Understanding West Nile virus ecology in Europe: Culex pipiens host feeding preference in a hotspot of virus emergence

Parasites and Vectors

Volumn 8, Issue 1, 2015, Pages

  Rizzoli, Annapaola ^a   Bolzoni, Luca ^a,b   Chadwick, Elizabeth A ^c   Capelli, Gioia ^d   Montarsi, Fabrizio ^d   Grisenti, Michela ^a,e   De La Puente, Josue Martínez ^f   Muñoz, Joaquin ^f   Figuerola, Jordi ^f   Soriguer, Ramon ^f   Anfora, Gianfranco ^a   Di Luca, Marco ^g   Rosà, Roberto ^a  

^a RESEARCH AND INNOVATION CENTRE   (Italy)

^b ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLA LOMBARDIA E DELL EMILIA ROMAGNA   (Italy)

^c CARDIFF UNIVERSITY   (United Kingdom)

^d ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLE VENEZIE   (Italy)

^e UNIVERSITY OF TURIN   (Italy)

^f DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

^g ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Behavioural bioassay; Blood meal analysis; Culex pipiens; Feeding preference; Mosquito host selection; Multinomial simulations; Pica pica; Reservoir host; Turdus merula

Indexed keywords

ARTICLE; BARN SWALLOW; BIRD; BLACKBIRD; COLUMBA LIVIA; CULEX PIPIENS; DELICHON URBICUM; DISEASE CARRIER; FEEDING BEHAVIOR; FEEDING PREFERENCE; HOST PARASITE INTERACTION; ITALY; NONHUMAN; PASSER DOMESTICUS; PICA PICA; STREPTOPELIA DECAOCTO; STURNUS VULGARIS; WEST NILE VIRUS; ANIMAL; BLOOD; CULEX; GENETICS; ISOLATION AND PURIFICATION; PHYSIOLOGY; SPECIES DIFFERENCE; VIROLOGY; WEST NILE FEVER;

ARBOVIRUS; AVES; CORVIDAE; CULEX PIPIENS; PASSER DOMESTICUS; PICA PICA; TURDUS MERULA; VERTEBRATA; WEST NILE VIRUS;

DNA; FRAGRANCE;

ANIMALS; BIRDS; CULEX; DISEASE RESERVOIRS; DNA; FEEDING BEHAVIOR; ODORANTS; SPECIES SPECIFICITY; WEST NILE FEVER; WEST NILE VIRUS;

EID: 84928568371     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/s13071-015-0831-4     Document Type: Article

References (69)

