Abstract
Knowledge on host-feeding pattern of blood-sucking insects helps to understand the epidemiology of a vector-born disease. We determined blood meal origin from blood-fed Culicoides thanks to molecular techniques. A set of primers was used to selectively amplify segment of vertebrates' prepronociceptin gene from abdomen of engorged Culicoides (Diptera: Ceratopogonidae). Vertebrate DNA was successfully amplified in 91% of blood-fed Culicoides assayed. Direct sequencing and comparison of resultant sequences with sequences in GenBank, using BLAST, lead to the specific identification of the host in 100% of the cases. A total of 157 blood-fed females belonging to 13 different Culicoides' species were captured thanks to light traps in different areas of France between 2008 and 2009. Blood meal origin was determined for 143 blood-fed midges: 59 Culicoides obsoletus, 18 Culicoides dewulfi, 16 Culicoides scoticus, 11 Culicoides chiopterus, 10 Culicoides lupicaris, 1 Culicoides pulicaris, 8 Culicoides punctatus, 10 Culicoides pallidicornis, 3 Culicoides achrayi, 2 Culicoides furcillatus, 3 Culicoides brunnicans, 1 Culicoides picturatus and 1 Culicoides poperinghensis. The predominant species in our study belong to the C. obsoletus complex; they are considered as putative vectors of Bluetongue virus in the north of Europe. C. chiopterus sampled fed only on cattle, while blood meal origin of C. dewulfi, C. obsoletus and C. scoticus was diversified. In our sampling, we found that midges were fed mainly on cattle (54%), rabbits (20%), horses (17%), sheep (4%), pigs or wild boars (4%) and human (1%). Cattle DNA was found in at least 11 different species of Culicoides assayed.
Similar content being viewed by others
References
Augot D, Sauvage F, Jouet D, Simphal E, Veuille M, Couloux A, Kaltenbach ML, Depaquit J (2010) Discrimination of Culicoides obsoletus and Culicoides scoticus, potential bluetongue vectors, by morphometrical and mitochondrial cytochrome oxidase subunit I analysis. Infect Genet Evol 10(5):629–637. doi:10.1016/j.meegid.2010.03.016
Balczun C, Vorsprach B, Meiser CK, Schaub GA (2009) Changes of the abundance of Culicoides obsoletus s.s. and Culicoides scoticus in Southwest Germany identified by a PCR-based differentiation. Parasitol Res 105(2):345–349. doi:10.1007/s00436-009-1412-2
Baldet T, Delecolle J-C, Cetre-Sossah C, Mathieu B, Meiswinkel R, Gerbier G (2008) Indoor activity of Culicoides associated with livestock in the bluetongue virus (BTV) affected region of northern France during autumn 2006. Prev Vet Med 87(1–2):84–97. doi:10.1016/j.prevetmed.2008.06.014
Bartsch S, Bauer B, Wiemann A, Clausen PH, Steuber S (2009) Feeding patterns of biting midges of the Culicoides obsoletus and Culicoides pulicaris groups on selected farms in Brandenburg, Germany. Parasitol Res 105(2):373–380. doi:10.1007/s00436-009-1408-y
Blackwell A, Mordue AJ, Mordue W (1994) Identification of bloodmeals of the Scottish biting midge, Culicoides impunctatus, by indirect enzyme-linked immunosorbent assay (ELISA). Med Vet Entomol 8(1):20–24
Blackwell A, Brown M, Mordue W (1995) The use of an enhanced ELISA method for the identification of Culicoides bloodmeals in host-preference studies. Med Vet Entomol 9(2):214–218
Boakye DA, Tang J, Truc P, Merriweather A, Unnasch TR (1999) Identification of bloodmeals in haematophagous Diptera by cytochrome B heteroduplex analysis. Med Vet Entomol 13(3):282–287
Braverman Y, Boreham PF, Galum R (1971) The origin of blood meals of female Culicoides pallidipennis trapped in a sheepfold in Israeil. J Med Entomol 8(4):379–381
