Diptera: Ceratopogonidae), Vectors of African Horse Sickness and Bluetongue Viruses in Senegal Moussa Fall, Assane G

Host preferences and circadian rhythm of Culicoides (Diptera: Ceratopogonidae), vectors of African horse sickness and bluetongue viruses in Senegal Moussa Fall, Assane G. Fall, Momar T. Seck, Jérémy Bouyer, Maryam Diarra, Renaud Lancelot, Geoffrey Gimonneau, Claire Garros, Mame T. Bakhoum, Ousmane Faye, et al.

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Moussa Fall, Assane G. Fall, Momar T. Seck, Jérémy Bouyer, Maryam Diarra, et al.. Host preferences and circadian rhythm of Culicoides (Diptera: Ceratopogonidae), vectors of African horse sickness and bluetongue viruses in Senegal. Acta Tropica, Elsevier, 2015, 149, pp.239-245. 10.1016/j.actatropica.2015.06.012. hal-02641485

HAL Id: hal-02641485 https://hal.inrae.fr/hal-02641485 Submitted on 28 May 2020

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Version postprint Lancelot, R.,Gimonneau, G.,Garros, C.,Bakhoum, M.T.,Faye,O., Baldet,T.,Balenghien, T. (2015). African horse sickness and bluetongue viruses in Senegal. Acta Tropica, 149, 239-245. DOI : Host preferences and circadian rhythm of Culicoides (Diptera: Ceratopogonidae), vectors of Fall, M. (Auteurdecorrespondance), Fall,A.G.,Seck, M.T.,Bouyer, J.,Diarra, M., laect hsatcea:Fl,Mus,Fl,Asn . ek oa T., Momar Seck, G., Assane Fall, Moussa, Fall, as: article J this Bouyer, 12-6-2015 cite 10-6-2015 Please 5-3-2015 date: Accepted date: http://dx.doi.org/doi:10.1016/j.actatropica.2015.06.012 Revised S0001-706X(15)30032-2 3654 date: ACTROP Received in: appear To Reference: DOI: PII: Balenghien Faye Thomas Ousmane Baldet Bakhoum Thierry T. Mame Garros Claire Geoffrey J Gimonneau Lancelot Seck T. Renaud Momar Diarra Fall Maryam G. Bouyer Assane Fall Moussa Author: Senegal in viruses sickness bluetongue horse and African of vectors of Ceratopogonidae), rhythm (Diptera: circadian and preferences Host Title: Manuscript Accepted rosmyb icvrdwihcudafc h otn,adallgldsliesthat disclaimers legal all and pertain. content, journal the the affect to could apply which manuscript. discovered the be its of may in errors version proof published early resulting is this the of it providing review before and are typesetting, copyediting, we undergo customers will manuscript our The to service a As PDF Tropica a Senegal.Acta is in This viruses Ceratopogonidae), bluetongue (Diptera: and sickness Culicoides horse of http://dx.doi.org/10.1016/j.actatropica.2015.06.012 Thomas, African rhythm Balenghien, of Thierry, circadian vectors Baldet, and Ousmane, preferences Faye, Host T., Mame Bakhoum, Claire, 10.1016/j.actatropica.2015.06.012 er ´ Comment citer cedocument: m,Dar,Mra,Lneo,Rnu,Gmneu efry Garros, Geoffrey, Gimonneau, Renaud, Lancelot, Maryam, Diarra, emy, ´ ﬁ eo nueie aucitta a enacpe o publication. for accepted been has that manuscript unedited an of le caTropica Acta

