Hostname: page-component-848d4c4894-ndmmz Total loading time: 0 Render date: 2024-05-06T01:53:31.492Z Has data issue: false hasContentIssue false

Blood meal sources of mosquitoes (Diptera: Culicidae) in domestic and open green environments from two urbanisations of temperate Argentina

Published online by Cambridge University Press:  19 December 2023

Karelly Melgarejo-Colmenares*
Affiliation:
IIIA-UNSAM-CONICET, Instituto de Investigación e Ingeniería Ambiental, Escuela de Hábitat y Sostenibilidad, San Martín, Provincia de Buenos Aires, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
Darío Vezzani
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina Instituto Multidisciplinario sobre Ecosistemas y Desarrollo Sustentable, UNCPBA-CICPBA, Tandil, Provincia de Buenos Aires, Argentina
Alejandra Gallego
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina Instituto Multidisciplinario sobre Ecosistemas y Desarrollo Sustentable, UNCPBA-CICPBA, Tandil, Provincia de Buenos Aires, Argentina
María V Cardo
Affiliation:
IIIA-UNSAM-CONICET, Instituto de Investigación e Ingeniería Ambiental, Escuela de Hábitat y Sostenibilidad, San Martín, Provincia de Buenos Aires, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
*
Corresponding author: Karelly Melgarejo-Colmenares; Email: kmelgarejo@unsam.edu.ar

Abstract

Understanding the blood-feeding patterns of mosquitoes is essential for evaluating their potential as disease vectors, especially in urban areas where mosquitoes coexist with humans, domestic animals and wildlife. This study aimed to bridge a substantial gap in regional knowledge by identifying the blood meal sources of field-collected mosquitoes in domestic and open green environments from two urbanisations of temperate Argentina, the Área Metropolitana de Buenos Aires (AMBA) and Tandil, using molecular techniques. Female mosquitoes were collected from November 2019 to March 2020 and April–May 2021. A bipartite network analysis was performed for each environment and urbanisation. A total of 103 blood meals from Aedes (2 species) and Culex (7 species) were identified. Among these, five mammal and 18 bird species were recognised as hosts. Aedes mosquitoes exclusively fed on mammals, while Culex mosquitoes exhibited a broader host range including both birds and mammals. In AMBA, the open green environments were composed by more mosquito species than the domestic environments, while both presented similar numbers of vertebrate species. In contrast, in open green environments from Tandil only blood-fed Aedes albifasciatus were collected. For open green environments of AMBA and domestic environments of Tandil, results suggested some degree of host selection. For the three main vectors of diseases in the region, Aedes aegypti, Ae. albifasciatus and Culex pipiens molestus, we present the first molecular evidence of human blood meals in South America. Epidemiological significance of the present findings is discussed.

Type
Research Paper
Copyright
Copyright © The Author(s), 2023. 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.)

References

Albaladejo, C, Barthe, L, Bustos, R, Iscaro, M, Petrantonio, M and Taulelle, F (2017) The role of intermediate cities in Argentinan Pampa in the Province of Buenos Aires regarding the structuration of agrarian areas: an analysis of governance process in three municipalities. Territoire en mouvement Revue de géographie et aménagement 33, 121.Google Scholar
Almeida-Neto, M, Guimarães, P, Guimarães, PR, Loyola, RD and Ulrich, W (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117, 12271239.CrossRefGoogle Scholar
Almirón, WR and Brewer, MM (1995) Host preference of Culicidae (Diptera) collected in central Argentina. Revista de Saúde Pública 29, 108114.CrossRefGoogle ScholarPubMed
Andersson, E (2006) Urban landscapes and sustainable cities. Ecology and Society 11, 34.CrossRefGoogle Scholar
