An overview of studies on sex pheromones of insect vectors of pathogenic trypanosomatids of medical and veterinary importance
DOI:
https://doi.org/10.33448/rsd-v11i11.32864Keywords:
Insect vectors; Sex pheromones; Control strategies.Abstract
Insect vectors of Leishmaniases, Chagas disease and African trypanosomiasis remain human health, veterinary and economic problems worldwide. Several sex pheromones molecules that contribute to mating behavior have been identified in these vectors. These chemical signals are potential alternatives to traditional chemical insecticides. This review discusses the diversity of sex pheromone molecules and their role in the mating behavior of insect vectors of Leishmaniases, Chagas disease and African trypanosomiasis. The selection of studies was made based on research and review articles that presented sex pheromone aspects regarding insect vectors. In some species, these molecules have a dual function as serving as sex and aggregation pheromone. We also highlight the current knowledge of these substances as potential vector control tools. The studies revealed that sex pheromones applicability is largely experimental and restricted to some vectors. Based on these limitations, we included updated tables with the chemical identity of several sex pheromone compounds and other relevant information concerning the target species, which can contribute to future studies of control methodologies.
References
Akhoundi, M., Kuhls, K., Cannet, A., Votýpka, J., Marty, P., Delaunay, P., & Sereno, D. (2016). A Historical Overview of the Classification, Evolution, and Dispersion of Leishmania Parasites and Sandflies. PLoS Neglected Tropical Diseases, 10(3), 1–40.
Alvar, J., Vélez, I. D., Bern, C., Herrero, M., Desjeux, P., Cano, J., Jannin, J., et al. (2012). Leishmaniasis worldwide and global estimates of its incidence. PLoS ONE, 7(5).
Ando, K., Ohkuni, Y., Makino, H., Komatsu, A., Matsunuma, R., Nakashima, K., Asai, N., et al. (2002). A clinical review of pleurodesis for patients with poor performance status. British Medical Journal, 325, 203–206.
Araki, A. S., Vigoder, F. M., Bauzer, L. G. S. R., Ferreira, G. E. M., Souza, N. A., Araújo, I. B., Hamilton, J. G. C., et al. (2009). Molecular and behavioral differentiation among Brazilian populations of Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae). PLoS Neglected Tropical Diseases, 3(1), 1–12.
Baldwina, W. F., Knight, G., & Lynn, K. R. (1971). A Sex Pheromone In The Insect Rhodnius Prolixus (Hemiptera : Reduviidae). The Canadian Entomologist, 103(1), 18–22.
Barrett, M. P., Burchmore, R. J. S., Stich, A., Lazzari, J. O., Frasch, A. C., Cazzulo, J. J., & Krishna, S. (2003). The trypanosomiases. Lancet, 362(9394), 1469–1480.
Bekele, E. E., Eshetu, E., & Begejo, B. (2015). The Current Situation and Diagnostic Approach of Nagana in Africa Helminth control in Small runants View project Rational Strategic Internal Helminth parasites View project The Current Situation and Diagnostic Approach of Nagana in Africa: A review. Journal of Natural Sciences Research www.iiste.org ISSN, 5(17), 117–125. www.iiste.org
Bell, M. J., Sedda, L., Gonzalez, M. A., de Souza, C. F., Dilger, E., Brazil, R. P., Courtenay, O., et al. (2018). Attraction of Lutzomyia longipalpis to synthetic sex-aggregation pheromone: Effect of release rate and proximity of adjacent pheromone sources. PLoS Neglected Tropical Diseases, 12(12), 1–19.
Blomquist, G. J., Jurenka, R., Schal, C., & Tittiger, C. (2012). Pheromone Production: Biochemistry and Molecular Biology. Insect Endocrinology.
Bohman, B., Weinstein, A. M., Unelius, C. R., & Lorenzo, M. G. (2018). Attraction of Rhodnius prolixus males to a synthetic female-pheromone blend. Parasites and Vectors, 11(1). Parasites & Vectors.
