The olfactory response of insect vectors such as phlebotomine sand flies is a key facet for investigating their interactions with vertebrate hosts and associated vector-borne pathogens. Such studies are mainly performed by assessing the electrophysiological response and the olfactory behaviour of these arthropods towards volatile organic compounds (VOCs) produced by hosts. Nonetheless, few studies are available for species of the subgenera Lutzomyia and Nyssomyia in South America, leaving a void for Old World sand fly species of the genus Phlebotomus. In this study, we evaluated the olfactory responses of Phlebotomus perniciosus, one of the most important vectors of Leishmania infantum in the Old World. To test the P. perniciosus behavioural response to VOCs, 28 compounds isolated from humans and dogs were assessed using electrophysiological (i.e., electroantennogram, EAG) and behavioural assays (i.e., Y-tube olfactometer). In the EAG trials, 14 compounds (i.e., acetic acid, nonanoic acid, 2-propanol, 2-butanol, pentanal, hexanal, nonanal, trans-2-nonenal, decanal, myrcene, p-cymene, verbenone, 2-ethyl-1-hexanol, and acetonitrile) elicited high antennal responses (i.e., ≥ 0.30 mV) in female sand flies, being those VOCs selected for the behavioural assays. From the 14 compounds tested in the Y-tube olfactometer, nonanal was significantly attractive for P. perniciosus females, whereas myrcene and p-cymene were significantly repellents (p < 0.05). The attraction indexes varied from 0.53 for nonanal (i.e., most attractive) to -0.47 to p-cymene (i.e., most repellent). Overall, our results shed light on the role of olfactory cues routing host seeking behaviour in P. perniciosus, with implications to develop sustainable sand fly monitoring as well as control in leishmaniasis endemic areas.

Department of Agricultural Sciences Food Natural Resources and Engineering University of Foggia Foggia Italy

Department of Agriculture Food and Environment University of Pisa Pisa Italy

Department of Parasitology Faculty of Science Charles University Staré Město Czech Republic

Department of Veterinary Clinical Sciences City University of Hong Kong Hong Kong China

Department of Veterinary Medicine University of Bari Bari Italy

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Dantas-Torres F, Solano-Gallego L, Baneth G, Ribeiro VM, de Paiva-Cavalcanti M, Otranto D. Canine leishmaniosis in the Old and New Worlds: unveiled similarities and differences. Trends Parasitol. 2012;28: 531–538. doi: 10.1016/j.pt.2012.08.007 PubMed DOI

Alvar J, Vélez ID, Bern C, Herrero M, Desjeux P, Cano J, et al. Leishmaniasis worldwide and global estimates of its incidence. PLoS One. 2012;7: e35671. doi: 10.1371/journal.pone.0035671 PubMed DOI PMC

Dantas-Torres F. The role of dogs as reservoirs of PubMed DOI

Otranto D, Dantas-Torres F, Mihalca AD, Traub RJ, Lappin M, Baneth G. Zoonotic Parasites of Sheltered and Stray Dogs in the Era of the Global Economic and Political Crisis. Trends Parasitol. 2017;33: 813–825. doi: 10.1016/j.pt.2017.05.013 PubMed DOI

Svobodová M, Sádlová J, Chang KP, Volf P. Short report: distribution and feeding preference of the sand flies PubMed

Hlavackova K, Dvorak V, Chaskopoulou A, Volf P, Halada P. A novel MALDI-TOF MS-based method for blood meal identification in insect vectors: A proof of concept study on phlebotomine sand flies. PLoS Negl Trop Dis. 2019;13: e0007669. doi: 10.1371/journal.pntd.0007669 PubMed DOI PMC

Messahel NE, Benallal KE, Halada P, Lafri I, Manseur H, Hakem A, et al. Identification of blood source preferences and PubMed DOI

Remadi L, Farjallah D, Chargui N, Belgacem S, Baba H, Zrieq R, et al. Blood meal analysis and molecular detection of mammalian PubMed DOI

Sadlova J, Vojtkova B, Becvar T, Lestinova T, Spitzova T, Bates P, et al. Host competence of the African rodents PubMed DOI PMC

Mendoza-Roldan JA, Zatelli A, Latrofa MS, Iatta R, Bezerra-Santos MA, Annoscia G, et al. PubMed DOI PMC

