Seasonal dynamics of Culicoides (Diptera: Ceratopogonidae) biting midges, potential vectors of African horse sickness and bluetongue viruses in the Niayes area of Senegal

Particle and Fibre Toxicology

Hélène Guis¹  Jérémy Bouyer¹  Massouka Ndao³  Ange Michel Dosum³  Mame Thierno Bakhoum³  Iba Mall³  Renaud Lancelot¹  Ignace Rakotoarivony¹  Xavier Allène¹  Thomas Balenghien¹  Claire Garros¹  Momar Talla Seck³  Aliou Diop²  Assane G Fall³  Moussa Fall⁴  Maryam Diarra² 

[1] INRA, UMR1309 CMAEE, F-34398 Montpellier, France;Université Gaston Berger, Laboratoire d’Etudes et de Recherches en Statistiques et Développement, Saint-Louis, Sénégal;Institut Sénégalais de Recherches Agricoles, Laboratoire National de l’Elevage et de Recherches Vétérinaires, Dakar, Sénégal;Faculté des Sciences et Techniques, Département de Biologie Animale, Université Cheikh Anta Diop, Dakar, Sénégal

关键词: Equids;    Orbivirus;    Arbovirus;    Africa;    Culicoides imicola;    Culicoides oxystoma;    Light traps;    Spatial and temporal dynamics;    Insect vectors;    Vector-borne disease;   

Others  :  822783
DOI  :  10.1186/1756-3305-7-147

 received in 2013-12-26, accepted in 2014-03-11,  发布年份 2014

【 摘 要 】

Background

The African horse sickness epizootic in Senegal in 2007 caused considerable mortality in the equine population and hence major economic losses. The vectors involved in the transmission of this arbovirus have never been studied specifically in Senegal. This first study of the spatial and temporal dynamics of the Culicoides (Diptera: Ceratopogonidae) species, potential vectors of African horse sickness in Senegal, was conducted at five sites (Mbao, Parc Hann, Niague, Pout and Thies) in the Niayes area, which was affected by the outbreak.

Methods

Two Onderstepoort light traps were used at each site for three nights of consecutive collection per month over one year to measure the apparent abundance of the Culicoides midges.

Results

In total, 224,665 specimens belonging to at least 24 different species (distributed among 11 groups of species) of the Culicoides genus were captured in 354 individual collections. Culicoides oxystoma, Culicoides kingi, Culicoides imicola, Culicoides enderleini and Culicoides nivosus were the most abundant and most frequent species at the collection sites. Peaks of abundance coincide with the rainy season in September and October.

Conclusions

In addition to C. imicola, considered a major vector for the African horse sickness virus, C. oxystoma may also be involved in the transmission of this virus in Senegal given its abundance in the vicinity of horses and its suspected competence for other arboviruses including bluetongue virus. This study depicted a site-dependent spatial variability in the dynamics of the populations of the five major species in relation to the eco-climatic conditions at each site.