Bray, D. P., Bandi, K. K., Brazil, R. P., Oliveira, A. G., & Hamilton, J. G. C. (2009). Synthetic Sex Pheromone Attracts the Leishmaniasis Vector Lutzomyia longipalpis (Diptera: Psychodidae) to Traps in the Field. Journal of Medical Entomology, 46(3), 428–434.
Bray, Daniel P., Alves, G. B., Dorval, M. E., Brazil, R. P., & Hamilton, J. G. C. (2010). Synthetic sex pheromone attracts the leishmaniasis vector Lutzomyia longipalpis to experimental chicken sheds treated with insecticide. Parasites and Vectors, 3(1), 1–11.
Bray, Daniel P., Carter, V., Alves, G. B., Brazil, R. P., Bandi, K. K., & Hamilton, J. G. C. (2014). Synthetic Sex Pheromone in a Long-Lasting Lure Attracts the Visceral Leishmaniasis Vector, Lutzomyia longipalpis, for up to 12 Weeks in Brazil. PLoS Neglected Tropical Diseases, 8(3).
Brazil, R. P., Caballero, N. N., & Hamilton, J. G. C. (2009). Identification of the sex pheromone of Lutzomyia longipalpis (Lutz & Neiva, 1912) (Diptera: Psychodidae) from Asuncián, Paraguay. Parasites and Vectors, 2(1), 13–15.
Brazil, R. P., & Hamilton, J. G. C. (2002). Isolation and identification of 9-methylgermacrene-B as the putative sex pheromone of Lutzomyia cruzi (Mangabeira, 1938) (Diptera: Psychodidae). Memorias do Instituto Oswaldo Cruz, 97(3), 435–436.
Brindley, M. D. (1930). On the metasternal scent-glands of certain Heteroptera. Trans. ent. SOC. Lond. 78, 199-207.
Burza, S., Croft, S. L., & Boelaert, M. (2018). Leishmaniasis. The Lancet, 392(10151), 951–970.
Cardoso, L., Schallig, H., Persichetti, M. F., & Pennisi, M. G. (2021). New epidemiological aspects of animal leishmaniosis in europe: The role of vertebrate hosts other than dogs. Pathogens, 10(3).
Carlson, D. A., Mramba, F., Sutton, B. D., Bernier, U. R., Geden, C. J., & Mori, K. (2005). Sex pheromone of the tsetse species, Glossina austeni: Isolation and identification of natural hydrocarbons, and bioassay of synthesized compounds. Medical and Veterinary Entomology, 19(4), 470–479.
Carlson, D. A., Nelson, D. R., Langley, P. A., Coates, T. W., Davis, T. L., & Leegwater-Van Der Linden, M. E. (1984). Contact sex pheromone in the tsetse fly Glossina pallidipes (Austen) Identification and Synthesis. Journal of Chemical Ecology, 10(3), 429–450.
Carlson, D. A., Sutton, B. D., & Bernier, U. R. (2000). Cuticular hydrocarbons of glossina austeni and g. pallidipes: Similarities between populations. Insect Science and its Application, 20(4), 281–294.
Carlson, L. and H. (1978). Sex Pheromone of the Tsetse Fly : Isolation , Identification , and Synthesis of Contact Aphrodisiacs, 201(4357), 750–753.
Casanova, C., Colla-Jacques, F. E., Hamilton, J. G. C., Brazil, R. P., & Shaw, J. J. (2015). Distribution of Lutzomyia longipalpis Chemotype Populations in São Paulo State, Brazil. PLoS Neglected Tropical Diseases, 9(3), 1–14.
Chagas, C. (1909). Nova tripanozomiaze humana: estudos sobre a morfolojia e o ciclo evolutivo do Schizotrypanum cruzi n. gen., n. sp., ajente etiolojico de nova entidade morbida do homem. Memórias do Instituto Oswaldo Cruz.
