Orientation behaviour of Culicoides obsoletus (Diptera: Ceratopogonidae), a relevant virus vector in northern Europe, toward host-associated odorant cues

Veterinary Parasitology

Volumn 211, Issue 3-4, 2015, Pages 274-282

  Zimmer, Jean Yves ^a   Verheggen, François J ^a   Haubruge, Eric ^a   Francis, Frédéric ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Culicoides obsoletus; Flight tunnel; Host preferences; Odours; Olfactometer; Vectors

Indexed keywords

CARBON DIOXIDE; VOLATILE ORGANIC COMPOUND;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BEHAVIORAL SCIENCE; BIOASSAY; CALF (BOVINE); CHICKEN; CONTROLLED STUDY; CULICOIDES; CULICOIDES OBSOLETUS; DISEASE CARRIER; EXHALATION; FEMALE; HOST PARASITE INTERACTION; HOST RANGE; HOST SELECTION; HUMAN; HUMAN EXPERIMENT; MALE; NONHUMAN; ODOR; SHEEP; SKIN; ANIMAL; BOVINE; CERATOPOGONIDAE; EUROPE; PHYSIOLOGY;

ARBOVIRUS; CERATOPOGONIDAE; CULICOIDES OBSOLETUS; DIPTERA; HEXAPODA; OVIS ARIES;

ANIMALS; BEHAVIOR, ANIMAL; CATTLE; CERATOPOGONIDAE; CHICKENS; EUROPE; FEMALE; HUMANS; MALE; ODORS; SHEEP;

EID: 84938289126     PISSN: 03044017     EISSN: 18732550     Source Type: Journal    
DOI: 10.1016/j.vetpar.2015.05.013     Document Type: Article

References (95)

1. Anon., New disease. In: Report of the South African cattle and sheep disease commission Report 16 1876; 189-194.
2. Atchley W.R. The Culicoides of New Mexico (Diptera: Ceratopogonidae). Univ. Kansas Sci. Bull. 1967, 46:937-1020.
3. Augot D., Sauvage F., Jouet D., Simphal E., Veuille M., Couloux A., Kaltenbach M.L., Depaquit J. Discrimination of Culicoides obsoletus and Culicoides scoticus potential bluetongue vectors, by morphometrical and mitochondrial cytochrome oxidase subunit I analysis. Infect. Genet. Evol. 2010, 10:629-637.
4. Ayllón T., Nijhof A.M., Weiher W., Bauer B., Allène X., Clausen P.H. Feeding behaviour of Culicoides spp. (Diptera: Ceratopogonidae) on cattle and sheep in northeast Germany. Parasit. Vectors 2014, 7:34. 10.1186/1756-3305-7-34.
5. Baldet T., Delécolle J.-C., Cêtre-Sossah C., Mathieu B., Meiswinkel R., Gerbier G. Indoor activity of Culicoides associated with livestock in the bluetongue virus (BTV) affected region of northern France during autumn 2006. Prev. Vet. Med. 2008, 87(1-2):84-97.
6. Bartsch S., Bauer B., Wiemann A., Clausen P.H., Steuber S. Feeding patterns of biting midges of the Culicoides obsoletus and Culicoides pulicaris groups on selected farms in Brandenburg, Germany. Parasitol. Res. 2009, 105(2):373-380. 10.1007/s00436-009-1408-y.
7. Bennett G.F. On some ornithophilic blood-sucking diptera in Algonquin Park, Ontario, Canada. Can. J. Zool. 1960, 38:377-389.
8. Bhasin A., Mordue (Luntz) A.J., Mordue W. Electrophysiological and behavioural identification of host kairomones as olfactory cues for Culicoides impunctatus and C. nubeculosus. Physiol. Entomol. 2000, 25:6-16.
9. 2 and 1-octen-3-ol in a wind tunnel. Med. Vet. Entomol. 2000, 14(3):300-307.
10. Bhasin A., Mordue (Luntz) A.J., Mordue W. Field studies on efficacy of host odour baits for the biting midge Culicoides impunctatus in Scotland. Med. Vet. Entomol. 2001, 15(2):147-156.
11. Bishop A.L., McKenzie H.J., Spohr L.J. Attraction of Culicoides brevitarsis Kieffer (Diptera: Ceratopogonidae) and Culex annulirostris Skuse (Diptera: Culicidae) to simulated visual and chemical stimuli from cattle. Aust. J. Entomol. 2008, 47:121-127.
