Tracing Pathogen Transmission by Mosquitoes under a Global Change Perspective: On the Role of the Identification of Mosquito Bloodmeals

Abstract

Mosquitoes play a central role in the transmission of vector‐borne pathogens causing important diseases in humans, livestock and wildlife. The identification of mosquito blood feeding preferences represents an essential step in epidemiological studies to identify the potential reservoirs and the contact rates between infective and susceptible hosts. Different methods have been used to trace mosquito bloodmeal origins in ecology and public health studies providing valuable results. These studies are specially relevant under a global change scenario, where habitat alteration and changes in the distribution of the ecological community of mosquitoes could affect the dynamics of transmission of mosquito‐borne pathogens.

Key Concepts

  • Mosquitoes play a central role in the transmission of many vector‐borne pathogens.
  • Environmental conditions determine the mosquito community structure in the area, potentially affecting the dynamics of transmission of vector‐borne pathogens.
  • Female mosquitoes feed on blood to obtain resources for egg development.
  • The bloodmeals of mosquitoes provide a valuable source of genetic material allowing the identification of vertebrate species origin even to the level of individuals host and the pathogens interacting with them.
  • Integrating information on the feeding patterns of mosquitoes into epidemiological models contributes to identifying the risk of transmission of vector‐borne pathogens to human and other animals.

Keywords: Aedes; Culex; blood‐sucking insects; Flavivirus; humans; vector‐borne pathogens; West Nile virus

Figure 1. Aedes female mosquito biting on a human hand. Aedes mosquitoes are important vectors of pathogens affecting people including Dengue virus, Chikungunya virus and Zika virus.
Figure 2. Recently engorged female mosquitoes of the species Ochlerotatus (Aedes) caspius resting after biting on a vertebrate host.
Figure 3. Success of host identification of mosquito females according to the Sella stage of bloodmeal digestion status and the method of DNA isolation (black columns: QIAGEN DNeasy Blood and Tissue®, grey colums: HotSHOT procedure). Source: Data from Martínez‐de la Puente et al. .
Figure 4. Percentage of mosquito bloodmeals derived from humans (black), horses (green), other mammals (blue), reptiles (grey) and birds (red) for the six most common mosquito species sampled in southern Spain. Sample sizes are shown above bars. Source: Data from Alcaide et al. ; Muñoz et al. ; Roiz et al. ; Martínez‐de la Puente et al. , , .
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References

Alcaide M, Rico C, Ruiz S, et al. (2009) Disentangling Vector‐borne transmission networks: a universal DNA barcoding method to identify vertebrate hosts from arthropod bloodmeals. PLoS One 4: e7092.

Bahuon C, Lecollinet S and Beck C (2015) West Nile virus infection. In: eLS. Chichester: John Wiley & Sons Ltd. DOI: 10.1002/9780470015902.a0023274.

Bannister LH and Sherman IW (2013) Malaria. In: eLS. Chichester: John Wiley & Sons Ltd. DOI: 10.1002/9780470015902.a0001927.pub2.

Barbazan P, Thitithanyanont A, Missé D, et al. (2008) Detection of H5N1 avian influenza virus from mosquitoes collected in an infected poultry farm in Thailand. Vector‐Borne and Zoonotic Diseases 8: 105–109.

Beerntsen BT, James AA and Christensen BM (2000) Genetics of mosquito vector competence. Microbiology and Molecular Biology Reviews 64: 115–137.

Bitome‐Essono P‐Y, Ollomo B, Arnathau C, et al. (2017) Tracking zoonotic pathogens using blood‐sucking flies as ‘flying syringes’. eLife 6: e22069.

Börstler J, Jöst H, Garms R, et al. (2016) Host‐feeding patterns of mosquito species in Germany. Parasites & Vectors 9: 318.

Brugman VA, Hernández‐Triana LM, Prosser SWJ, et al. (2015) Molecular species identification, host preference and detection of myxoma virus in the Anopheles maculipennis complex (Diptera: Culicidae) in southern England, UK. Parasites & Vectors 8: 421.

