thailand. Journal of the American Mosquito Control Association 22, 222228.CrossRefGoogle ScholarPubMed
Valença, MA, Marteis, LS, Steffler, LM, Silva, AM and Santos, RLC (2013) Dynamics and characterization of Aedes aegypti (L.) (Diptera: Culicidae) key breeding sites. Neotropical Entomology 42, 311316.CrossRefGoogle ScholarPubMed
Vargo, AM and Foster, WA (1982) Responsiveness of female Aedes aegypti (Diptera: Culicidae) to flower extracts. Journal of Medical Entomology 19, 710718.CrossRefGoogle Scholar
von Oppen, S, Masuh, H, Licastro, SA, Zerba, EN and Gonzalez-Audino, P (2015) A floral-derived attractant for Aedes aegypti mosquitoes. Entomologia Experimentalis et Applicata 155, 184192.Google Scholar
Wensler, RJD (1972) The effect of odors on the behavior of adult Aedes aegypti and some factors limiting responsiveness. Canadian Journal of Zoology 50, 415420.CrossRefGoogle ScholarPubMed
World Health Organization (WHO) (2008) WHO Position Statement on Integrated Vector Management. Geneva, Switzerland: World Health Organization. Available at http://apps.who.int/iris/bitstream/handle/10665/69745/WHO_HTM_NTD_VEM_2008.2_eng.pdf?sequence=1&isAllowed=y (Accessed 8 November 2020).Google Scholar
Xue, RD, Müller, GC, Kline, DL and Barnard, DR (2003) Effect of application rate and persistence of boric acid sugar baits applied to plants for control of Aedes albopictus. Journal of the American Mosquito Control Association 27, 5660.CrossRefGoogle Scholar
Xue, R-D, Ali, A, Kline, DL and Barnard, DR (2008) Field evaluation of boric acid- and fipronil-based bait stations against adult mosquitoes. Journal of the American Mosquito Control Association 24, 415418.CrossRefGoogle ScholarPubMed
Xue, RD, Müller, GC, Qualls, WA, Smith, ML, Scott, JM, Lear, J and Cope, SE (2013) Attractive targeted sugar baits: field evaluations and potential for use in mosquito control. Wing Beats Spring 24, 1318.Google Scholar
Ye, YH, Chenoweth, SF, Carrasco, AM, Allen, SL, Frentiu, FD, van den Hurk, AF, Beebe, NW and McGraw, EA (2016) Evolutionary potential of the extrinsic incubation period of dengue virus in Aedes aegypti. Evolution (N. Y) 70, 24592469.Google ScholarPubMed
Yee, WL and Foster, WA (1992) Diel sugar-feeding and host-seeking rhythms in mosquitoes (Diptera: Culicidae) under laboratory conditions. Journal of Medical Entomology 29, 784791.CrossRefGoogle ScholarPubMed
Yuval, B (1992) The other habit: sugar feeding by mosquitoes. Bulletin of the Society for Vector Ecologist 17, 150156.Google Scholar