1. Cutler SJ, Fooks AR, van der Poel WH. Public health threat of new, reemerging, and neglected zoonoses in the industrialized world. Emerg Infect Dis. 2010;16:1-7.
2. Weaver SC, Reisen WK. Present and future arboviral threats. Antivir Res. 2010;85:328-45.
3. Simpson JE, Hurtado PJ, Medlock J, Molaei G, Andreadis TG, Galvani AP, et al. Vector host-feeding preferences drive transmission of multi-host pathogens: West Nile virus as a model system. P Roy Soc B-Biol Sci. 2012;279:925-33.
4. Kilpatrick AM. Globalization, land use, and the invasion of West Nile virus. Science. 2011;334:323-7.
5. Reisen WK. The ecology of West Nile virus in North America. Viruses. 2013;5:2079-105.
6. Marcantonio M, Rizzoli A, Metz M, Rosà R, Marini G, Chadwick EA, et al. Identifying the Environmental Conditions Favouring West Nile Virus Outbreaks in Europe. PLoS ONE. 2015;10:e0121158.
7. Rosà R, Marini G, Bolzoni L, Neteler M, Metz M, Delucchi L, et al. Early warning of West Nile virus mosquito vector: climate and land use models successfully explain phenology and abundance of Culex pipiens mosquitoes in north-western Italy. Parasites Vectors. 2014;7:269.
8. Mackenzie JS, Gubler DJ, Petersen LR. Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat Med. 2004;10:S98-109.
9. Hay SI, Okiro EA, Gething PW, Patil AP, Tatem AJ, Guerra CA, et al. Estimating the Global Clinical Burden of Plasmodium falciparum Malaria in 2007. PLoS Med. 2010;7:e1000290.
10. Ross R. The prevention of malaria. 2nd ed. J. Murray, London, UK; 1911.
11. Macdonald G. The analysis of equilibrium in malaria. Trop Dis Bull. 1952;49:813-29.
12. Reiner Jr RC, Perkins TA, Barker CM, Niu T, Chaves LF, Ellis AM, et al. Systematic review of mathematical models of mosquito-borne pathogen transmission: 1970-2010. J R Soc Interface. 2013;10:20120921.
13. Smith DL, Perkins TA, Reiner Jr RC, Barker CM, Niu T, Chaves LF, et al. Recasting the theory of mosquito-borne pathogen transmission dynamics and control. Trans R Soc Trop Med Hyg. 2014;108:185-97.
14. Kilpatrick AM, Daszak P, Jones MJ, Marra PP, Kramer LD. Host heterogeneity dominates West Nile virus transmission. P Roy Soc B-Biol Sci. 2006;273:2327-33.
15. Burkett-Cadena ND, Graham SP, Hassan HK, Guyer C, Eubanks MD, Katholi CR, et al. Blood feeding patterns of potential arbovirus vectors of the genus Culex targeting ectothermic hosts. Am J Trop Med Hyg. 2008;79:809-15.
16. Farajollahi A, Fonseca DM, Kramer LD, Kilpatrick AM. "Bird biting" mosquitoes and human disease: A review of the role of Culex pipiens complex mosquitoes in epidemiology. Infect Genet Evol. 2011;11:1577-85.
17. Kilpatrick AM, Kramer LD, Jones MJ, Marra PP, Daszak P. West Nile virus epidemics in North America are driven by shifts in mosquito feeding behavior. PLoS Biol. 2006;4:e82.
18. Hamer GL, Chaves LF, Anderson TK, Kitron UD, Brawn JD, Ruiz MO, et al. Fine-Scale Variation in Vector Host Use and Force of Infection Drive Localized Patterns of West Nile Virus Transmission. PLoS One. 2011;6:e23767.
19. Thiemann TC, Lemenager DA, Kluh S, Carroll BD, Lothrop HD, Reisen WK. Spatial variation in host feeding patterns of Culex tarsalis and the Culex pipiens complex (Diptera: Culicidae) in California. J Med Entomol. 2012;49:903-16.
20. Takken W, Verhulst NO. Host preferences of blood-feeding mosquitoes. Annu Rev Entomol. 2013;58:433.
21. Burkett-Cadena ND, Hassan HK, Eubanks MD, Cupp EW, Unnsach TR. Winter severity predicts the timing of host shifts in the mosquito Culex erraticus. Biol Lett. 2012;8:567-9.
22. Janousek WM, Marra PP, Kilpatrick AM. Avian roosting behaviour influences vector-host interactions for West Nile virus hosts. Parasit Vector. 2014;7:399.
23. Carver S, Bestall A, Jardine A, Ostfeld RS. Influence of Hosts on the Ecology of Arboviral Transmission: Potential Mechanisms Influencing Dengue, Murray Valley Encephalitis, and Ross River Virus in Australia. Vector-Borne Zoonot. 2009;9:51-64.
24. Hassan HK, Cupp EW, Hill GE, Katholi CR, Klingler K, Unnasch TR. Avian host preference by vectors of eastern equine encephalomyelitis virus. Am J Trop Med Hyg. 2003;69:641-7.