【 授权许可】

   
2014 Diarra et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Borkent A: World species of biting midges (Diptera: Ceratopogonidae). 2014. [http://wwx.inhs.illinois.edu/files/9913/9144/3328/CeratopogonidaeCatalog.pdf webcite]
• [2]Borkent A: The subgeneric classification of species of Culicoides - thoughts and a warning. 2014. [http://wwx.inhs.illinois.edu/files/9613/9136/7590/CulicoidesSubgenera.pdf webcite]
• [3]Carpenter S, Groschup MH, Garros C, Felippe-Bauer ML, Purse BV: Culicoides biting midges, arboviruses and public health in Europe. Antiviral Res 2013, 100(1):102-113.
• [4]Linley JR, Hoch AL, Pinheiro FP: Biting midges (Diptera: Ceratopogonidae) and human health. J Med Entomol 1983, 20(4):347-364.
• [5]Mellor P, Baylis M, Mertens P: Bluetongue. Oxford, UK: Elsevier; 2009.
• [6]OIE List of diseases in force in 2006 http://www.oie.int/en/animal-health-in-the-world/oie-listed-diseases-2006/ webcite
• [7]Carpenter S, Wilson A, Mellor PS: Culicoides and the emergence of bluetongue virus in northern Europe. Trends Microbiol 2009, 17(4):172-178.
• [8]Mellor PS, Wittmann EJ: Bluetongue Virus in the Mediterranean Basin 1998–2001. Vet J 2002, 164(1):20-37.
• [9]Purse BV, Mellor PS, Rogers DJ, Samuel AR, Mertens PP, Baylis M: Climate change and the recent emergence of bluetongue in Europe. Nat Rev Microbiol 2005, 3(2):171-181.
• [10]Curasson G: Introduction de la blue tongue en Afrique occidentale française. Bull Soc Pathol Exot 1925, 18:215-218.
• [11]Lefèvre PC, Calvez D: La fièvre catarrhale du mouton (bluetongue) en Afrique intertropicale: influence des facteurs écologiques sur la prévalence de l’infection. Rev Elev Med Vet Pays Trop 1986, 39(3–4):263-268.
• [12]Lefèvre PC, Taylor WP: Situation épidémiologique de la fièvre catarrhale ovine (Blue tongue) au Sénégal. Rev Elev Med Vet Pays Trop 1983, 36(3):241-245.
• [13]Mellor PS, Boorman J, Baylis M: Culicoides biting midges: their role as arbovirus vectors. Annu Rev Entomol 2000, 45:307-340.
• [14]Mellor PS, Hamblin C: African horse sickness. Vet Res 2004, 35(4):445-466.
• [15]Bazarusanga T: Contribution à l'étude de l’épidémiosurveillance de la peste équine au Sénégal: enquêtes sérologiques dans les zones de Rufisque, Kaffrine et Dahra. In Veterinary thesis. Université Cheikh Anta Diop de Dakar; 1995.
• [16]Akakpo AJ, Wombou Toukam CM, Mankor A, Ly C: Impact économique de l’épizootie de peste équine de 2007 au Sénégal. Bull Anim Hlth Prod Afr 2011, 59:1-16.
• [17]Diouf ND, Etter E, Lo MM, Lo M, Akakpo AJ: Outbreaks of African horse sickness in Senegal, and methods of control of the 2007 epidemic. Vet Rec 2013, 172(6):152.
• [18]Bakhoum MT, Fall M, Fall AG, Bellis GA, Gottlieb Y, Labuschagne K, Venter GJ, Diop M, Mall I, Seck MT, Allène X, Diarra M, Gardès L, Bouyer J, Delécolle JC, Balenghien T, Garros C: First Record of Culicoides oxystoma Kieffer and Diversity of Species within the Schultzei Group of Culicoides Latreille (Diptera: Ceratopogonidae) Biting Midges in Senegal. PloS One 2013, 8(12):e84316.
• [19]Cornet M: Les Culicoïdes (Diptera Ceratopogonidae) de l’Ouest africain (1ère note). Cah ORSTOM, sér Ent méd Parasitol 1969, VII(4):341-364.
• [20]Cornet MJB: Révision des espèces de Culicoides apparentées à C. schultzei (Enderlein, 1908) dans la région afrotropicale (Diptera, Ceratopogonidae). Bull Soc Entomol France 1994, 92(2):149-164.
• [21]Van Ark H, Meiswinkel R: Subsampling of large light trap catches of Culicoides (Diptera: Ceratopogonidae). Onderstepoort J Vet Res 1992, 59(3):183-189.
• [22]Glick JI: Culicoides biting midges (Diptera: Ceratopogonidae) of Kenya. J Med Entomol 1990, 27(2):85-195.
• [23]Khamala CPM, Kettle DS: The Culicoides Latreille (Diptera: Ceratopogonidae) of East Africa. TransR ent Soc Lond 1971, 123(1):1-95.