Brugman VA, Hernández‐Triana LM, England, ME et al. (2017) Blood‐feeding patterns of native mosquitoes and insights into their potential role as pathogen vectors in the Thames estuary region of the United Kingdom. Parasites & Vectors 10:163.

Burkett‐Cadena ND, Bingham AM and Unnasch TR (2014) Sex‐biased avian host use by arbovirus vectors. Royal Society Open Science 1: 140262.

Cancrini G, Frangipane di Regalbono A, Ricci I, et al. (2003) Aedes albopictus is a natural vector of Dirofilaria immitis in Italy. Veterinary Parasitology 118: 195–202.

Detinova TS (1962) Age‐grouping Methods in Diptera of Medical Importance: With Special Reference to Some Vectors of Malaria, Vol. 47. Geneva: World Health Organization.

Egizi A, Healy SP and Fonseca DM (2013) Rapid blood meal scoring in anthropophilic Aedes albopictus and application of PCR blocking to avoid pseudogenes. Infection, Genetics and Evolution 16: 122–128.

Elizondo‐Quiroga A, Flores‐Suarez A, Elizondo‐Quiroga D, et al. (2006) Gonotrophic cycle and survivorship of Culex quinquefasciatus (Diptera: Culicidae) using sticky ovitraps in Monterrey, northeastern Mexico. Journal of the American Mosquito Control Association 22: 10–14.

Faraji A, Egizi A, Fonseca DM, et al. (2014) Comparative host feeding patterns of the Asian tiger mosquito, Aedes albopictus, in urban and suburban Northeastern USA and implications for disease transmission. PLoS Neglected Tropical Disease 8: e3037.

Ferraguti M, Martínez‐de la Puente J, Roiz D, et al. (2016) Effects of landscape anthropization on mosquito community composition and abundance. Scientific Reports 6: 29002.

Grubaugh ND, Sharma S, Krajacich BJ, et al. (2015) Xenosurveillance: a novel mosquito‐based approach for examining the human‐pathogen landscape. PLoS Neglected Tropical Diseases 9: e0003628.

Gutiérrez‐López R, Martínez‐de la Puente J, Gangoso L, et al. (2016) Do mosquitoes transmit the avian malaria–like parasite Haemoproteus? An experimental test of vector competence using mosquito saliva. Parasites & Vectors 9: 609.

Hadj‐Henni L, De Meulemeester T, Depaquit J, et al. (2015) Comparison of vertebrate cytochrome b and prepronociceptin for blood meal analyses in Culicoides. Frontiers in Veterinary Science 2: 15.

Harper DR, Litaker J and Logan J (2018) Zika virus. In: eLS. Chichester: John Wiley & Sons Ltd. DOI: 10.1002/9780470015902.a0026916.

Hebert PD, Cywinska A, Ball SL, et al. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London B: Biological Sciences 270: 313–321.

Hernández‐Triana LM, Brugman VA, Prosser SWJ, et al. (2017) Molecular approaches for blood meal analysis and species identification of mosquitoes (Insecta: Diptera: Culicidae) in rural locations in southern England, United Kingdom. Zootaxa 4250: 67–76.

Hess A, Hayes RO and Tempelis C (1968) The use of the forage ratio technique in mosquito host preference studies. Mosquito News 28: 386–389.

Jones KE, Patel NG, Levy MA, et al. (2008) Global trends in emerging infectious diseases. Nature 451: 990–994.

Kent RJ and Norris DE (2005) Identification of mammalian bloodmeals in mosquitoes by a multiplexed polymerase chain reaction targeting cytochrome b. The American Journal of Tropical Medicine and Hygiene 73: 336–342.

Kent RJ (2009) Molecular methods for arthropod bloodmeal identification and applications to ecological and vector‐borne disease studies. Molecular Ecology Resources 9: 4–18.

Kilpatrick AM, Kramer LD, Campbell SR, et al. (2005) West Nile virus risk assessment and the bridge vector paradigm. Emerging Infectious Diseases 11: 425–429.