Bahnck, CM and Fonseca, DM (2006) Rapid assay to identify the two genetic forms of Culex (Culex) pipiens L. (Diptera: Culicidae) and hybrid populations. The American Journal of Tropical Medicine and Hygiene 75, 251255.CrossRefGoogle ScholarPubMed
Bascompte, J, Jordano, P and Olesen, JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312, 431433.CrossRefGoogle ScholarPubMed
Bellekom, B, Hackett, TD and Lewis, OT (2021) A network perspective on the vectoring of human disease. Trends in Parasitology 37, 391400.CrossRefGoogle ScholarPubMed
BEN (2023) Boletín Epidemiológico Nacional N° 663, Semana Epidemiológica 30. Argentina: Ministerio de Salud.Google Scholar
Blüthgen, N, Menzel, F and Blüthgen, N (2006) Measuring specialization in species interaction networks. BMC Ecology 6, 9.CrossRefGoogle ScholarPubMed
Cardo, MV and Vezzani, D (2023) Host-mosquito interactions in rural and urban equestrian facilities from temperate Argentina. Medical and Veterinary Entomology 37, 816825. doi: https://doi.org/10.1111/mve.12686CrossRefGoogle Scholar
Cardo, MV, Vezzani, D and Carbajo, AE (2011) Community structure of groundwater breeding mosquitoes driven by land use in a temperate wetland of Argentina. Acta Tropica 119, 7683.CrossRefGoogle Scholar
Cardo, MV, Vezzani, D and Carbajo, AE (2012) Oviposition strategies of temporary pool mosquitoes in relation to weather, tidal regime and land use in a temperate wetland. Bulletin of Entomological Research 102, 651662.CrossRefGoogle Scholar
Cardo, MV, Rubio, A, Junges, M, Vezzani, D and Carbajo, AE (2018) Heterogeneous distribution of Culex pipiens, Culex quinquefasciatus and their hybrids along the urbanisation gradient. Acta Tropica 178, 229235.CrossRefGoogle ScholarPubMed
Cardo, MV, Rubio, A, Junges, MT, Vezzani, D and Carbajo, AE (2020a) A rural-urban latitudinal study of the distributions of Culex quinquefasciatus and Culex pipiens bioforms in their southernmost sympatric fringe. Medical and Veterinary Entomology 34, 3443.CrossRefGoogle ScholarPubMed
Cardo, MV, Rubio, A, Vezzani, D and Carbajo, AE (2020b) Assessment of Culex pipiens bioforms in the world's southernmost distribution limit. Memórias do Instituto Oswaldo Cruz 115, e190390.CrossRefGoogle ScholarPubMed
Cardo, MV, Carbajo, AE, Mozzoni, C, Kliger, M and Vezzani, D (2023) Blood feeding patterns of the Culex pipiens complex in equestrian land uses and their implications for arboviral encephalitis risk in temperate Argentina. Zoonoses and Public Health 70, 256268.CrossRefGoogle ScholarPubMed
CEPAL (2017) Comisión Económica para América Latina y el Caribe. Desarrollo sostenible, urbanización y desigualdad en América Latina y el Caribe. Dinámicas y desafíos para el cambio estructural. (LC/PUB.2017/19), Santiago.Google Scholar
Charlwood, JD, Graves, PM and de Marsharll, TF (1988) Evidence for a memorized home range in Anopheles farauti females from Papua New Guinea. Medical and Veterinary Entomology 2, 101108.CrossRefGoogle ScholarPubMed
Clements, AN (1999). The Biology of Mosquitoes. Vol. 2. Sensory, reception and behaviour. Wallinford: CABI Publishing.Google Scholar
Climate-data.org (2023) CLIMATE: ARGENTINA. Available at https://en.climate-data.org/south-america/argentina-11/Google Scholar
Collins, JP, Kinzig, A, Grimm, NB, Fagan, WF, Hope, D, Wu, J and Borer, ET (2000) A new urban ecology. Modeling human communities as integral parts of ecosystems poses special problems for the development and testing of ecological theory. American Scientist 88, 416425.CrossRefGoogle Scholar
Contigiani, MS, Díaz, LA and Spinsanti, LI (2016) Arbovirus. In Berón, C, Campos, RE, Gleiser, RM, Díaz Nieto, LM, Salomón, OD and Schweigmann, N (eds), Investigaciones Sobre Mosquitos de Argentina. Primera edición. Mar del Plata: Universidad Nacional de Mar del Plata, pp. 157178.Google Scholar
Davis, MW (2021) ApE – A plasmid Editor. Available at https://jorgensen.biology.utah.edu/wayned/ape/.Google Scholar