• [24]Meiswinkel P: Afrotropical Culicoides: a redescription of C. (Avaritia) imicola Kieffer, 1913 (Diptera: Ceratopogonidae) with description of the closely allied C. (A.) bolitinos sp. nov. reared from the dung of the African buffalo, blue wildebeest and cattle in South Africa. Onderstepoort J Vet Res 1989, 56(1):23-39.
• [25]Meiswinkel R: Afrotropical Culicoides: C (Avaritia) miombo sp. nov., a widespread species closely allied to C. (A.) imicola Kieffer, 1913 (Diptera: Ceratopogonidae). Onderstepoort J Vet Res 1991, 58(3):155-170.
• [26]Wirth WW, Hubert AA: The Culicoides of Southeast Asia (Diptera: Ceratopogonidae). Mem Am Entomol Inst 1989, 44:1-509.
• [27]Baylis M, el Hasnaoui H, Bouayoune H, Touti J, Mellor PS: The spatial and seasonal distribution of African horse sickness and its potential Culicoides vectors in Morocco. Med Vet Entomol 1997, 11(3):203-212.
• [28]Hollander M, Wolfe DA: Non parametric statistical methods. New York: Wiley; 1973.
• [29]R Development Core Team: R: a language and environment for statistical computing. [http://cran.r-project.org/manuals.html webcite]
• [30]Meiswinkel R, Scolamacchia F, Dik M, Mudde J, Dijkstra E, VDV IJ, Elbers AR: The Mondrian matrix: Culicoides biting midge abundance and seasonal incidence during the 2006–2008 epidemic of bluetongue in the Netherlands. Med Vet Entomol 2013, 28(1):10-20.
• [31]Rawlings P, Snow WF, Boorman J, Denison E, Hamblin C, Mellor PS: Culicoides in relation to transmission of African horse sickness virus in The Gambia. Med Vet Entomol 1998, 12(2):155-159.
• [32]El Sinnary KA, Muller R, Atta el Mannan A, Hussein SH: The diurnal activity of Culicoides kingi in northern Sudan. Rev Elev Med Vet Pays Trop 1985, 38(3):270-275.
• [33]Mellor PS, Carpenter S, White DM: Bluetongue virus in the insect host. In Bluetongue. Edited by Mellor P, Baylis M, Mertens P. Oxford, UK: Elsevier; 2009:295-320.
• [34]Yanase T, Kato T, Kubo T, Yoshida K, Ohashi S, Yamakawa M, Miura Y, Tsuda T: Isolation of bovine arboviruses from Culicoides biting midges (Diptera: Ceratopogonidae) in southern Japan: 1985–2002. J Med Entomol 2005, 42(1):63-67.
• [35]Mellor PS, Osborne R, Jennings DM: Isolation of bluetongue and related viruses from Culicoides spp. in the Sudan. J Hyg (Lond) 1984, 93(3):621-628.
• [36]Venter GJ, Mellor PS, Paweska JT: Oral susceptibility of South African stock-associated Culicoides species to bluetongue virus. Med Vet Entomol 2006, 20(3):329-334.
• [37]Meiswinkel R, Gomulski LM, Delecolle JC, Goffredo M, Gasperi G: The taxonomy of Culicoides vector complexes - unfinished business. Vet Ital 2004, 40(3):151-159.
• [38]Venter GJ, Paweska JT, Van Dijk AA, Mellor PS, Tabachnick WJ: Vector competence of Culicoides bolitinos and C. imicola for South African bluetongue virus serotypes 1, 3 and 4. Med Vet Entomol 1998, 12(4):378-385.
• [39]Venter GJ, Graham SD, Hamblin C: African horse sickness epidemiology: vector competence of south african Culicoides species for virus serotypes 3, 5 and 8. Med Vet Entomol 2000, 14(3):245-250.
• [40]Venter GJ, Groenewald D, Venter E, Hermanides KG, Howell PG: A comparison of the vector competence of the biting midges, Culicoides (Avaritia) bolitinos and C. (A.) imicola, for the Bryanston serotype of equine encephalosis virus. Med Vet Entomol 2002, 16(4):372-377.
• [41]Venter GJ, Groenewald DM, Paweska JT, Venter EH, Howell PG: Vector competence of selected South African Culicoides species for the Bryanston serotype of equine encephalosis virus. Med Vet Entomol 1999, 13(4):393-400.
• [42]Paweska JT, Venter GJ, Hamblin C: A comparison of the susceptibility of Culicoides imicola and C. bolitinos to oral infection with eight serotypes of epizootic haemorrhagic disease virus. Med Vet Entomol 2005, 19(2):200-207.