12. Blackwell A., Mordue (Luntz) A.J., Mordue W. Identification of bloodmeals of the Scottish biting midge, Culicoides impunctatus, by indirect enzyme-linked immunosorbent assay (ELISA). Med. Vet. Entomol. 1994, 8(1):20-24.
13. Blackwell A., Dyer C., Mordue (Luntz) A.J., Wadhams L.J., Mordue W. The role of 1-octen-3-ol as a host-odour attractant for the biting midge, Culicoides impunctatus Goetghebuer, and interactions of 1-octen-3-ol with a volatile pheromone produced by parous female midges. Physiol. Entomol. 1996, 21(1):15-19.
14. Borkent, A., 2014. World Species of Biting Midges (Diptera: Ceratopogonidae),. http://wwx.inhs.illinois.edu/files/9913/9144/3328/CeratopogonidaeCatalog.pdf.
15. Bowen M.F. The sensory physiology of host-seeking behavior in mosquitoes. Annu. Rev. Entomol. 1991, 36:139-158.
16. Braverman Y., Wegis M.C., Mullens B.A. Response of Culicoides sonorensis (Diptera: Ceratopogonidae) to 1-octen-3-ol and three plant-derived repellent formulations in the field. J. Am. Mosq. Contr. 2000, 16(2):158-163.
17. Braverman Y., Rechtman S., Frish A., Braverman R. Dynamics of biting activity of C. imicola Kieffer (Diptera: Ceratopogonidae) during the year. Isr. J. Vet. Med. 2003, 58:46-56.
18. Calvo J.H., Berzal B., Calvete C., Miranda M.A., Estrada R., Lucientes J. Host feeding patterns of Culicoides species (Diptera: Ceratopogonidae) within the Picos de Europa National Park in northern Spain. Bull. Entomol. Res. 2012, 102(6):692-697. 10.1017/S0007485312000284.
19. Carpenter S., McArthur C., Selby R., Ward R., Nolan D.V., Mordue (Luntz) A.J., Dallas J.F., Tripet F., Mellor P.S. Experimental infection studies of UK Culicoides species midges with bluetongue virus serotypes 8 and 9. Vet. Rec. 2008, 163:589-592. 10.1136/vr.163.20.589.
20. Cerny O., Votypka J., Svobodova M. Spatial feeding preferences of ornithophilic mosquitoes: blackflies and biting midges. Med. Vet. Entomol. 2011, 25:104-108.
21. Cilek J.E., Kline D.L. Adult biting midge response to trap type, carbon dioxide, and an octenol/phenol mixture in northwestern Florida. J. Am. Mosq. Contr. 2002, 18(3):228-231.
22. Conraths F., Eschbaumer M., Freuling C., Gethmann J., Hoffmann B., Kramer M., Probst C., Staubach C., Beer M. Bluetongue disease: an analysis of the epidemic in Germany 2006-2009. Arthropods as Vectors of Emerging Diseases, Parasitology Research Monographs 2012, 103-135. Springer, Berlin, Heidelberg. H. Mehlhorn (Ed.).
23. De Regge N., Deblauwe I., De Deken R., Vantieghem P., Madder M., Geysen D., Smeets F., Losson B., Van den Berg T., Cay A.B. Detection of Schmallenberg virus in different Culicoides spp. by real-time RT-PCR Transbound. Emerg. Dis. 2012, 10.1111/tbed.12000.
24. Delécolle, J.-C., (Thèse d'Université) 1985. Nouvelle contribution à l'étude systématique et iconographique des espèces du genre Culicoides (Diptera: Ceratopogonidae) du Nord-Est de la France. Université Louis Pasteur de Strasbourg, UFR des Sciences de la Vie et de la Terre, Strasbourg, France, 238 pp.
25. Elbers A.R.W., Meiswinkel R., van Weezep E., Sloet van Oldruitenborgh-Oosterbaan M.M., Kooi E.A. Schmallenberg virus in Culicoides spp. biting midges, the Netherlands, 2011. Emerg. Infect. Dis. 2013, 19:106-109.
26. Fahrner J., Barthelmess C. Rearing of Culicoides nubeculosus (Diptera: Ceratopogonidae) by natural or artificial feeding in the laboratory. Vet. Parasitol. 1988, 28(4):307-313.