de Carvalho, GC, Malafronte Rdos, S, Miti Izumisawa, C, Souza Teixeira, R, Natal, L and Marrelli, MT (2014) Blood meal sources of mosquitoes captured in municipal parks in São Paulo, Brazil. Journal of Vector Ecology 39, 146152.CrossRefGoogle ScholarPubMed
Díaz, LA, Quaglia, A, Flores, FS and Contigiani, MS (2011) Virus West Nile en Argentina: un agente infeccioso emergente que plantea nuevos desafíos. Hornero 26, 528.CrossRefGoogle Scholar
Díaz, LA, Albrieu Llinás, G, Vázquez, A, Tenorio, A and Contigiani, MS (2012) Silent circulation of St. Louis encephalitis virus prior to an encephalitis outbreak in Cordoba, Argentina (2005). PLoS Neglected Tropical Disease 6, e1489.CrossRefGoogle Scholar
Díaz, A, Flores, FS, Quaglia, AI and Contigiani, MS (2018) Evaluation of Argentinean bird species as amplifying hosts for St. Louis Encephalitis Virus (Flavivirus, Flaviviridae). The American Journal of Tropical Medicine and Hygiene 99, 216221.CrossRefGoogle ScholarPubMed
Dunne, JA, Williams, RJ and Martinez, ND (2002) Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecology Letters 5, 558567.CrossRefGoogle Scholar
Gomes, B, Sousa, C, Vicente, JL, Pinho, L, Calderón, I, Arez, E, Almeida, A, Donnelly, M and Pinto, J (2013) Feeding patterns of molestus and pipiens forms of Culex pipiens (Diptera: Culicidae) in a region of high hybridization. Parasites and Vectors 6, 93.CrossRefGoogle Scholar
Goodman, H, Egizi, A, Fonseca, DM, Leisnham, PT and LaDeau, SL (2018) Primary blood-hosts of mosquitoes are influenced by social and ecological conditions in a complex urban landscape. Parasites and Vectors 11, 218.CrossRefGoogle Scholar
Groenewegen, PP, Van den Berg, AE, De Vries, S and Verheij, RA (2006) Vitamin G: effects of green space on health, well-being, and social safety. BMC Public Health 6, 149.CrossRefGoogle ScholarPubMed
Hack, WH, Torales, GJ, Bar, ME and Oscherov, B (1978) Observaciones etológicas sobre culícidos de Corrientes. Revista de la Sociedad Entomológica Argentina 37, 137151.Google Scholar
Harrington, L, Edman, JD and Scott, TW (2001) Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? Journal of Medical Entomology 38, 411422.CrossRefGoogle ScholarPubMed
Hernandez-Colina, A, Gonzalez-Olvera, M, Lomax, E, Townsend, F, Maddox, A, Hesson, JC, Sherlock, K, Ward, D, Eckley, L, Vercoe, M, Lopez, J and Baylis, M (2021) Blood-feeding ecology of mosquitoes in two zoological gardens in the United Kingdom. Parasites and Vectors 14, 249.CrossRefGoogle ScholarPubMed
Hopken, MW, Reyes-Torres, LJ, Scavo, N, Piaggio, AJ, Abdo, Z, Taylor, D, Pierce, J and Yee, DA (2021) Temporal and spatial blood feeding patterns of urban mosquitoes in the San Juan Metropolitan Area, Puerto Rico. Insects 12, 129.CrossRefGoogle Scholar
Hoyos, J, Carrasquilla, MC, León, C, Montgomery, JM, Salyer, S, Komar, N and González, C (2021) Host selection pattern and flavivirus screening of mosquitoes in a disturbed Colombian rainforest. Scientific Reports 11, 18656.CrossRefGoogle Scholar
INDEC (2022) Instituto Nacional de Estadística y Censos. Censo nacional de población. Secretaría de planeación, Presidencia de la Nación, Argentina.Google Scholar
Jansen, CC, Webb, CE, Graham, GC, Craig, SB, Zborowski, P, Ritchie, SA, Russel, RC and van den Hurk, AF (2009) Blood sources of mosquitoes collected from urban and peri-urban environments in eastern Australia with species-specific molecular analysis of avian blood meals. The American Journal of Tropical Medicine and Hygiene 81, 849857.CrossRefGoogle Scholar
Kent, RJ (2009) Molecular methods for arthropod bloodmeal identification and applications to ecological and vector-borne disease studies. Molecular Ecology Resources 9, 418.CrossRefGoogle Scholar
Leveau, LM and Zuria, I (2017) Flocking the city: avian demography and population dynamics in urban Latin America. Avian Ecology in Latin American Cityscapes, 5777.CrossRefGoogle Scholar
Lyimo, IN and Ferguson, H (2009) Ecological and evolutionary determinants of host species choice in mosquito vectors. Trends in Parasitology 25, 189196.CrossRefGoogle ScholarPubMed