Kilpatrick AM, Kramer LD, Jones MJ, et al. (2006) West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior. PLoS Biology 4: e82.

Kraemer MU, Sinka ME, Duda KA, et al. (2015) The global distribution of the arbovirus vectors Aedes aegypti and Ae. albopictus. eLife 4: e08347.

Kurucz MV, Savage HM, Lopatina JV, et al. (2006) Evaluation of potential West Nile virus vectors in Volgograd region, Russia, 2003 (Diptera: Culicidae): species composition, bloodmeal host utilization, and virus infection rates of mosquitoes. Journal of Medical Entomology 43: 552–563.

Kurucz K, Kepner A, Krtinic B, et al. (2018) Blood‐meal analysis and avian malaria screening of mosquitoes collected from human‐inhabited areas in Hungary and Serbia. Journal of the European Mosquito Control Association 36: 3–13.

La Ruche G, Souarès Y, Armengaud A, et al. (2010) First two autochthonous dengue virus infections in metropolitan France, September 2010. Eurosurveillance 15: 19676.

Lloyd‐Smith JO, Schreiber SJ, Kopp PE, et al. (2005) Superspreading and the effect of individual variation on disease emergence. Nature 438: 355–359.

Lowe SJ, Browne M and Boudjelas S (2000) 100 of the World's Worst Invasive Alien Species. Auckland: IUCN/SSC Invasive Species Specialist Group (ISSG).

Manguin S and Boëte C (2011) Global impact of mosquito biodiversity, human vector–borne diseases and environmental change. In: López JP (ed) The Importance of Biological Interactions in the Study of Biodiversity, pp. 27–50. InTech Publisher.

Martínez‐de la Puente J, Ruiz S, Soriguer R, et al. (2013) Effect of blood meal digestion and DNA extraction protocol on the success of blood meal source determination in the malaria vector Anopheles atroparvus. Malaria Journal 12: 109.

Martínez‐de la Puente J, Mendez M, Ruiz S, et al. (2015a) Individual identification of endangered species using mosquito blood meals: a proof‐of‐concept study in Iberian lynx. Parasitology Research 114: 1607–1610.

Martínez‐de la Puente J, Muñoz J, Capelli G, et al. (2015b) Avian malaria parasites in the last supper: identifying encounters between parasites and the invasive Asian mosquito tiger and native mosquito species in Italy. Malaria Journal 14: 32.

Martínez‐de la Puente J, Ferraguti M, Ruiz S, et al. (2016) Culex pipiens forms and urbanization: effects on blood feeding sources and transmission of avian Plasmodium. Malaria Journal 15: 589.

Martínez‐de la Puente J, Ferraguti M, Ruiz S, et al. (2018) Mosquito community influences West Nile virus seroprevalence in wild birds: implications for the risk of spillover into human populations. Scientific Reports 8: 2599.

Medlock JM, Hansford KM, Schaffner F, et al. (2012) A review of the invasive mosquitoes in Europe: ecology, public health risks, and control options. Vector Borne Zoonotic Disease 12 (6): 435–447.

Millet J‐P, Montalvo T, Bueno‐Marí R, et al. (2017) Imported Zika virus in a European city: how to prevent local transmission? Frontiers in Microbiology 8: 1319.

Muñoz J, Ruiz S, Soriguer R, et al. (2012) Feeding patterns of potential West Nile virus vectors in South‐West Spain. PLoS One 7: e39549.

Mwangangi JM, Mbogo CM, Nzovu JC, et al. (2003) Blood‐meal analysis for anopheline mosquitoes sampled along the Kenyan coast. Journal of the American Mosquito Control Association 19: 371–375.

Niare S, Berenger JM, Dieme C, et al. (2016) Identification of blood meal sources in the main African malaria mosquito vector by MALDI‐TOF MS. Malaria Journal 15: 87.

Niare S, Tandina F, Davoust B, et al. (2017) Accurate Identification of Anopheles gambiae Giles Trophic Preferences by MALDI‐TOF MS. Genetics and Evolution: Infection, in press.