Chelbi, I., Zhioua, E., & Hamilton, J. G. C. (2011). Behavioral Evidence for the Presence of a Sex Pheromone in Male Phlebotomus papatasi Scopoli (Diptera: Psychodidae). Journal of Medical Entomology, 48(3), 518–525.
Cocchiararo-Bastias, L. M., Mijailovsky, S. J., Calderon-Fernández, G. M., Figueiras, A. N. L., & Juárez, M. P. (2011). Epicuticle Lipids Mediate Mate Recognition in Triatoma infestans. Journal of Chemical Ecology, 37(3), 246–252.
Courtenay, O., Dilger, E., Calvo-Bado, L. A., Kravar-Garde, L., Carter, V., Bell, M. J., Alves, G. B., et al. (2019). Sand fly synthetic sex-aggregation pheromone co-located with insecticide reduces the incidence of infection in the canine reservoir of visceral leishmaniasis: A stratified cluster randomised trial. PLoS Neglected Tropical Diseases, 13(10), 1–25.
Crespo, J. G., & Manrique, G. (2007). Mating behavior of the hematophagous bug Triatoma infestans: Role of Brindley’s and metasternal glands. Journal of Insect Physiology, 53(7), 708–714.
Depaquit, J., Grandadam, M., Fouque, F., Andry, P. E., & Peyrefitte, C. (2010). Arthropod-borne viruses transmitted by Phlebotomine sandflies in Europe: A review. Eurosurveillance, 15(10), 40–47.
Dufour, S., Castets, P., Pickett, J. A., & Hooper, A. M. (2012). A diastereoselective synthesis of (1SR,3SR,7RS)-3-methyl-α- himachalene, the sex pheromone of the sandfly, Lutzomyia longipalpis (Diptera: Psychodidae). Tetrahedron, 68(25), 5102–5108. Elsevier Ltd. Retrieved from http://dx.doi.org/10.1016/j.tet.2012.04.037
Durden, L. A., & Mullen, G. R. (2019). Introduction. Medical and Veterinary Entomology. Elsevier Inc. Retrieved from http://dx.doi.org/10.1016/B978-0-12-814043-7.00001-7
Englx, T., Michalkova, V., Weiss, B. L., Uzel, G. D., Takac, P., Miller, W. J., Abd-Alla, A. M. M., et al. (2018). Effect of antibiotic treatment and gamma-irradiation on cuticular hydrocarbon profiles and mate choice in tsetse flies (Glossina m. morsitans) 06 Biological Sciences 0605 Microbiology. BMC Microbiology, 18(Suppl 1).
Galvis-Ovallos, F., Casanova, C., Sevá, A. da P., & Galati, E. A. B. (2017). Ecological parameters of the (S)-9-methylgermacrene-B population of the Lutzomyia longipalpis complex in a visceral leishmaniasis area in São Paulo state, Brazil. Parasites and Vectors, 10(1), 1–9. Parasites & Vectors.
Gao, J. M., Qian, Z. Y., Hide, G., Lai, D. H., Lun, Z. R., & Wu, Z. D. (2020). Human African trypanosomiasis: The current situation in endemic regions and the risks for non-endemic regions from imported cases. Parasitology, 147(9), 922–931.
Golding, N., Wilson, A. L., Moyes, C. L., Cano, J., Pigott, D. M., Velayudhan, R., Brooker, S. J., et al. (2015). Integrating vector control across diseases. BMC Medicine, 13(1), 1–6. BMC Medicine.
