Culicoides (Diptera: Ceratopogonidae) midges, the vectors of African horse sickness virus – a host/vector contact study in the Niayes area of Senegal

Particle and Fibre Toxicology

Thierry Baldet⁴  Ousmane Faye¹  Lassana Konaté¹  Massouka Ndao³  Ange M Dusom³  Mame T Bakhoum³  Ignace Rakotoarivony⁴  Jean-Claude Delécolle²  Iba Mall³  Xavier Allène⁴  Geoffrey Gimonneau⁴  Claire Garros⁴  Jérémy Bouyer⁴  Momar T Seck³  Thomas Balenghien⁵  Assane G Fall³  Maryam Diarra³  Moussa Fall¹ 

[1] Faculté des Sciences et Techniques, Département de Biologie Animale, Université Cheikh Anta Diop, Dakar BP 5005, Senegal;UdS, IPPTS, Faculté de Médecine, Strasbourg, F-67000, France;ISRA, Laboratoire National de l’Elevage et de Recherches Vétérinaires, Route Front de Terre, Dakar, Senegal;INRA, UMR1309 CMAEE, Montpellier, F-34398, France;Cirad, UMR CMAEE, Montpellier, F-34398, France

关键词: Population dynamics;    Culicoides imicola;    Culicoides oxystoma;    Suspected vectors;    Animal health;   

Others  :  1147583
DOI  :  10.1186/s13071-014-0624-1

 received in 2014-07-23, accepted in 2014-12-26,  发布年份 2015

【 摘 要 】

Background

African horse sickness (AHS) is an equine disease endemic to Senegal. The African horse sickness virus (AHSV) is transmitted to the mammalian hosts by midges of the Culicoides Latreille genus. During the last epizootic outbreak of AHS in Senegal in 2007, 1,169 horses died from this disease entailing an estimated cost of 1.4 million euros. In spite of the serious animal health and economic implications of AHS, very little is known about determinants involved in transmission such as contact between horses and the Culicoides species suspected of being its vectors.

Methods

The monthly variation in host/vector contact was determined in the Niayes area, Senegal, an area which was severely affected by the 2007 outbreak of AHS. A horse-baited trap and two suction light traps (OVI type) were set up at each of five sites for three consecutive nights every month for one year.

Results

Of 254,338 Culicoides midges collected 209,543 (82.4%) were female and 44,795 (17.6%) male. Nineteen of the 41 species collected were new distribution records for Senegal. This increased the number of described Culicoides species found in Senegal to 53. Only 19 species, of the 41 species found in light trap, were collected in the horse-baited trap (23,669 specimens) largely dominated by Culicoides oxystoma (22,300 specimens, i.e. 94.2%) followed by Culicoides imicola (482 specimens, i.e. 2.0%) and Culicoides kingi (446 specimens, i.e. 1.9%).

Conclusions

Culicoides oxystoma should be considered as a potential vector of AHSV in the Niayes area of Senegal due to its abundance on horses and its role in the transmission of other Culicoides-borne viruses.