Marconi, PL, Perelman, PE and Salgado, VG (2022) Green in times of COVID-19: urban green space relevance during the COVID-19 pandemic in Buenos Aires City. Urban Ecosystems 25, 941953.CrossRefGoogle ScholarPubMed
Melgarejo-Colmenares, K, Cardo, MV and Vezzani, D (2022) Blood feeding habits of mosquitoes: hardly a bite in South America. Parasitology Research 121, 18291852.CrossRefGoogle ScholarPubMed
Migueltorena, A (2019) Producción de la vivienda y mercado inmobiliario en la ciudad intermedia de Tandil (Argentina), a comienzos del siglo XXI. Boletim Campineiro de Geografa 9, 139163.CrossRefGoogle Scholar
Municipio de Tandil (2023) Espacio Verde Público. Available at https://gobiernoabierto.tandil.gov.ar/acceso-informacion-publica/ambiente/espacio-verde-publico/ (accesed 18 May 2023).Google Scholar
National Center for Biotechnology Information (NCBI) [Internet] (2022) National Center for Biotechnology Information. Bethesda, MD: National Library of Medicine (US), [1988] – [cited 2023 Dec 03]. Available from: https://www.ncbi.nlm.nih.gov/.Google Scholar
Observatorio, AMBA (2023) Available at https://observatorioamba.org/ (accesed 18 May 2023).Google Scholar
Orsborne, J, Furuya-Kanamori, L, Jeffries, CL, Kristan, M, Mohammed, AR, Afrane, YA, O'Reilly, K, Massad, E, Drakeley, C, Walker, T and Yakob, L (2019) Investigating the blood-host plasticity and dispersal of Anopheles coluzzii using a novel field-based methodology. Parasites and Vectors 12, 143.CrossRefGoogle ScholarPubMed
Patefield, WM (1981) Algorithm AS 159: an efficient method of generating random R × C tables with given Rowand column totals. Journal of the Royal Statistical Society Series C 30, 9197.Google Scholar
Pickett, STA, Cadenasso, ML, Grove, JM, Boone, CG, Groffman, PM, Irwin, E, Kaushal, SS, Marshall, V, Mcgrath, BP, Nilon, CH, Pouyat, RV, Szlavecz, K and Warren, Troy A (2011) Urban ecological systems: Scientific foundations and a decade of progress. Journal of Environmental Management 92, 331362.CrossRefGoogle Scholar
Poisot, T, Lepennetier, G, Martinez, E, Ramsayer, J and Hochberg, ME (2011) Resource availability affects the structure of a natural bacteria-bacteriophage community. Biology Letters 7, 201204.CrossRefGoogle ScholarPubMed
Ramos, HF, Nunes, FG and dos Santos, AM (2020) Índice de áreas verdes como estratégia ao desenvolvimento urbano sustentável das Regiões Norte, Noroeste e Meia Ponte de Goiânia-GO, Brasil. Cuadernos de Geografía: Revista Colombiana de Geografía 29, 86101.Google Scholar
Reeves, LE, Gillett-Kaufman, JL, Kawahara, AY and Kaufman, PE (2018) Barcoding blood meals: new vertebrate-specific primer sets for assigning taxonomic identities to host DNA from mosquito blood meals. PLoS Neglected Tropical Diseases 12, e0006767.CrossRefGoogle ScholarPubMed
Romanello, M, McGushin, A, Di Napoli, C, Drummond, P, Hughes, N, Jamart, L, Kennard, H, Lampard, P, Solano Rodriguez, B, Arnell, N, Ayeb-Karlsson, S, Belesova, K, Cai, W, Campbell-Lendrum, D, Capstick, S, Chambers, J, Chu, L, Ciampi, L, Dalin, C, Dasandi, N, Dasgupta, S, Davies, M, Dominguez-Salas, P, Dubrow, R, Ebi, K, Eckelman, M, Ekins, P, Escobar, L, Georgeson, L, Grace, D, Graham, H, Gunther, S, Hartinger, S, He, K, Heaviside, C, Hess, J, Hsu, SC, Jankin, S, Jimenez, M, Kelman, I, Kiesewetter, G, Kinney, P, Kjellstrom, T, Kniveton, D, Lee, J, Lemke, B, Liu, Y, Liu, Z, Lott, M, Lowe, R, Martinez-Urtaza, J, Maslin, M, McAllister, L, McMichael, C, Mi, Z, Milner, J, Minor, K, Mohajeri, N, Moradi-Lakeh, M, Morrissey, K, Munzert, S, Murray, K, Neville, T, Nilsson, M, Obradovich, N, Odhiambo-Sewe, M, Oreszczyn, T, Otto, M, Owfi, F, Pearman, O, Pencheon, D, Rabbaniha, M, Robinson, E, Rocklöv, J, Salas, R, Semenza, J, Sherman, J, Shi, L, Springmann, M, Tabatabaei, M, Taylor, J, Trinanes, J, Shumake-Guillemot, J, Vu, B, Wagner, F, Wilkinson, P, Winning, M, Yglesias, M, Zhang, S, Gong, P, Montgomery, H, Costello, A and Hamilton, I (2021) The 2021 report of the Lancet Countdown on health and climate change: code red for a healthy future. The Lancet 398, 16191662.CrossRefGoogle ScholarPubMed