González-Caballero, N., Rodríguez-Vega, A., Dias-Lopes, G., Valenzuela, J. G., Ribeiro, J. M. C., Carvalho, P. C., Valente, R. H., et al. (2014). Expression of the mevalonate pathway enzymes in the Lutzomyia longipalpis (Diptera: Psychodidae) sex pheromone gland demonstrated by an integrated proteomic approach. Journal of Proteomics, 96, 117–132. Elsevier B.V. http://dx.doi.org/10.1016/j.jprot.2013.10.028
González-Caballero, N., Valenzuela, J. G., Ribeiro, J. M. C., Cuervo, P., & Brazil, R. P. (2013). Transcriptome exploration of the sex pheromone gland of Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae). Parasites and Vectors, 6(1), 1–16.
González, M. A., Bandi, K. K., Bell, M. J., Brazil, R. P., Dilger, E., Gonza, M. A., Guerrero, A., et al. (2017). A temporal comparison of sex-aggregation pheromone gland content and dynamics of release in three members of the Lutzomyia longipalpis (Diptera: Psychodidae) species complex. PLoS Neglected Tropical Diseases, 1–17.
González, M. A., Bell, M. J., Bernhardt, S. A., Brazil, R. P., DIlger, E., Courtenay, O., & Hamilton, J. G. C. (2019). Susceptibility of wild-caught Lutzomyia longipalpis (Diptera: Psychodidae) sand flies to insecticide after an extended period of exposure in western São Paulo, Brazil. Parasites and Vectors, 12(1), 1–9. BioMed Central. https://doi.org/10.1186/s13071-019-3364-4
González, M. A., Bell, M., Souza, C. F., Maciel-De-freitas, R., Brazil, R. P., Courtenay, O., & Hamilton, J. G. C. (2020). Synthetic sex-aggregation pheromone of Lutzomyia longipalpis, the South American sand fly vector of leishmania infantum, attracts males and females over long-distance. PLoS Neglected Tropical Diseases, 14(10), 1–18.
Hamilton, J. G. C., Brazil, R. P., Campbell-Lendrum, D., Davies, C. R., Kelly, D. W., Pessoa, F. A. C., & De Queiroz, R. G. (2001). Distribution of putative male sex pheromones among Lutzomyia sandflies (Diptera: Psychodidae). Annals of Tropical Medicine and Parasitology, 96(1), 83–92.
Hamilton, J. G. C., Brazil, R. P., & Maingon, R. (2004). A Fourth Chemotype of Lutzomyia longipalpis (Diptera: Psychodidae) from Jaíbas, Minas Gerais State, Brazil. Journal of Medical Entomology, 41(6), 1021–1026.
Hamilton, J. G. C., Dawson, G. W., & Pickett, J. A. (1996a). 9-methylgermacrene-B; proposed structure for novel homosesquiterpene from the sex pheromone glands of Lutzomyia longipalpis (Diptera: Psychodidae) from Lapinha, Brazil. Journal of Chemical Ecology, 22(8), 1477–1491.
Hamilton, J. G. C., Dawson, G. W., & Pickett, J. A. (1996b). 3-Methyl-α-himachalene: Proposed structure for novel homosesquiterpene sex pheromone of Lutzomyia longipalpis (Diptera: Psychodidae) from Jacobina, Brazil. Journal of Chemical Ecology, 22(12), 2331–2340.
Hamilton, J. G. C., Maingon, R. D. C., Alexander, B., Ward, R. D., & Brazil, R. P. (2005). Analysis of the sex pheromone extract of individual male Lutzomyia longipalpis sandflies from six regions in Brazil. Medical and Veterinary Entomology, 19(4), 480–488.
Hamilton, J. G. C., & Ward, R. D. (1994). Chemical analysis of a putative sex pheromone from Lutzomyia pessoai (Diptera: Psychodidae). Annals of Tropical Medicine and Parasitology, 88(4), 405–412.
Hamilton, J. G. C., Ward, R. D., Dougherty, M. J., & Maignon, R. (1996). Comparison of the sex-pheromone components of Lutzomyia longipalpis (Diptera: Psychodidae) from areas of visceral and atypical cutaneous leishmaniasis in Honduras and Costa Rica. Annals of Tropical Medicine and Parasitology, 90(5), 533–541.