【 授权许可】

   
2015 Fall et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Borkent A. World species of biting midges (Diptera: Ceratopogonidae). RBC Museum, British Colombia, Canada; 2014.
• [2]Du Toit RM. The transmission of blue-tongue and horse sickness by Culicoides. Onderstepoort J Vet Sci Anim Ind. 1944; 19:7-16.
• [3]Coetzer JAW, Erasmus BJ. African horse sickness. In: Infectious Disease of Livestock with Special Reference to Southern Africa. Coetzer JAW, Thomson GR, Tustin RC, editors. Oxford University Press, Cape Town; 1994: p.460-75.
• [4]Mellor PS, Hamblin C. African horse sickness. Vet Res. 2004; 35(4):445-66.
• [5]African Horse Sickness. 2009.
• [6]Coetzer JAW, Guthrie AJ. African horse sickness. In: Infectious Diseases of Livestock, 2nd. Coetzer JAW, Tustin RC, editors. Oxford University Press, Southern Africa; 2004: p.1231-46.
• [7]Carpenter S, Mellor PS, Torr SJ. Control techniques for Culicoides biting midges and their application in the U.K. and northwestern Palaearctic. Med Vet Entomol. 2008; 22:175-87.
• [8]Akakpo AJ, Wombou Toukam CM, Mankor A, Ly C. Impact economique de l’epizootie de peste equine de 2007 au Senegal. Bull Anim Health Prod Afr. 2011; 59:1-16.
• [9]MacLachlan NJ, Guthrie AJ. Re-emergence of bluetongue, African horse sickness, and other orbivirus diseases. Vet Res. 2010; 41(6):35.
• [10]Bourdin P, Sarr J, Lejan C. Isolement et identification de la Peste équine africaine en zone sahélienne à partir de foyers récents. Bull Int Epiz. 1976; 86:717-9.
• [11]Sarr J, Diop M, Cissoko S. La peste equine africaine au senegal :un nouveau foyer a type 9 dans la commune de Thies. 1987.
• [12]Cornet M. Les Culicoides (Diptera: Ceratopogonidae) de l'Ouest Africain (1ere note). Cah ORSTOM Ser Entomol med Parasitol. 1969; 7(4):341-364.
• [13]Cornet M, Brunhes J. Révision des espèces de Culicoides apparentées à C. shultzei (Enderleini, 1908) dans la région afro-tropicale (Diptera: Ceratopogonidae). Bull Soc Entomol Fr. 1994; 92(2):149-64.
• [14]Cornet M, Chateau R. Les Culicoides de l’Ouest africain (2° note) Espèces apparentées à C. similis Carter, Ingrain et Macfie, 1920 (Diptera: Ceratopogonidae). Cah ORSTOM Ser Entomol med Parasitol. 1970; 8(2):141-73.
• [15]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):245-50.
• [16]Meiswinkel R, Paweska JT. Evidence for a new field Culicoides vector of African horse sickness in South Africa. Prev Vet Med. 2003; 60(3):243-53.
• [17]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; 21:377-83.
• [18]Meiswinkel R, Gomulski LM, Delécolle JC, Goffredo M, Gasperi G. The taxonomy of Culicoides vector complexes - unfinished business. Vet Ital. 2004; 40(3):151-9.
• [19]Bakhoum MT, Fall M, Fall AG, Bellis GA, Gottlieb Y, Labuschagne K et al.. 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):1-8.
• [20]Diarra M, Fall M, Fall AG, Diop A, Seck MT, Garros C et al.. Seasonal dynamics of Culicoides (Diptera: Ceratopogonidae) biting midges, potential vectors of African horse sickness and bluetongue viruses in the Niayes area of Senegal. Parasit Vectors. 2014; 7:147. BioMed Central Full Text
• [21]Sagna P. Le climat. In: Atlas du Sénégal. 2000.16-9.
• [22]Faye O, Gaye O, Fontenille D, Hébrard G, Konate L, Sy N et al.. La sécheresse et la baisse du paludisme dans les Niayes du Sénégal. Cah Santé. 1995; 5:299-305.
• [23]Fall AG, Diaite A, Lancelot R, Tran A, Soti V, Etter E et al.. Feeding behaviour of potential vectors of West Nile virus in Senegal. Parasit Vectors. 2011; 99(4):1-7.