27. Foxi C., Delrio G. Larval habitats and seasonal abundance of Culicoides biting midges found in association with sheep in northern Sardinia Italy. Med. Vet. Entomol. 2010, 24:199-209.
28. Garros C., Gardès L., Allène X., Rakotoarivony I., Viennet E., Rossi S., Balenghien T. Adaptation of a species-specific multiplex PCR assay for the identification of bloodmeal source in Culicoides (Ceratopogonidae: Diptera): applications on Palaearctic biting midge species, vectors of Orbiviruses. Infect. Genet. Evol. 2011, 11:1103-1110.
29. Garvin M.C., Greiner E.C. Ecology of Culicoides (Diptera: Ceratopogonidae) in southcentral Florida and experimental Culicoides vectors of the avian hematozoan Haemoproteus danilewskyi Kruse. J. Wildl. Dis. 2003, 39:170-178.
30. Gibson G., Torr S.J. Visual and olfactory responses of haematophagous Diptera to host stimuli. Med. Vet. Entomol. 1999, 13:2-23.
31. Glukhova V.M., Dubrovskaia V.V. Autogenic maturation of the eggs of bloodsucking midges (Diptera: Ceratopogonidae). Parazitologiia 1972, 6(4):309-319.
32. Grant A.J., Kline D.L. Electrophysiological responses from Culicoides (Diptera: Ceratopogonidae) to stimulation with carbon dioxide. J. Med. Entomol. 2003, 40:284-293.
33. Hair J.A., Turner E.C. Preliminary host preference studies on Virginia Culicoides (Diptera: Ceratopogonidae). Mosq. News 1968, 28:103-107.
34. 2 and enantiomers of 1-octen-3-ol in the United Kingdom. J. Med. Entomol. 2012, 49(1):112-121.
35. Hendry G., Godwin G. Biting midges in Scottish forestry: a costly irritant or a trivial nuisance?. Scot. Forest 1988, 42:113-119.
36. Herder V., Wohlsein P., Peters M., Hansmann F., Baumgärtner W. Salient lesions in domestic ruminants infected with the emerging so-called Schmallenberg virus in Germany. Vet. Pathol. 2012, 49:588-591.
37. Hoffmann B., Bauer B., Bauer C., Bätza H.-J., Beer M., Clausen P.-H., Geier M., Gethmann J.M., Kiel E., Liebisch G., Liebisch A., Mehlhorn H., Schaub G.A., Werner D., Conraths F.J. Monitoring of putative vectors of bluetongue virus serotype 8, Germany. Emerg. Infect. Dis. 2009, 15(9):1481-1484.
38. Hoffmann B., Scheuch M., Höper D., Jungblut R., Holsteg M., Schirrmeier H., Eschbaumer M., Goller K.V., Wernike K., Fischer M., Breithaupt A., Mettenleiter T.C., Beer M. Novel orthobunyavirus in cattle, Europe, 2011. Emerg. Infect. Dis. 2012, 18(3):469-472. 10.3201/eid1803.111905.
39. Humphreys J.G., Turner E.C. Blood-feeding activity of female Culicoides (Diptera: Ceratopogonidae). J. Med. Entomol. 1973, 10(1):79-83.
40. Jones R.H. Mass production methods in rearing Culicoides variipennis (Coquillett). Bull. Wld. Hlth. Org 1964, 31:571-572.
41. Kettle D.S. The bionomics and control of Culicoides and Leptoconops (Diptera: Ceratopogonidae=Heleidae). Annu. Rev. Entomol. 1962, 7:401-418.
42. Kettle D.S. Biology and bionomics of bloodsucking Ceratopogonids. Annu. Rev. Entomol. 1977, 22:33-51.
43. Kline D.L., Hagan D.V., Wood J.R. Culicoides responses to 1-octen-3-ol and carbondioxide in salt marshes near Sea Island, Georgia, USA. Med. Vet. Entomol. 1994, 8(1):25-30.
44. Koch H.G., Axtell R.C. Attraction of Culicoides furens and C. hollensis (Diptera: Ceratopogonidae) to animal hosts in a salt marsh habitat. J. Med. Entomol. 1979, 15(5-6):494-499.