Carpenter S, Mc Arthur C et al (2008) Experimental infection studies of UK Culicoides species midges with bluetongue virus serotypes 8 and 9. Vet Rec 163:589–592
Clausen PH, Stephan A, Bartsch S, Jandowsky A, Hoffmann-Kohler P, Schein E, Mehlitz D, Bauer B (2009) Seasonal dynamics of biting midges (Diptera: Ceratopogonidae, Culicoides spp.) on dairy farms of Central Germany during the 2007/2008 epidemic of bluetongue. Parasitol Res 105(2):381–386. doi:10.1007/s00436-009-1417-x
Daba S, Daba A, Shehata MG, El Sawaf BM (2004) A simple micro-assay method for estimating blood meal size of the sand fly, Phlebotomus langeroni (Diptera: Psychodidae). J Egypt Soc Parasitol 34(1):173–182
Delécolle J-C (1985) Nouvelle contribution à l’étude systématique et iconographique des espèces du genre Culicoides (Diptera: Ceratopogonidae) du Nord-est de la France. Thèse d'Université, Université Louis Pasteur de Strasbourg, UER Sciences Vie et Terre
Dijkstra E, van der Ven IJ, Meiswinkel R, Holzel DR, Van Rijn PA (2008) Culicoides chiopterus as a potential vector of bluetongue virus in Europe. Vet Rec 162(13):422
Dyce AL (1969) The recognition of nulliparous and parous Culicoides (Diptera: Ceratopogonidae) without dissection. J Aust Entomol Soc 8:11–15
Hall TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 4:95–98
Haouas N, Pesson B, Boudabous R, Dedet JP, Babba H, Ravel C (2007) Development of a molecular tool for the identification of Leishmania reservoir hosts by blood meal analysis in the insect vectors. Am J Trop Med Hyg 77(6):1054–1059
Horbrand T, Geier M (2009) Monitoring of Culicoides at nine locations in Southern Germany (2007–2008). Parasitol Res 105(2):387–392. doi:10.1007/s00436-009-1415-z
Kent RJ, Norris DE (2005) Identification of mammalian blood meals in mosquitoes by a multiplexed polymerase chain reaction targeting cytochrome B. Am J Trop Med Hyg 73(2):336–342
Kiel E, Liebisch G, Focke R, Liebisch A, Werner D (2009) Monitoring of Culicoides at 20 locations in northwest Germany. Parasitol Res 105(2):351–357. doi:10.1007/s00436-009-1409-x
Kirstein F, Gray JS (1996) A molecular marker for the identification of the zoonotic reservoirs of Lyme borreliosis by analysis of the blood meal in its European vector Ixodes ricinus. Appl Environ Microbiol 62(11):4060–4065
Lee JH, Hassan H, Hill G, Cupp EW, Higazi TB, Mitchell CJ, Godsey MS Jr, Unnasch TR (2002) Identification of mosquito avian-derived blood meals by polymerase chain reaction-heteroduplex analysis. Am J Trop Med Hyg 66(5):599–604
Leprince DJ, Higgins JA, Church GE, Issel CJ, McManus JM, Foil LD (1989) Body size of Culicoides variipennis (Diptera: Ceratopogonidae) in relation to bloodmeal size estimates and the ingestion of Onchocerca cervicalis (Nematoda: Filarioidea) microfiliariae. J Am Mosq Control Assoc 5(1):100–103
Mehlhorn H, Walldorf V, Klimpel S, Jahn B, Jaeger F, Eschweiler J, Hoffmann B, Beer M (2007) First occurrence of Culicoides obsoletus-transmitted Bluetongue virus epidemic in Central Europe. Parasitol Res 101(1):219–228. doi:10.1007/s00436-007-0519-6
Mehlhorn H, Walldorf V, Klimpel S, Schaub G, Kiel E, Focke R, Liebisch G, Liebisch A, Werner D, Bauer C, Clausen H, Bauer B, Geier M, Horbrand T, Batza HJ, Conraths FJ, Hoffmann B, Beer M (2009) Bluetongue disease in Germany (2007–2008): monitoring of entomological aspects. Parasitol Res 105(2):313–319. doi:10.1007/s00436-009-1416-y
Meiswinkel R, van Rijn P, Leijs P, Goffredo M (2007) Potential new Culicoides vector of bluetongue virus in northern Europe. Vet Rec 161(16):564–565