Hamilton, J. G., & Ward, R. D. (1991). Gas-chromatographic analysis of Lutzomyia longipalpis tergal pheromone gland extract. Parassitologia, 33 Suppl(January), 283–289.
Hertig., C. W. Y. M. (1926). The development of flagellates in Chinese sandflies (phleboto- mus) fed on hamsters infected with Leishmania donovani. Proceedings of the Society for Experimental Biology and Medicine, 23(7), 611–615.
Hickner, P. V., Timoshevskaya, N., Nowling, R. J., Labbé, F., Nguyen, A. D., McDowell, M. A., Spiegel, C. N., et al. (2020). Molecular signatures of sexual communication in the phlebotomine sand flies. PLoS Neglected Tropical Diseases, 14(12), 1–18.
Himeidan, Y. E., Temu, E. A., & Kweka, E. J. (2012). Insecticides for Vector-Borne Diseases: Current Use, Benefits, Hazard and Resistance. Insecticides - Advances in Integrated Pest Management, (January).
Huyton, P. M., Langley, P. A., Carlson, D. A., & Schwarz, M. (1980). Specificity of contact sex pheromones in tsetse flies, Glossina spp. Physiological Entomology, 5(3), 253–264.
Jansen, A. M., & Roque, A. L. R. (2010). Domestic and Wild Mammalian Reservoirs. American Trypanosomiasis, 249–276.
Jansen, A. M., Xavier, S. C. C., & Roque, A. L. R. (2015). The multiple and complex and changeable scenarios of the Trypanosoma cruzi transmission cycle in the sylvatic environment. Acta Tropica, 151(1), 1–15. Elsevier B.V. http://dx.doi.org/10.1016/j.actatropica.2015.07.018
Johansson, B. G., & Jones, T. M. (2007). The role of chemical communication in mate choice. Biological Reviews, 82(2), 265–289.
Kasozi, K. I., Zirintunda, G., Ssempijja, F., Buyinza, B., Alzahrani, K. J., Matama, K., Nakimbugwe, H. N., et al. (2021). Epidemiology of Trypanosomiasis in Wildlife—Implications for Humans at the Wildlife Interface in Africa. Frontiers in Veterinary Science, 8(June), 1–15.
Kitchen, L. W., Lawrence, K. L., & Coleman, R. E. (2009). The Role of the United States Military in the Development of Vector Control Products, Including Insect Repellents, Insecticides, and Bed Nets. Journal of Vector Ecology, 34(1), 50–61.
Kumar, V., Krishnakumari, B., Kesari, S., Kumari, K., Kumar, R., Ranjan, A., & Das, P. (2012). Preliminary Observations on the Female Behavior of the Indian Sandfly Vector, Phlebotomus argentipes (Diptera: Psychodidae). Annals of the Entomological Society of America, 105(2), 201–205.
Langley, P. A., Coates, T. W., Carlson, D. A., Vale, G. A., & Marshall, J. (1982). Prospects for autosterilisation of tsetse flies, Glossina spp. (Diptera: Glossinidae), using sex pheromone and bisazir in the field. Bulletin of Entomological Research, 72(2), 319–327.
Lidani, K. C. F., Andrade, F. A., Bavia, L., Damasceno, F. S., Beltrame, M. H., Messias-Reason, I. J., & Sandri, T. L. (2019). Chagas disease: From discovery to a worldwide health problem. Journal of Physical Oceanography, 49(6), 1–13.
Lopes, R. L., Santos-Mallet, J. R., Barbosa, C. F., Gomes, S. A. O., & Spiegel, C. N. (2020). Morphological and ultrastructural analysis of an important place of sexual communication of Rhodnius prolixus (Heteroptera: Reduviidae): the Metasternal Glands. Tissue and Cell, 67(September), 101416. Elsevier. https://doi.org/10.1016/j.tice.2020.101416
Lorenzo, M. G., Vidal, D. M., & Zarbin, P. H. G. (2014). Control of Neglected Disease Insect Vectors: Future Prospects for the Use of Tools Based on Behavior Manipulation-Interference. Journal of the Brazilian Chemical Society, 25(10), 1799–1809.