45. Kremer M., Lienhart E. Elevage de Culicoides nubeculosus (Diptera: Ceratopogonidae). Parasite 1998, 5(3):211-214.
46. Kremer M., Molet B., Rebholtz-Hirtzel C., Delécolle J.-C. Culicoides nubeculosus (Ceratopogonidae) feeding on engorged Aedes aegypti under laboratory conditions. Mosq. News 1974, 34(4):471-472.
47. Lacroix R., Mukabana W.R., Gouagna L.C., Koella J.C. Malaria infection increases attractiveness of humans to mosquitoes. PLoS Biol. 2005, 3:1590-1593.
48. Lassen S.B., Nielsen S.A., Skovgard H., Kristensen M. Molecular identification of bloodmeals from biting midges (Diptera: Ceratopogonidae: Culicoides Latreille) in Denmark. Parasitol. Res. 2011, 108(4):823-829.
49. Lassen S.B., Nielsen S.A., Kristensen M. Identity and diversity of blood meal hosts of biting midges (Diptera: Ceratopogonidae: Culicoides Latreille) in Denmark. Parasit. Vectors 2012, 5:143. 10.1186/1756-3305-5-143.
50. Linden A., Mousset B., Grégoire F., Hanrez D., Vandenbussche F., Vandemeulebroucke E., Vanbinst T., Verheyden B., de Clerck K. Bluetongue virus antibodies in wild red deer in southern Belgium. Vet. Rec. 2008, 162:459.
51. Logan J.G., Birkett M.A. Semiochemicals for biting fly control: their identification and exploitation. Pest. Manag. Sci. 2007, 63:647-657.
52. Lyimo I.N., Ferguson H.M. Ecological and evolutionary determinants of host species choice in mosquito vectors. Trends Parasitol. 2009, 25(4):189-196.
53. Ma Y., Xu J., Yang Z., Wang X., Lin Z., Zhao W., Wang Y., Li X., Shi H. A video clip of the biting midge Culicoides anophelis ingesting blood from an engorged Anopheles mosquito in Hainan, China. Parasit. Vectors 2013, 6:326.
54. Mands V., Kline D.L., Blackwell A. Culicoides midge trap enhancement with animal odour baits in Scotland. Med. Vet. Entomol. 2004, 18:336-342.
55. Marquardt W.C., Demaree R.S., Grieve R.B. Parasitology and Vector Biology 2000, Academic Press, San Diego, 702 pp. Second Edition.
56. Martinez-de la Puente J., Martinez J., Ferraguti M., Morales-de la Nuez A., Castro N., Figuerola J. Genetic characterization and molecular identification of the bloodmeal sources of the potential bluetongue vector Culicoides obsoletus in the Canary Islands, Spain. Parasit. Vectors 2012, 5:147. 10.1186/1756-3305-5-147.
57. Martinez-de la Puente J., Merino S., Tomas G., Moreno J., Morales J., Lobato E., Talavera S., Monteys V.S.I. Factors affecting Culicoides species composition and abundance in avian nests. Parasitology 2009, 136(9):1033-1041.
58. Mehlhorn H., Walldorf V., Klimpel S., Jahn B., Jaeger F., Eschweiler J., Hoffmann B., Beer M. First occurrence of Culicoides obsoletus-transmitted Bluetongue virus epidemic in Central Europe. Parasitol. Res. 2007, 101:219-228. 10.1007/s00436-007-0519-6.
59. 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., Hörbrand T., Bätza H.J., Conraths F.J., Hoffmann B., Beer M. Bluetongue disease in Germany (2007-2008): monitoring of entomological aspects. Parasitol. Res. 2009, 105:313-319.
60. Mellor P.S., Booman J., Baylis M. Culicoides biting midges: their role as arbovirus vectors. Annu. Rev. Entomol. 2000, 45:307-340. 10.1146/annurev.ento.45.1.307.
61. Mordue (Luntz) A.J. Arthropod semiochemicals: mosquitoes, midges and sealice. Biochem. Soc. Trans. 2003, 31:128-133.
62. Mordue (Luntz) A.J., Mordue W. Biting midge chemical ecology. Biologist 2003, 50:159-162.
63. Mullens B.A., Cardona C.J., McClellan L., Szijj C.E., Owen J.P. Culicoides bottimeri as a vector of Haemoproteus lophortyx to quail in California. U. S. A. Vet. Parasitol. 2006, 140:35-43.