• [24]Fall AG, Diaite A, Seck MT, Bouyer J, Lefrançois T, Vachiery N et al.. West Nile virus transmission in sentinel chickens and potential mosquito vectors, Senegal river delta, 2008–2009. Int J Environ Res Public Health. 2013; 10:4718-27.
• [25]Venter GJ, Paweska JT, Van Dijk AA, Mellor PS, Tabachnick WJ. Vector competence of Culicoides bolitinos and C. imicola (Diptera: Ceratopogonidae) for South African bluetongue virus serotypes 1, 3 and 4. Med Vet Entomol. 1998; 12:378-85.
• [26]Goffredo M, Meiswinkel R. Entomological surveillance of bluetongue in Italy: methods of capture, catch analysis and identification of Culicoides biting midges. Vet Ital. 2004; 40(3):260-5.
• [27]Venter GJ, Majatladi DM, Labuschagne K, Boikanyo SNB, 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; 190:222-9.
• [28]Wirth WW, Marston N. A method for mounting small insects on microscope slides in canada balsam. Ann Entomol Soc Am. 1968; 61:783-4.
• [29]Cornet M, Nevill EM, Walker AR. Notes sur les Culicoides (Diptera: Ceratopogonidae), du groupe de C. milnei Auten,1909, en Afrique orientale et australe. Cah ORSTOM Ser Entomol med Parasitol. 1974; 12(4):231-43.
• [30]Boorman J. Culicoides (Diptera: Ceratopogonidae) of the Arabian Peninsula with Notes on their médical and veterinary importance. Fauna Saudi Arabia. 1979; 10:160-224.
• [31]Boorman J, Dipeolu OO. A taxonomic study of adult Nigerian Culicoides Latreille (Diptera: Ceratopogoaidae) species. Occ Publ Ent Soc Nigeria. 1979; 22:1-121.
• [32]Meiswinkel R. Afrotropical Culicoides: a redescription of C. (Avaritia) imicola Kieffer, 1913 (Diptera: Ceratopogonidae) with description of the closely allied C. (Avaritia) bolitinos sp. Nov. reared from the dung of the african buffalo, blue wildebeest and cattle in South Africa. Onderstepoort J Vet Res. 1989; 56:23-39.
• [33]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):155-70.
• [34]Glick JI. Culicoides biting midges (Diptera: Ceratopogonidae) of Kenya. J Med Entomol. 1990; 27(2):85-195.
• [35]Van Ark H, Meiswinkel R. Subsampling of large light trap catches of Culicoides (Diptera: Ceratopogonidae). Onderstepoort J Vet Res. 1992; 59:183-9.
• [36]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):203-12.
• [37]Hollander M, Wolfe DA. Non parametric statistical inference. John Wiley & Sons, Inc, N Y; 1973.
• [38]Benzécri JP. Analyse de l’inertie intra-classe par l’analyse d’un tableau de correspondances. Cah Anal Donnees. 1983; 8:351-8.
• [39]Dolédec S, Chessel D. Rythmes saisonniers et composantes stationnelles en milieu aquatique I- Description d’un plan d'observations complet par projection de variables. Acta Oecologica, Oecologia Generalis. 1987; 8(3):403-26.
• [40]R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria; 2005.
• [41]Wirth WW, Hubert AA. The Culicoides of southeast Asia (Diptera: Ceratopogonidae). Mem Am Entomol Inst. 1989; 44:1-509.
• [42]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 Record. 2013; 172(6):152.
• [43]Kurogi H, Akiba K, Inaba Y, Matumoto M. Isolation of Akabane virus from the biting midge Culicoides oxystoma in Japan. Vet Microbiol. 1987; 15(3):243-8.
• [44]Yanase T, Kato T, Kubo T, Yoshida K, Ohashi S, Yamakawa M et al.. Isolation of bovine arboviruses from Culicoides biting midges (Diptera: Ceratopogonidae) in southern Japan: 1985–2002. J Med Entomol. 2005; 42(1):63-7.
• [45]Morag N, Saroya Y, Bravermann Y, Klement E, Gottlieb Y. Molecular identification, phylogenetic status and geographic distribution of Culicoides oxystoma (Diptera: Ceratopogonidae) in Israel. PLoS ONE. 2012; 7(3):e33610.