• [43]Meiswinkel R, Paweska JT: Evidence for a new field Culicoides vector of African horse sickness in South Africa. Prev Vet Med 2003, 60(3):243-253.
• [44]Lee VH: Isolation of viruses from field populations of Culicoides (Diptera: Ceratopogonidae) in Nigeria. J Med Entomol 1979, 16(1):76-79.
• [45]Venter GJ, Koekemoer JJ, Paweska JT: Investigations on outbreaks of African horse sickness in the surveillance zone in South Africa. Rev Sci Tech 2006, 25(3):1097-1109.
• [46]Venter GJ, Mellor PS, Wright I, Paweska JT: Replication of live-attenuated vaccine strains of bluetongue virus in orally infected South African Culicoides species. Med Vet Entomol 2007, 21(3):239-247.
• [47]Venter GJ, Paweska JT: Virus recovery rates for wild-type and live-attenuated vaccine strains of African horse sickness virus serotype 7 in orally infected South African Culicoides species. Med Vet Entomol 2007, 21(4):377-383.
• [48]Venter GJ, Majatladi DM, Labuschagne K, Boikanyo SN, Morey L: The attraction range of the Onderstepoort 220 V light trap for Culicoides biting midges as determined under South African field conditions. Vet Parasitol 2012, 190(1–2):222-229.
• [49]Nevill EM: The use of cattle to protect sheep from bluetongue infection. J SAfrVetAssoc 1978, 49(2):129-130.
• [50]Venter GJ, Meiswinkel R, Nevill EM, Edwardes M: Culicoides (Diptera:Ceratopogonidae) associated with livestock in the Onderstepoort area, Gauteng, South Africa as determined by light-trap collections. Onderstepoort J Vet Res 1996, 63(4):315-325.
• [51]Herniman KA, Boorman JP, Taylor WP: Bluetongue virus in a Nigerian dairy cattle herd. 1. Serological studies and correlation of virus activity to vector population. J Hyg (Lond) 1983, 90(2):177-193.
• [52]Mushi EZ, Isa JF, Chabo RG, Binta MG, Kapaata RW: Culicoides (Diptera: Ceratopogonidae) associated with horses at Mogoditshane, Gaborone, Botswana. Vet Res Commun 1998, 22(5):295-297.
• [53]Musuka GN, Meiswinkel R, Baylis M, Kelly PJ, Mellor PS: Prevalence of Culicoides imicola and other species (Diptera: Ceratopogonidae) at eight sites in Zimbabwe. J S Afr Vet Assoc 2001, 72(2):62-63.
• [54]Harrup LE, Purse BV, Golding N, Mellor PS, Carpenter S: Larval development and emergence sites of farm-associated Culicoides in the United Kingdom. Med Vet Entomol 2013, 27(4):441-449.
• [55]Poddar TK, Ray S, Choudhury A: Ecology of larval Culicoides oxystoma (Diptera: Ceratopogonidae) in the Hooghly estuary, Sagar Island India. Ann Entomol 1992, 10(1):19-25.
• [56]Garcia-Saenz A, McCarter P, Baylis M: The influence of host number on the attraction of biting midges, Culicoides spp., to light traps. Med Vet Entomol 2010, 25(1):113-115.
• [57]Kluiters G, Sugden D, Guis H, McIntyre KM, Labuschagne K, Vilar MJ, Baylis M: Modelling the spatial distribution of Culicoides biting midges at the local scale. J Appl Ecol 2013, 50(1):232-242.
• [58]Carpenter S, Szmaragd C, Barber J, Labuschagne K, Gubbins S, Mellor P: An assessment of Culicoides surveillance techniques in northern Europe: have we underestimated a potential bluetongue virus vector? J Appl Ecol 2008, 45(4):1237-1245.
• [59]Scheffer EG, Venter GJ, Labuschagne K, Page PC, Mullens BA, MacLachlan NJ, Osterrieder N, Guthrie AJ: Comparison of two trapping methods for Culicoides biting midges and determination of African horse sickness virus prevalence in midge populations at Onderstepoort, South Africa. Vet Parasitol 2012, 185(2–4):265-273.
• [60]Viennet E, Garros C, Lancelot R, Allene X, Gardes L, Rakotoarivony I, Crochet D, Delecolle JC, 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. BioMed Central Full Text