64. Nelson R.L. Carbon dioxide as an attractant for Culicoides. J. Med. Entomol. 1965, 2:56-57.
65. Nielsen B.O. Some observations on biting midges (Diptera: Ceratopogonidae) attacking grazing cattle in Denmark. Ent. Scand. 1971, 2:94-98.
66. Nielsen S.A., Kristensen M. Morphological and molecular identification of species of the Obsoletus group (Diptera: Ceratopogonidae) in Scandinavia. Parasitol. Res. 2011, 109:1133-1141.
67. Ninio C., Augot D., Delécolle J.-C., Dufour B., Depaquit J. Contribution to the knowledge of Culicoides (Diptera: Ceratopogonidae) host preferences in France. Parasitol. Res. 2011, 108(3):657-663. 10.1007/s00436-010-2110-9.
68. Parker A.H. Observations on the seasonal and daily incidence of certain biting midges (Culicoides Latreille-Diptera; Ceratopogonidae) in Scotland. Trans. R. Entomol. Soc. Lond. 1949, 100:179-190.
69. Pettersson E., Bensch S., Ander M., Chirico J., Sigvald R., Ignell R. Molecular identification of bloodmeals and species composition in Culicoides biting midges. Med. Vet. Entomol. 2013, 27(1):104-112. 10.1111/j.1365-2915.2012.01038.x.
70. Ritchie S.A., Van Essen P.H.A., Kemme J.A., Kay B.H., Allaway D. Response of biting midges (Diptera: Ceratopogonidae) to carbon dioxide, octenol, and light in southeastern Queensland, Australia. J. Med. Entomol. 1994, 31:645-648.
71. Saegerman C., Berkvens D., Mellor P.S., Dal Pozzo F., Porter S., Zientara S. Fièvre catarrhale ovine: l'Europe au carrefour de l'enzootie. Point Vét. 2008, 290:41-47.
72. Schmidtmann E.T., Jones C.J., Gollands B. Comparative host-seeking attractivity of Culicoides (Diptera: Ceratopogonidae) attracted to pastured livestock in Central New York State. U. S. A. J. Med. Entomol. 1980, 17:221-231.
73. Service M.W. Light trap catches of Culicoides spp. from southern England. Bull. Entomol. Res. 1969, 59:317-322.
74. Sollai G., Solari P., Masala C., Crnjar R., Liscia A. Effects of avermectins on olfactory responses of Culicoides imicola (Diptera: Ceratopogonidae). J. Med. Entomol. 2007, 44:656-659.
75. Takken W., Verhulst N., Scholte E.J., Jacobs F., Jongema Y., van Lammeren R. The phenology and population dynamics of Culicoides spp. in different ecosystems in The Netherlands. Prev. Vet. Med. 2008, 87(1-2):41-54.
76. Tanner G.D., Turner J.E.C. Vertical activities and host preferences of several Culicoides species in a southwestern Virginia Forest. Mosq. News 1974, 34(1):66-70.
77. Thiry E., Saegerman C., Guyot H., Kirten P., Losson B., Rollin F., Bodmer M., Czaplicki G., Toussaint J.F., De Clercq K., De Dochy J.M., Dufey J., Gilleman J.L., Messeman K. Bluetongue in northern Europe. Vet. Rec. 2006, 159:327. 10.1136/vr.159.10.327.
78. Torres-Estrada J.L., Rodriguez M.H. Physic-chemical signals involved in host localization and induction of disease vector mosquito bites. Salud Publica de Mex. 2003, 45(6):497-505.
79. Van den Brom R., Luttikholt S.J., Lievaart-Peterson K., Peperkamp N.H., Mars M.H., van der Poel W.H., Vellema P. Epizootic of ovine congenital malformations associated with Schmallenberg virus infection. Tijdschr. Diergeneeskd. 2012, 137:106-111.
80. Van der Rijt R., van den Boom R., Jongema Y., van Oldruitenborgh-Oosterbaan M.M. Culicoides species attracted to horses with and without insect hypersensitivity. Vet. J. 2008, 178(1):91-97.
81. Velthuis A.G., Saatkamp H.W., Mourits M.C., de Koeijer A.A., Elbers A.R. Financial consequences of the Dutch bluetongue serotype 8 epidemics of 2006 and 2007. Prev. Vet. Med. 2010, 93(4):294-304.