Bezerra-Santos MA, Benelli G, Germinara GS, Volf P, Otranto D. Smelly interactions: host-borne volatile organic compounds triggering behavioural responses in mosquitoes, sand flies, and ticks. Parasit Vectors. 2024;17: 227. doi: 10.1186/s13071-024-06299-1 PubMed DOI PMC

Vargas-Abasolo R, Gutiérrez-Cabrera AE, Cruz-López L, Alavez-Rosas D, Benelli G, Córdoba-Aguilar A. Chagas disease vector control strategies: where we are and where we should go from here. Entomol Generalis. 2023;43: 771–788. doi: 10.1127/entomologia/2023/1882 DOI

Alavez-Rosas D, Vargas-Abasolo R, Albores-Flores CI, Meneses-Arias MG, Gutiérrez-Cabrera AE, Benelli G, et al. Chemical ecology of triatomines: current knowledge and implications for Chagas disease vector management. J Pest Sci. 2024;97: 507–520. doi: 10.1007/s10340-023-01678-6 DOI

Rebollar-Tellez EA, Hamilton JGC, Ward RD. Response of female DOI

Andrade AJ, Andrade MR, Dias ES, Pinto MC, Eiras ÁE. Are light traps baited with kairomones effective in the capture of PubMed DOI

Pinto MC, Bray DP, Eiras AE, Carvalheira HP, Puertas CP. Attraction of the cutaneous leishmaniasis vector PubMed DOI PMC

Machado VE, Corrêa AG, Goulart TM, Silva FB, Ortiz DG, Pinto MC. Attraction of the sand fly PubMed DOI PMC

Tavares DDS, Salgado VR, Miranda JC, Mesquita PRR, Rodrigues FM, Barral-Netto M, et al. Attraction of phlebotomine sandflies to volatiles from skin odors of individuals residing in an endemic area of tegumentary leishmaniasis. PLoS One. 2018;13: e0203989. doi: 10.1371/journal.pone.0203989 PubMed DOI PMC

Magalhães-Junior JT, Barrouin-Melo SM, Corrêa AG, da Rocha Silva FB, Machado VE, Govone JS, et al. A laboratory evaluation of alcohols as attractants for the sandfly PubMed DOI PMC

Magalhães-Junior JT, Oliva-Filho AA, Novais HO, Mesquita PRR, M Rodrigues F, Pinto MC, et al. Attraction of the sandfly PubMed DOI

Staniek ME, Hamilton JGC. Odour of domestic dogs infected with PubMed DOI PMC

Chelbi I, Maghraoui K, Zhioua S, Cherni S, Labidi I, Satoskar A, et al. Enhanced attraction of sand fly vectors of PubMed DOI PMC

Schneider D. Electrophysiological investigations on the olfactory specificity of sexual attracting substances in different species of moth. J Insect Physiol. 1962;8: 15–30. doi: 10.1016/0022-1910(62)90051-3 DOI

Van Der Pers JNC. Comparison of electroantennogram response spectra to plant volatiles in seven species of DOI

Barbosa-Cornelio R, Cantor F, Coy-Barrera E, Rodríguez D. Tools in the investigation of volatile semiochemicals on insects: from sampling to statistical analysis. Insects. 2019;10: 241. doi: 10.3390/insects10080241 PubMed DOI PMC

Lawyer P, Killick-Kendrick M, Rowland T, Rowton E, Volf P. Laboratory colonization and mass rearing of phlebotomine sand flies (Diptera, Psychodidae). Parasite. 2017;24: 42. doi: 10.1051/parasite/2017041 PubMed DOI PMC

Dormont L, Bessière JM, Cohuet A. Human skin volatiles: a review. J Chem Ecol. 2013;39: 569–578. doi: 10.1007/s10886-013-0286-z PubMed DOI

Magalhães-Junior JT, Mesquita PR, Oliveira WF, Oliveira FS, Franke CR, Rodrigues FM, et al. Identification of biomarkers in the hair of dogs: new diagnostic possibilities in the study and control of visceral leishmaniasis. Anal Bioanal Chem. 2014;406: 6691–6700. doi: 10.1007/s00216-014-8103-2 PubMed DOI