Lukeš, J., Skalický, T., Týč, J., Votýpka, J., & Yurchenko, V. (2014). Evolution of parasitism in kinetoplastid flagellates. Molecular and Biochemical Parasitology, 195(2), 115–122.
Maggi, R. G., & Krämer, F. (2019). A review on the occurrence of companion vector-borne diseases in pet animals in Latin America. Parasites and Vectors, 12(1), 1–37. BioMed Central. https://doi.org/10.1186/s13071-019-3407-x
Maingon, R. D. C., Ward, R. D., Hamilton, J. G. C., Noyes, H. A., Souza, N., Kemp, S. J., & Watts, P. C. (2003). Genetic identification of two sibling species of Lutzomyia longipalpis (Diptera: Psychodidae) that produce distinct male sex pheromones in Sobral, Ceará State, Brazil. Molecular Ecology, 12(7), 1879–1894.
Manrique, G., Vitta, A. C. R., Ferreira, R. A., Zani, C. L., Unelius, C. R., Lazzari, C. R., Diotaiuti, L., et al. (2006). Chemical communication in chagas disease vectors. Source, identity, and potential function of volatiles released by the metasternal and Brindley’s glands of Triatoma infestans adults. Journal of Chemical Ecology, 32(9), 2035–2052.
Marchant, A., Mougel, F., Jacquin-Joly, E., Costa, J., Almeida, C. E., & Harry, M. (2016). Under-Expression of Chemosensory Genes in Domiciliary Bugs of the Chagas Disease Vector Triatoma brasiliensis. PLoS Neglected Tropical Diseases, 10(10), 1–26.
Maroli, M., Feliciangeli, M. D., Bichaud, L., Charrel, R. N., & Gradoni, L. (2013). Phlebotomine sandflies and the spreading of leishmaniases and other diseases of public health concern. Medical and Veterinary Entomology, 27(2), 123–147.
Maslov, D. A., Votýpka, J., Yurchenko, V., & Lukeš, J. (2013). Diversity and phylogeny of insect trypanosomatids: All that is hidden shall be revealed. Trends in Parasitology, 29(1), 43–52.
May-Concha, I. J., Cruz-López, L. C., Rojas, J. C., & Ramsey, J. M. (2018). “Sweeter than a rose”, at least to Triatoma phyllosoma complex males (Triatominae: Reduviidae). Parasites & vectors, 11:95.
May-Concha, I., Rojas, J. C., Cruz-López, L., Millar, J. G., & Ramsey, J. M. (2013). Volatile compounds emitted by Triatoma dimidiata, a vector of Chagas disease: Chemical analysis and behavioural evaluation. Medical and Veterinary Entomology, 27(2), 165–174.
May-Concha, Irving, Rojas, J. C., Cruz-López, L., Ibarra-Cerdeña, C. N., & Ramsey, J. M. (2015). Volatile compound diversity and conserved alarm behaviour in Triatoma dimidiata. Parasites and Vectors, 8(1), 1–14.
McDowell, P. G., Whitehead, D. L., Chaudhury, M. F. B., & Snow, W. F. (1981). The isolation and identification of the cuticular sex-stimulant pheromone of the tsetse Glossina pallidipes Austen (Diptera:Glossinidae). International Journal of Tropical Insect Science, 2(03), 181–187.
Moreno, J., & Alvar, J. (2002). Canine leishmaniasis: Epidemiological risk and the experimental model. Trends in Parasitology, 18(9), 399–405.
NIgam, Y., & Ward, R. D. (1991). The effect of male sandfly pheromone and host factors as attractants for female Lutzomyia longipalpis (Diptera: Psychodidae). Physiological Entomology, 16(3), 305–312.