82. Venter G.J., Labuschagne K., Boikanyo S.N., Majatladi D.M., Morey L. The effect of 1-octen-3-ol and 4-methylphenol on Culicoides midge numbers collected with suction light traps in South Africa. Vet. Parasitol. 2011, 175(1-2):182-186. 10.1016/j.vetpar.2010.09.010.
83. Viennet E., Garros C., Gardès L., Rakotoarivony I., Allène X., Lancelot R., Crochet D., Moulia C., Baldet T., Balenghien T. Host preferences of Palaearctic Culicoides biting midges: implications for transmission of orbiviruses. Med. Vet. Entomol. 2013, 27(3):255-266. 10.1111/j.1365-2915.2012.01042.x.
84. Viennet E., Garros C., Lancelot R., Allène X., Gardès L., Rakotoarivony I., Crochet D., Delécolle J.-C., Moulia C., Baldet T., Balenghien T. Assessment of vector/host contact: comparison of animal-baited traps and UV-light/suction trap for collecting Culicoides biting midges (Diptera: Ceratopogonidae), vectors of Orbiviruses. Parasit. Vectors 2011, 4:119. 10.1186/1756-3305-4-119.
85. Votypka J., Synek P., Svobodova M. Endophagy of biting midges attacking cavity nesting birds. Med. Vet. Entomol. 2009, 23(3):277-280.
86. Wieser-Schimpf L., Foil L.D., Holbrook F.R. Effect of carbon dioxide on the collection of adult Culicoides spp. (Diptera: Ceratopogonidae) by a new modification of black light New Jersey light traps. J. Am. Mosquito Contr. 1991, 7(3):462-466.
87. 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. Breeding sites of bluetongue vectors in northern Europe. Vet. Rec. 2008, 162(131). 10.1136/vr.162.4.131.
88. Zimmer J.-Y., Losson B., Saegerman C., Haubruge E. Ecologie et distribution des espèces de Culicoides Latreille 1809 (Diptera: Ceratopogonidae) à proximité d'une exploitation bovine en Belgique. Ann. Soc. Entomol. Fr. 2009, 45(3):393-400.
89. Zimmer J.-Y., Saegerman C., Losson B., Beckers Y., Haubruge E., Francis F. Chemical composition of silage residues sustaining the larval development of the Culicoides obsoletus/Culicoides scoticus species (Diptera: Ceratopogonidae). Vet. Parasitol. 2013, 191:197-201. 10.1016/j.vetpar.2012.08.014.
90. Zimmer J.-Y., Smeets F., Simonon G., Fagot J., Haubruge E., Francis F., Losson B. Are bogs reservoirs for emerging disease vectors? Evaluation of Culicoides populations in the Hautes Fagnes Nature Reserve (Belgium). PLoS One 2013, 8:e66893. 10.1371/journal.pone.0066893.
91. Zimmer J.-Y., Losson B., Saegerman C., Haubruge E., Francis F. Breeding sites and species association of the main Bluetongue and Schmallenberg virus vectors, the Culicoides species (Diptera: Ceratopogonidae), in northern Europe. Ann. Soc. Entomol. Fr. 2013, 49(3):335-344.
92. Zimmer J.-Y., Losson B., Saegerman C., Kirschvink N., Haubruge E., Francis F. Comparaison des populations de Culicoides Latreille 1809 (Diptera: Ceratopogonidae) présentes au sein d'une bergerie belge et d'une prairie ovine associée. Ann. Soc. Entomol. Fr. 2013, 49(4):446-459.
93. Zimmer J.-Y., Haubruge E., Francis F. Synthèse bibliographique: l'écologie larvaire des culicoïdes (Diptera: Ceratopogonidae). Biotechnol. Agron. Soc. Environ. 2014, 18(2):301-312.
94. Zimmer J.-Y., Saegerman C., Martinelle L., Losson B., Leroy P., Haubruge E., Francis F. Les porcheries: réservoirs des Culicoides (Diptera: Ceratopogonidae), vecteurs des virus de la Maladie de la Langue bleue et de Schmallenberg?. Biotechnol. Agron. Soc. Environ. 2014, 18(4):480-487.
95. Zimmer J.-Y., Brostaux Y., Haubruge E., Francis F. Larval development sites of the main Culicoides species (Diptera: Ceratopogonidae) in northern Europe and distribution of coprophilic species larvae in Belgian pastures. Vet. Parasitol. 2014, 205:676-686. 10.1016/j.vetpar.2014.08.029.