• [46]Dadawala AI, Biswas SK, Rehman W, Chand K, De A, Mathapati BS et al.. Isolation of bluetongue virus serotype 1 from Culicoides vector captured in livestock farms and sequence analysis of the viral genome segment-2. Transbound Emerg Dis. 2012; 59:361-8.
• [47]Venter GJ, Mellor PS, Paweska JT. Oral susceptibility of South African stock-associated Culicoides species to bluetongue virus. Med Vet Entomol. 2006; 20:329-334.
• [48]Rawlings P, Pro MJ, Pena I, Ortega MDC. Spatial and seasonal distribution of Culicoides imicola in Iberia in relation to the transmission of African horse sickness virus. Med Vet Entomol. 1997; 11:49-57.
• [49]Mellor PS, Boorman J, Baylis M. Culicoides biting midges: their role as arbovirus vectors. Annu Rev Entomol. 2000; 45:307-40.
• [50]Mellor PS, Osborne R, Jennings DM. Isolation of bluetongue and related viruses from Culicoides spp. in the Sudan. J Hyg. 1984; 93(3):621-8.
• [51]Nevill EM, Venter GJ, Edwardes M. Potential Culicoides vectors of livestock orbiviruses. In: Bluetongue, African horse sickness, and related orbiviruses: Proceedings of the 2nd International Symposium. Walton TE, Osburn BI, editors. CRC Press, Boca Raton, Florida; 1992: p.306-13.
• [52]Venter GJ, Labuschagne K, Hermanides KG, Boikanyo SNB, Majatladi DM, Morey L. Comparison of the efficiency of five suction light traps under field conditions in South Africa for the collection of Culicoides species. Vet Parasitol. 2009; 166(3):299-307.
• [53]Yanase T, Matsumoto Y, Matsumori Y, Aizawa M, Hirata M, Kato T et al.. Molecular identification of field-collected Culicoides larvae in the southern part of Japan. J Med Entomol. 2013; 50(5):1105-10.
• [54]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. 1983; 90(2):177-93.
• [55]Bishop AL, Mckenzie J, Sporh LJ, Barchia IM. Culicoides brevitarsis Kieffer (Diptera: Ceratopogonidae) in different farm habitats. Aust J Zool. 1994; 42:372-84.
• [56]Wirth WW, Dyce AL. The taxonomic status of the Culicoides vectors of bluetongue viruses. In: Bluetongue and Related Orbiviruses. Barber TL, Jochim MM, Alan R, editors. Liss, NY; 1985: p.151-64.
• [57]Ray S, Choudhury A. Vertical distribution of a biting midge, Culicoides oxystoma (Diptera: Ceratopogonidae) during different seasons in the Hooghly Estuary, Sagar Island, India. Insect Sci Appl. 1988; 9(3):329-33.
• [58]Poddar TK, Ray S, Choudhury A. Ecology of larval Culicoides oxystoma (Diptera: Ceratopogonidea) in the Hoogly Estuary, Sagar Island, India. Ann Entomol Soc Am. 1992; 10(1):19-25.
• [59]Akogbeto M. Etude entomologique sur la transmission du paludisme côtier lagunaire : cas d’un village construit sur un lac d’eau saumâtre. Ann Soc Belge Med Trop. 1995; 75:219-27.
• [60]Nevill EM, Anderson D. Host preferences of Culicoides midges (Diptera: Ceratopogonidae) in South Africa as determined by precipitin tests and light trap catches. Onderstepoort J Vet Res. 1972; 39(3):147-52.
• [61]Meiswinkel R, Baylis M, Labuschagne K. Stabling and the protection of horses from Culicoides bolitinos (Diptera: Ceratopogonidae), a recently identified vector of African horse sickness. Bull Entomol Res. 2000; 90:509-15.
• [62]Viennet E, Garros C, Lancelot R, Allene X, Gardes L, Rakotoarivony I et al.. 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. Parasites Vectors. 2011; 4:119. BioMed Central Full Text
• [63]Scheffer EG, Venter GJ, Labuschagne K, Page PC, Mullens BA, MacLachlan NJ et al.. 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; 185:265-273.