Holderman CJ, Kaufman PE, Booth MM, Bernier UR. Novel collection method for volatile organic compounds (VOCs) from dogs. J Chromatogr B Analyt Technol Biomed Life Sci. 2017;1061–1062: 1–4. doi: 10.1016/j.jchromb.2017.06.044 PubMed DOI

Germinara GS, Ganassi S, Pistillo MO, Di Domenico C, De Cristofaro A, Di Palma AM. Antennal olfactory responses of adult meadow spittlebug, PubMed DOI PMC

Pistillo OM, D’Isita I, Germinara GS. Olfactory response of the spotted asparagus beetle, PubMed DOI

Kaissling KE, Thorson J. Insect olfactory sensilla: structural, chemical and electrical aspects of the functional organisation. In Sattelle DB, Hall LM, Hildebrand JG, editors. Receptors for neurotransmitters, hormones and pheromones in insects. Amsterdam: Elsevier/North-Holland Biomedical Press; pp. 261–282.

Nevatte TM, Ward RD, Sedda L, Hamilton JGC. After infection with PubMed DOI PMC

Canale A, Benelli G, Germinara GS, Fusini G, Romano D, Rapalini F, et al. Behavioural and electrophysiological responses to overlooked female pheromone components in the olive fruit fly, DOI

Light MD, Kamm JA, Buttery RG. Electroantennogram response of alfalfa seed chalcid, PubMed DOI

Raguso RA, Light DM. Electroantennogram responses of male DOI

Den Otter CJ, Tchicaya T, Schutte AM. Effects of age, sex and hunger on the antennal olfactory sensitivity of tsetse flies. Physiol Entomol. 1991;16: 173–182. doi: 10.1111/j.1365-3032.1991.tb00554.x DOI

Germinara GS, Pistillo M, Griffo R, Garonna AP, Di Palma A. Electroantennographic responses of PubMed DOI PMC

Germinara GS, De Cristofaro A, Rotundo G. Antennal olfactory responses to individual cereal volatiles in DOI

Jones R, Fountain MT, Günther CS, Eady PE, Goddard MR. Separate and combined PubMed DOI PMC

Fox J, Weisberg S. An R Companion to Applied Regression (Third). Sage. 2019. https://socialsciences.mcmaster.ca/jfox/Books/Companion/.

Lenth RV. Emmeans: Estimated Marginal Means, aka Least-Squares Means. 2022. https://CRAN.R-project.org/package=emmeans.

Syed Z, Leal WS. Acute olfactory response of PubMed DOI PMC

Robinson A, Busula AO, Voets MA, Beshir KB, Caulfield JC, Powers SJ, et al. PubMed DOI PMC

De Moraes CM, Wanjiku C, Stanczyk NM, Pulido H, Sims JW, Betz HS, et al. Volatile biomarkers of symptomatic and asymptomatic malaria infection in humans. Proc Natl Acad Sci U S A. 2018;115: 5780–5785. doi: 10.1073/pnas.1801512115 PubMed DOI PMC

Masyita A, Mustika Sari R, Dwi Astuti A, Yasir B, Rahma Rumata N, Emran TB, et al. Terpenes and terpenoids as main bioactive compounds of essential oils, their roles in human health and potential application as natural food preservatives. Food Chem X. 2022;13: 100217. doi: 10.1016/j.fochx.2022.100217 PubMed DOI PMC

Duarte JL, Di Filippo LD, Ribeiro TC, Silva ACJ, Hage-Melim LIDS, Duchon S, et al. Effective mosquito repellents: Myrcene- and Cymene-loaded nanohydrogels against PubMed DOI PMC

Borges LM, de Oliveira Filho JG, Ferreira LL, Louly CC, Pickett JA, Birkett MA. Identification of non-host semiochemicals for the brown dog tick, PubMed DOI

Zeringóta V, Pereira-Junior RA, Sarria ALF, Henrique ACC, Birkett MA, Borges LMF. Identification of a non-host semiochemical from miniature pinscher, PubMed DOI

Recent advances in Phlebotomine sand fly research: a review based on studies presented at ISOPS XI

A simplified system for the detection of antennal responses to host-borne volatile organic compounds in sand flies