25. Lefèvre T, Gouagna LC, Dabire KR, Elguero E, Fontenille D, Costantini C, et al. Evolutionary lability of odour-mediated host preference by the malaria vector Anopheles gambiae. Trop Med Int Health. 2009;14:228-36.
26. Smithburn KC, Hughes TP, Burke AW, Paul JH. A neurotropic virus isolated from the blood of a native of Uganda. Am J Trop Med Hyg. 1940;20:471-92.
27. Zeller HG, Schuffenecker I. West Nile Virus: An overview of its spread in Europe and the Mediterranean basin in contrast to its spread in the Americas. Eur J Clin Microbiol. 2004;23:147-56.
28. Radrova J, Seblova V, Votypka J. Feeding behavior and spatial distribution of Culex mosquitoes (Diptera: Culicidae) in wetland areas of the Czech Republic. J Med Entomol. 2013;50:1097-104.
29. Munoz J, Ruiz S, Soriguer R, Alcaide M, Viana DS, Roiz D, et al. Feeding Patterns of Potential West Nile Virus Vectors in South-West Spain. PLoS One. 2012;7:e39549.
30. Roiz D, Vazquez A, Rosà R, Munoz J, Arnoldi D, Rosso F, et al. Blood meal analysis, flavivirus screening, and influence of meteorological variables on the dynamics of potential mosquito vectors of West Nile virus in northern Italy. J Vector Ecol. 2012;37:1-9.
31. Gomes B, Sousa CA, Vicente JL. Feeding patterns of molestus and pipiens forms of Culex pipiens (Diptera: Culicidae) in a region of high hybridization. Parasit Vector. 2013;6:93.
32. Valinsky L, Ettinger G, Bar-Gal GK, Orshan L. Molecular identification of bloodmeals from sand flies and mosquitoes collected in Israel. J Med Entomol. 2014;51:678-85.
33. Engler O, Savini G, Papa A, Figuerola J, Groschup MH, Kampen H, et al. European surveillance for West Nile virus in mosquito populations. Int J Environ Res Public Health. 2013;10:4869-95.
34. Calzolari M, Monaco F, Montarsi F, Bonilauri P, Ravagnan S, Bellini R, et al. New incursions of West Nile virus lineage 2 in Italy in 2013: the value of the entomological surveillance as early warning system. Veter Ital. 2013;49:315-9.
35. Mulatti P, Bonfanti L, Capelli G, Capello K, Lorenzetto M, Terregino C, et al. West Nile virus in north-eastern Italy, 2011: entomological and equine IgM-based surveillance to detect active virus circulation. Zoonoses Public Health. 2013;60:375-82.
36. Busani L, Capelli G, Cecchinato M, Lorenzetto M, Savini G, Terregino C, et al. West Nile virus circulation in Veneto region in 2008-2009. Epidemiol Infect. 2011;139:818-25.
37. Barzon L, Pacenti M, Franchin E, Squarzon L, Lavezzo E, Cattai M, et al. The Complex Epidemiological Scenario of West Nile Virus in Italy. Int J Environ Res Public Health. 2013;10:4669-89.
38. Gobbi F, Capelli G, Angheben A, Giobbia M, Conforto M, Franzetti M, et al. Summer Fever Study Group. Human and entomological surveillance of West Nile fever, dengue and chikungunya in Veneto region, Italy, 2010-2012. BMC Infect Dis. 2014;4:60.
39. Severini F, Toma L, Di Luca M, Romi R. Le zanzare italiane: generalità e identificazione degli adulti (Diptera, Culicidae) (in italian). Fragmenta Entomologica. 2009;41:213-372.
40. Martínez-De La Puente J, Ruiz S, Soriguer R, Figuerola J. Effect of blood meal digestion and DNA extraction protocol on the success of blood meal source determination in the malaria vector Anopheles atroparvus. Malar J. 2013;12:109.
41. Alcaide M, Rico C, Ruiz S, Soriguer R, Munoz J, Figuerola J. Disentangling Vector-Borne Transmission Networks: A Universal DNA Barcoding Method to Identify Vertebrate Hosts from Arthropod Bloodmeals. PLoS One. 2009;4:e7092.
42. Snow B, Snow D. Bird and berries. Calton: Poyser; 1988.
43. Berthold P. Bird migration: a General Survey. Oxford University Press; 2001
44. Snow DW, Perrins CM. The Birds of the Western Palaearctic. Conciseth ed. Oxford, UK: Oxford University Press; 1998.
45. Campagna S, Mardon J, Celerier A, Bonadonna F. Potential Semiochemical Molecules from Birds: A Practical and Comprehensive Compilation of the Last 20 Years Studies. Chem Senses. 2012;37:3-25.
46. Whittaker DJ, Gerlach NM, Soini HA, Novotny MV, Ketterson ED. Bird odour predicts reproductive success. Anim Behav. 2013;86:697-703.
47. Syed Z, Leal WS. Acute olfactory response of Culex mosquitoes to a human- and bird-derived attractant. Proc Natl Acad Sci. 2009;106:18803-8.