Ngo KA and Kramer LD (2003) Identification of mosquito bloodmeals using polymerase chain reaction (PCR) with order‐specific primers. Journal of Medical Entomology 40: 215–222.

Osório HC, Zé‐Zé L and Alves MJ (2012) Host‐feeding patterns of Culex pipiens and other potential mosquito vectors (Diptera: Culicidae) of West Nile virus (Flaviviridae) collected in Portugal. Journal of Medical Entomology 49: 717–721.

Rezza G, Nicoletti L, Angelini R, et al. (2007) Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet 370: 1840–1846.

Rizzoli A, Bolzoni L, Chadwick EA, et al. (2015) Understanding West Nile virus ecology in Europe: Culex pipiens host feeding preference in a hotspot of virus emergence. Parasites & Vectors 8: 213.

Roche B, Rohani P, Dobson AP, et al. (2013) The impact of community organization on vector–borne pathogens. The American Naturalist 181: 1–11.

Roiz D, Roussel M, Muñoz J, et al. (2012) Efficacy of mosquito traps for collecting potential West Nile mosquito vectors in a natural Mediterranean wetland. The American Journal of Tropical Medicine and Hygiene 86 (4): 642–648.

Schmidt‐Chanasit J, Haditsch M, Schoneberg I, et al. (2010) Dengue virus infection in a traveller returning from Croatia to Germany. EuroSurveillance 15: 19677.

Scott TW, Githeko AK, Fleisher A, et al. (2006) DNA profiling of human blood in anophelines from lowland and highland sites in western Kenya. American Journal of Tropical Medicine and Hygiene 75: 231–237.

Smith DL, Battle KE, Hay SI, et al. (2012) Ross, Macdonald, and a theory for the dynamics and control of mosquito‐transmitted pathogens. PLoS Pathogens 8: e1002588.

Takken W and Verhulst NO (2013) Host preferences of blood‐feeding mosquitoes. Annual Review of Entomology 58: 433–453.

Tolle MA (2009) Mosquito‐borne diseases. Current Problems in Pediatric and Adolescent Health Care 39: 97–140.

Valkiūnas G (2011) Haemosporidian vector research: marriage of molecular and microscopical approaches is essential. Molecular Ecology 20: 3084–3086.

VanderWaal KL and Ezenwa VO (2016) Heterogeneity in pathogen transmission: mechanisms and methodology. Functional Ecology 30: 1606–1622.

Yan J, Gangoso L, Martínez‐de la Puente J, et al. (2017) Avian phenotypic traits related to feeding preferences in two Culex mosquitoes. The Science of Nature 104: 76.

Yan J, Martínez‐de la Puente J, Gangoso L, et al. (2018) Avian malaria infection intensity influences mosquito feeding patterns. International Journal for Parasitology 48: 257–264.

Ventim R, Ramos JA, Osório H, et al. (2012) Avian malaria infections in western European mosquitoes. Parasitology Research 111: 637–645.

Woolhouse ME, Dye C, Etard JF, et al. (1997) Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proceedings of the National Academy of Sciences 94: 338–342.

Further Reading

Gómez‐Díaz E and Figuerola J (2010) New perspectives in tracing vector‐borne interaction networks. Trends in Parasitology 26: 470–476.

Lehane MJ (2005) The Biology of Blood‐sucking in Insects. Cambridge, UK: Cambridge University Press.

Martínez‐de la Puente J, Figuerola J and Soriguer R (2015) Fur or feather? Feeding preferences of species of Culicoides biting midges in Europe. Trends in Parasitology 31: 16–22.

Merino S, Puente J (2010). Reproductive strategies of the malaria parasite. In eLS, John Wiley & Sons Ltd, Chichester. doi:10.1002/9780470015902.a0022860

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la Puente, Josué Martínez‐de, Ferraguti, Martina, Ruiz, Santiago, Montalvo, Tomás, Casimiro Soriguer, Ramón, and Figuerola, Jordi(Sep 2018) Tracing Pathogen Transmission by Mosquitoes under a Global Change Perspective: On the Role of the Identification of Mosquito Bloodmeals. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028179]