Rossi, GC, Mariluis, JC, Schnack, JA and Spinelli, GR (2002) Dípteros vectores (Culicidae y Calliphoridae) de la Provincia de Buenos Aires. Buenos Aires: Secretaría de Política Ambiental y Universidad de La Plata.Google Scholar
Rubio, A, Cardo, MV and Vezzani, D (2011) Tire-breeding mosquitoes of public health importance along an urbanization gradient in Buenos Aires, Argentina. Memórias do Instituto Oswaldo Cruz 106, 678684.CrossRefGoogle ScholarPubMed
Savage, HM, Aggarwal, D, Apperson, CS, Katholi, CR, Gordon, E, Hassan, HK, Anderson, M, Charnetzky, D, McMillen, L, Unnasch, EA and Unnasch, TR (2007) Host choice and West Nile virus infection rates in blood-fed mosquitoes, including members of the Culex pipiens complex, from Memphis and Shelby County, Tennessee, 2002–2003. Vector Borne and Zoonotic Diseases 7, 365386.CrossRefGoogle ScholarPubMed
Silva Santos, C, Roberto Pie, M, Carneiro da Rocha, T and Navarro-Silva, A (2019) Molecular identification of blood meals in mosquitoes (Diptera, Culicidae) in urban and forested habitats in southern Brazil. PLoS ONE 14, e0212517.CrossRefGoogle Scholar
Silver, JB (2008) Mosquito Ecology. Field Sampling Methods, 3rd Edn. Dordrecht: Springer.CrossRefGoogle Scholar
Sivan, A, Shriram, AN, Sunish, IP and Vidhya, PT (2015) Host-feeding pattern of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in heterogeneous landscapes of South Andaman, Andaman and Nicobar Islands, India. Parasitology Research 114, 35393546.CrossRefGoogle ScholarPubMed
Smith, JL and Fonseca, DM (2004) Rapid assays for identification of members of the Culex (Culex) pipiens complex, their hybrids and other sibling species (Diptera: Culicidae). The American Journal of Tropical Medicine and Hygiene 70, 339345.CrossRefGoogle ScholarPubMed
Taipe-Lagos, CB and Natal, D (2003) Culicidae mosquito abundance in a preserved metropolitan area and its epidemiological implications. Revista de Saúde Pública 37, 275279.CrossRefGoogle Scholar
Takken, W and Verhulst, NO (2013) Host preferences of blood-feeding mosquitoes. Annual Review of Entomology 58, 433453.CrossRefGoogle ScholarPubMed
Truett, GE, Heeger, P, Mynatt, RL, Truett, AA, Walker, JA and Warman, ML (2000) Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotechniques 29, 5254.CrossRefGoogle ScholarPubMed
UN (2014) United Nations. 2014 revision of the World Urbanization Prospects. Available at https://population.un.org/wup/default.aspxGoogle Scholar
Vazquez-Prokopec, GM, Galvin, WA, Kelly, R and Kitron, U (2009) A new, cost-effective, battery-powered aspirator for adult mosquito collections. Journal of Medical Entomology 46, 12561259.CrossRefGoogle ScholarPubMed
Vezzani, D and Eiras, D (2016) Actualización sobre Dirofilariasis en Argentina y el contexto en América. In Berón, C, Campos, RE, Gleiser, RM, Díaz Nieto, LM, Salomón, OD and Schweigmann, N (eds), Investigaciones Sobre Mosquitos de Argentina. Primera edición. Mar del Plata: Universidad Nacional de Mar del Plata, pp. 192200.Google Scholar
Vinogradova, EB (2000) Culex Pipiens Pipiens Mosquitoes: Taxonomy, Distribution, Ecology, Physiology, Genetics, Applied Importance and Control. Sofia: Pensoft Publishers.Google Scholar
Whiteman, NK, Goodman, SJ, Sinclair, BJ, Walsh, T, Cunningham, A, Kramer, LD and Parker, PG (2005) Establishment of the avian disease vector Culex quinquefasciatus Say, 1823 (Diptera: Culicidae) on the Galapagos Islands, Ecuador. Ibis: International Journal of Avian Science 147, 844847.CrossRefGoogle Scholar
Yee, DA, Bermond, C, Reyes-Torres, LJ, Fijman, NS, Scavo, NA, Nelsen, J and Yee, SH (2022) Robust network stability of mosquitoes and human pathogens of medical importance. Parasites & Vectors 15, 216.CrossRefGoogle ScholarPubMed