48. Anfora G, Tasin M, De Cristofaro A, Ioriatti C, Lucchi A. Synthetic grape volatiles attract mated Lobesia botrana females in laboratory and field bioassays. J Chem Ecol. 2009;35:1054-62.
49. Montarsi F, Mazzon L, Cazzin S, Ciocchetta S, Capelli G. Seasonal and daily activity patterns of mosquito (Diptera: Culicidae) vectors of pathogens in Northeastern Italy. J Med Entomol. 2015;52:56-62.
50. Balenghien T, Fouque F, Sabatier P, Bicout DJ. Horse-, bird-, and human-seeking behavior and seasonal abundance of mosquitoes in a West Nile virus focus of southern France. J Med Entomol. 2006;43:936-46.
51. Reddy MR, Lepore TJ, Pollack RJ, Kiszewski AE, Spielman A, Reiter P. Early evening questing and oviposition activity by the Culex (Diptera: Culicidae) vectors of west nile virus in Northeastern North America. J Med Entomol. 2007;44:211-4.
52. Ryan TA. Significance tests for multiple comparison of proportions, variances, and other statistics. Psychol Bull. 1960;57:18-328.
53. Thiemann TC, Reisen WK. Evaluating sampling method bias in Culex tarsalis and Culex quinquefasciatus (Diptera: Culicidae) bloodmeal identification studies. J Med Entomol. 2012;49:143-9.
54. Roiz D, Roussel M, Munoz J, Ruiz S, Soriguer R, Figuerola J. Efficacy of mosquito traps for collecting potential West Nile mosquito vectors in a natural Mediterranean wetland. Am J Trop Med Hyg. 2012;86:642-8.
55. Lundstrom JO, Lindstrom KM, Olsen B, Dufva R, Krakower DS. Prevalence of Sindbis virus neutralizing antibodies among Swedish passerines indicates that thrushes are the main amplifying hosts. J Med Entomol. 2001;38:289-97.
56. Turner AK, Rose C. Swallows and Martins of the world. London: Christopher Helm; 1989.
57. Gray KM, Burkett-Cadena ND, Eubanks MD, Unnasch TR. Crepuscular Flight Activity of Culex erraticus (Diptera: Culicidae). J Med Entomol. 2011;48:167-72.
58. Georgiev K, Iliev M. Numbers and Arrival Dynamics of Communally Roosting Magpies (Pica Pica) in the Dendrological Park of the University of Forestry - Sofia, Bulgaria. Biotechnol Biotec Eq. 2009;23:250-3.
59. Cramp S. The birds of the Western Palearctic. Vol. 5: Tyrant flycatchers to thrushes. Oxford, UK: Oxford Univ Press; 1988. p. 949-64.
60. European Centre for Disease Prevention and Control: Annual Epidemiological Report; 2013. pp. 155. http://www.ecdc.europa.eu/en/publications/-layouts/forms/Publication-DispForm.aspx?List=4f55ad51-4aed-4d32-b960-af70113dbb90&ID=989
61. Epidemiological Bulletins of the Istituto G. Caporale Teramo. West Nile disease in Italy; 2008-2014. http://sorveglianza.izs.it/emergenze/west-nile/emergenze.html
62. Buckley A, Dawson A, Moss SR, Hinsley SA, Bellamy PE, Gould EA. Serological evidence of West Nile virus, Usutu virus and Sindbis virus infection of birds in the UK. J Gen Virol. 2003;84:2807-17.
63. Balança G, Gaidet N, Savini G, Vollot B, Foucart A, Reiter P, et al. Low West Nile virus circulation in wild birds in an area of recurring outbreaks in Southern France. Vector-Borne Zoonot. 2009;9:737-41.
64. Lelli R, Calistri P, Bruno R, Monaco F, Savini G, Di Sabatino D, et al. West Nile transmission in resident birds in Italy. Transbound Emerg Dis. 2012;59:421-8.
65. López G, Jimenez-Clavero MA, Tejedor CG, Soriguer R, Figuerola J. Prevalence of West Nile virus neutralizing antibodies in Spain is related to the behavior of migratory birds. Vector-Borne Zoonot. 2008;8:615-21.
66. Valiakos G, Touloudi A, Athanasiou LV, Giannakopoulos A, Iacovakis C, Birtsas P, et al. Serological and molecular investigation into the role of wild birds in the epidemiology of West Nile virus in Greece. Virol J. 2012;9:266.
67. Del Amo J, Llorente F, Figuerola J, Soriguer R, Moreno AM, Cordioli P, et al. Experimental infection of house sparrows (Passer domesticus) with West Nile virus isolates of Euro-Mediterranean and North American origins. Vet Res. 2014;45:33.
68. Perez-Ramirez E, Llorente F, Jimenez-Clavero MA. Experimental Infections of Wild Birds with West Nile Virus. Viruses. 2014;6:752-81.
69. Komar N, Langevin S, Hinten S, Nemeth N, Edwards E, Hettler D, et al. Experimental infection of north American birds with the New York 1999 strain of West Nile virus. Emerg Infect Dis. 2003;9:311-22.