Oliveira, D. S., Brito, N. F., Franco, T. A., Moreira, M. F., Leal, W. S., & Melo, A. C. A. (2018). Functional characterization of odorant binding protein 27 (RproOBP27) from Rhodnius prolixus antennae. Frontiers in Physiology, 9(AUG), 1–11.
Ondarza, R. N., Gutiérrez-Martínez, A., & Malo, E. A. (1986). Evidence for the presence of sex and aggregation pheromones from Triatoma mazzottii (Hemiptera: Reduviidae). Journal of economic entomology, 79(3), 688–692.
Palatnik-De-Sousa, C. B., & Day, M. J. (2011). One Health: The global challenge of epidemic and endemic leishmaniasis. Parasites and Vectors, 4(1), 1–10.
Palframan, M. J., Bandi, K. K., Hamilton, J. G. C., & Pattenden, G. (2018). Sobralene, a new sex-aggregation pheromone and likely shunt metabolite of the taxadiene synthase cascade, produced by a member of the sand fly Lutzomyia longipalpis species complex. Tetrahedron Letters, 59(20), 1921–1923. The Authors. https://doi.org/10.1016/j.tetlet.2018.03.088
Pontes, G. B., & Lorenzo, M. G. (2012). Female metasternal gland odours mediate male aggregation in Rhodnius prolixus, a triatomid bug. Medical and Veterinary Entomology, 26(1), 33–36.
Pontes, Gina B., Bohman, B., Unelius, C. R., & Lorenzo, M. G. (2008). Metasternal gland volatiles and sexual communication in the triatomine bug, Rhodnius prolixus. Journal of Chemical Ecology, 34(4), 450–457.
Quinnell, R. J., & Courtenay, O. (2009). Transmission, reservoir hosts and control of zoonotic visceral leishmaniasis. Parasitology, 136(14), 1915–1934.
Ready, P. D. (2014). Epidemiology of visceral leishmaniasis. Clinical Epidemiology, 6(1), 147–154.
Ribeiro, R. R., Michalick, M. S. M., Da Silva, M. E., Dos Santos, C. C. P., Frézard, F. J. G., & Da Silva, S. M. (2018). Canine Leishmaniasis: An Overview of the Current Status and Strategies for Control. BioMed Research International, 2018(Cl).
Rivero, A., Vézilier, J., Weill, M., Read, A. F., & Gandon, S. (2010). Insecticide control of vector-borne diseases: When is insecticide resistance a problem? PLoS Pathogens, 6(8), 5–6.
Salomón, O. D., Araki, A. S., Hamilton, J. G. C., Acardi, S. A., & Peixoto, A. A. (2010). Sex pheromone and period gene characterization of Lutzomyia longipalpis sensu lato (Lutz & Neiva) (Diptera: Psychodidae) from Posadas, Argentina. Memorias do Instituto Oswaldo Cruz, 105(7), 928–930.
Serrano, A. K., Rojas, J. C., Cruz-López, L. C., Malo, E. A., Mikery, O. F., & Castillo, A. (2016). Presence of putative male-produced sex pheromone in Lutzomyia cruciata (Diptera: Psychodidae), Vector of leishmania Mexicana. Journal of Medical Entomology, 53(6), 1261–1267.
De Souza, N. A., Brazil, R. P., & Araki, A. S. (2017). The current status of the Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae) species complex. Memorias do Instituto Oswaldo Cruz, 112(3), 161–174.
Spiegel, C. N., Jeanbourquin, P., Guerin, P. M., Hooper, A. M., Claude, S., Tabacchi, R., Sano, S., et al. (2005). (1S,3S,7R)-3-methyl-α-himachalene from the male sandfly Lutzomyia longipalpis (Diptera: Psychodidae) induces neurophysiological responses and attracts both males and females. Journal of Insect Physiology, 51(12), 1366–1375.