Meiswinkel R, Baldet T, de Deken R, Takken W, Delecolle J-C, Mellor PS (2008) The 2006 outbreak of bluetongue in northern Europe–the entomological perspective. Prev Vet Med 87(1–2):55–63. doi:10.1016/j.prevetmed.2008.06.005
Mellor PS, Boorman J, Baylis M (2000) Culicoides biting midges: their role as arbovirus vectors. Annu Rev Entomol 45:307–340. doi:10.1146/annurev.ento.45.1.307
Morii T, Kitaoka S (1968) The laboratory colonization of Culicoides arakwae (Diptera. Ceratopogonidae). Natl Inst Anim Health Q (Tokyo) 8(1):26–30
Murphy WJ, Eizirik E, O’Brien SJ, Madsen O, Scally M, Douady CJ, Teeling E, Ryder OA, Stanhope MJ, de Jong WW, Springer MS (2001) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294(5550):2348–2351. doi:10.1126/science.1067179294/5550/2348
Nevill EM, Anderson D (1972) Host preferences of Culicoides midges (Diptera: Ceratopogonidae) in South Africa as determined by precipitin tests and light trap catches. Onderstepoort J Vet Res 39(3):147–152
Nielsen SA, Nielsen BO, Chirico J (2010) Monitoring of biting midges (Diptera: Ceratopogonidae: Culicoides Latreille) on farms in Sweden during the emergence of the 2008 epidemic of bluetongue. Parasitol Res 106(5):1197–1203. doi:10.1007/s00436-010-1791-4
Nolan DV, Carpenter S, Barber J, Mellor PS, Dallas JF, Mordue Luntz AJ, Piertney SB (2007) Rapid diagnostic PCR assays for members of the Culicoides obsoletus and Culicoides pulicaris species complexes, implicated vectors of bluetongue virus in Europe. Vet Microbiol 124(1–2):82–94. doi:10.1016/j.vetmic.2007.03.019
Townzen JS, Brower AV, Judd DD (2008) Identification of mosquito bloodmeals using mitochondrial cytochrome oxidase subunit I and cytochrome b gene sequences. Med Vet Entomol 22(4):386–393. doi:10.1111/j.1365-2915.2008.00760.x
Vanbinst T, Vandenbussche F, Vandemeulebroucke E, De Leeuw I, Deblauwe I, De Deken G, Madder M, Haubruge E, Losson B, De Clercq K (2009) Bluetongue virus detection by real-time RT-PCR in Culicoides captured during the 2006 epizootic in Belgium and development of an internal control. Transbound Emerg Dis 56(5):170–177
Vorsprach B, Meiser CK, Werner D, Balczun C, Schaub GA (2009) Monitoring of ceratopogonidae in southwest Germany. Parasitol Res 105(2):337–344. doi:10.1007/s00436-009-1411-3
Walker AR, Davies FG (1971) A preliminary survey of the epidemiology of bluetongue in Kenya. J Hyg (Lond) 69(1):47–60
Zimmer J-Y, Haubruge E, Francis F, Bortels J, Simonon G, Losson B, Mignon B, Paternostre J, De Deken R, De Deken G, Deblauwe I, Fassotte C, Cors R, Defrance T (2008) Breeding sites of bluetongue vectors in northern Europe. Vet Rec 162(4):131
Acknowledgments
We are grateful to David Hollert, Nicolas Pokorski and Cyriaque Meunier who participate in the trapping session in their own holdings, and DVM Gérard Bosquet for his help. The authors would like to thank Eric Chailloux and Nicolas Brichot, members of the ONF (Office National des Forêts), for their help on choosing trapping sites in the forests of Ardennes, Hubert, Pierre, and Agathe Ferté for capturing Culicoides in the south of France and Emilie Simphal for capturing Culicoides in the Aisne area.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ninio, C., Augot, D., Delecolle, JC. et al. Contribution to the knowledge of Culicoides (Diptera: Ceratopogonidae) host preferences in France. Parasitol Res 108, 657–663 (2011). https://doi.org/10.1007/s00436-010-2110-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-010-2110-9