Spiegel, C. N., Brazil, R. P., & Soares, M. J. (2002). Ultrastructure of male sex pheromone glands in abdominal tergites of five Lutzomyia sandfly species (Diptera: Psychodidae). Arthropod Structure and Development, 30(3), 219–227.
Spiegel, C. N., Brazil, R. P., & Soares, M. J. (2004). Ultrastructural cytochemistry of the sex pheromone glands of Lutzomyia cruzi male sand flies (Diptera: Psychodidae: Phlebotominae). Arthropod Structure and Development, 33(4), 399–404.
Spiegel, C. N., Dias, D. B. do. S., Araki, A. S., Hamilton, J. G. C., Brazil, R. P., & Jones, T. M. (2016). The Lutzomyia longipalpis complex: a brief natural history of aggregation-sex pheromone communication. Parasites and Vectors, 9(1), 1–15. Parasites & Vectors. Retrieved from http://dx.doi.org/10.1186/s13071-016-1866-x
Spiegel, C. N, Batista-pereira, L. G., Bretas, J. A. C., Eiras, Á. E., Hooper, A. M., Pelxoto, A. A., & Soares, M. J. (2011). Pheromone Gland Development and Pheromone Production in Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae), 48(3), 489–495.
Staddon, B. W. (1979). The Scent Glands of Heteroptera. Advances in Insect Physiology, 14(C), 351–418.
Steiger, S., & Stökl, J. (2014). The Role of Sexual Selection in the Evolution of Chemical Signals in Insects. Insects, 5(2), 423–438.
Steverding, D. (2008). The history of African trypanosomiasis. Parasites and Vectors, 1(1), 1–8.
Vitta, A. C. R, Bohman, B., Unelius, C. R., & Lorenzo, M. G. (2009). Behavioral and electrophysiological responses of Triatoma brasiliensis males to volatiles produced in the metasternal glands of females. Journal of Chemical Ecology, 35(10), 1212–1221.
Vitta, A. C. R., Serrão, J. E., Lima, E. R., & Villela, E. F. (2009). The metasternal and Brindley’s glands of Triatoma brasiliensis Neiva (Hemiptera: Reduviidae). Neotropical entomology, 38(2), 231–236.
Ward, R. D., Hamilton, J. G. C., Dougherty, M., Falcao, A. L., Feliciangeli, M. D., Perez, J. E., & Veltkamp, C. J. (1993). Pheromone disseminating structures in tergites of male phlebotomines (Diptera: Psychodidae). Bulletin of Entomological Research, 83(3), 437–445.
Watts, P. C., Hamilton, J. G. C., Ward, R. D., Noyes, H. A., Souza, N. A., Kemp, S. J., Feliciangeli, M. D., et al. (2005). Male sex pheromones and the phylogeographic structure of the Lutzomyia longipalpis species complex (Diptera: Psychodidae) from Brazil and Venezuela. American Journal of Tropical Medicine and Hygiene, 73(4), 734–743.
Weirauch, C. (2006). Metathoracic glands and associated evaporatory structures in Reduvioidea (Heteroptera: Cimicomorpha), with observation on the mode of function of the metacoxal comb. European Journal of Entomology, 103(1), 97–108.
Wilson, A. L., Courtenay, O., Kelly-Hope, L. A., Scott, T. W., Takken, W., Torr, S. J., & Lindsay, S. W. (2020). The importance of vector control for the control and elimination of vector-borne diseases. PLoS Neglected Tropical Diseases (Vol. 14).
Wyatt, T. D. (2017). Pheromones. Current Biology, 27(15), R739–R743.
Zacharias, C. A., Pontes, G. B., Lorenzo, M. G., & Manrique, G. (2010). Flight initiation by male Rhodnius prolixus is promoted by female odors. Journal of Chemical Ecology, 36(4), 449–451.
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