ﬁ a om laent htdrn h rdcinprocess production the during that note Please form. nal Culicoides er ´ emy ´ Version postprint Lancelot, R.,Gimonneau, G.,Garros, C.,Bakhoum, M.T.,Faye,O., Baldet,T.,Balenghien, T. (2015). African horse sickness and bluetongue viruses in Senegal. Acta Tropica, 149, 239-245. DOI : Host preferences and circadian rhythm of Culicoides (Diptera: Ceratopogonidae), vectors of Abstract Highlights [email protected] E-mail: +221 3679 832 33 Fax: 45 + Tel.: 26 953 77 221 Fall, Moussa ISRA-LNERV, Front du Route de Terre, B Correspondingauthor. hôt ‘Interactions dansles maladies tropicales négligées try dues aux Recherche de Mixte Unité (CIRAD), 6 Burkina Dioulasso, Faso 5 4 University,Dakar BP Senegal 5005, Anim Maladies 3 des Contrôle International Campus de Baillarguet, F34398, Montpe Recherche de Mixte Unité 2 RecherchesVétérinaires, BP Dakar 2057, - Hann, Sén 1 Fay e LancelotRenaud Fall Moussa Ceratopogonidae), vectors of African horse sickness horse African of vectors Ceratopogonidae), ete e oprto Itrainl e Rcece A Recherche en Internationale Coopération de Centre C Eradication Trypanosomosis and Tsetse Pan-African InstitutNational de la Recherche Agronomique (INRA Facultédes Sciences et Techniques, Département de Fall, M. (Auteurdecorrespondance), Fall,A.G.,Seck, M.T.,Bouyer, J.,Diarra, M., Centre de Coopération Internationale en Recherche A Recherche en Internationale Coopération de Centre nttt ééaas e ehrhs gioe, Labora Agricoles, Recherches de Sénégalais Institut • • • • • 3 , Thierry , Baldet Midgespreferred horse compared sheep to and are ma ed We the nuisance associated with compared We preferences host of these described We host-seeking activity of Host preferences and circadian rhythm of circadian and preferences Host 1,3 Asn G Fall G. Assane , 2 Gofe Gimonneau Geoffrey , 2 10.1016/j.actatropica.2015.06.012 , Thomas BalenghienThomas , Comment citer cedocument: 1 Mmr . Seck T. Momar ,

in Senegal Senegal in 1,2 Lasiohelae 2 Car Garros Claire ,

C.oxystoma Culicoides panosomatidés’,France Montpellier, 34398 1 Jrm Bouyer Jérémy , BiologieAnta Animale, Diop Cheikh égal llier, France llier, sp for sp animals ), Unité Mixte de Recherche ),Unité Mixte 1309 P 2057, Dakar-Hann, 2057, P Sénégal. gronomique pour le Développement, Développement, le pour gronomique gronomique pour le Développement Développement le pour gronomique and es-vecteurs-parasites-environnement es-vecteurs-parasites-environnement for horse and sheep . toire National de l'Elevage et de de et l'Elevage de National toire

2 , , mag, 1 P 07 Bobo- 1087, BP 01 ampaign, Culicoides inlycrepuscular ales Exotiques et Emergentes, Emergentes, et Exotiques ales ae . Bakhoum T. Mame C.imicola and bluetongue viruses viruses bluetongue and

1,2,4,5,6 in Senegal in (Diptera: (Diptera: Mra Diarra Maryam , 1 Ousmane , 1 , , Version postprint Lancelot, R.,Gimonneau, G.,Garros, C.,Bakhoum, M.T.,Faye,O., Baldet,T.,Balenghien, T. (2015). African horse sickness and bluetongue viruses in Senegal. Acta Tropica, 149, 239-245. DOI : Host preferences and circadian rhythm of Culicoides (Diptera: Ceratopogonidae), vectors of grsie oad hre (Fall horses towards aggressive epizoo previous the by affected particularly region al. oxystoma Culicoides vector control methods. i which BT, and AHS of transmission the in involved ecologyof and biology the about known (Rawlings(BTV) virus (Venter bolitinos Culicoides Culicoides ( Orbiviruses by caused ar (BT) bluetongue and (AHS) sickness horse African Introduction activity,Thiès (Senegal) words: Key forpest animal species both used as bait. Unexpe sunset. after Lasiohelea peak with nocturnal mostly was collected numbers in peaks with diel the throughout for 26 hors between ratio predicted (the sheep to compared ( that found We rhythm. circadian orbivirus these of vectors potential of preferences stud this of purpose The virus. the of transmission on knowledge our improve to undertaken been 200 in sickness horse African outbreak epizootic of to and horses to Ceratopogonidae) (Diptera: midges or are virus bluetongue and sickness- horse African C.imicola Fall, M. (Auteurdecorrespondance), Fall,A.G.,Seck, M.T.,Bouyer, J.,Diarra, M., 21) Ti seis s bnat n ih-rp in light-traps in abundant is species This 2013). , et al. et . imicola C. , , (Diptera: Ceratopogonidae). In southern Africa, Africa, southern In Ceratopogonidae). (Diptera: was also collected during this study. This diurnal This study. this during collected also was C. bolitinos C. , 1999; Venter 1999; , Culicoides ), and were mostly crepuscular: crepuscular: mostly were and ), Meiswinkel are proven vectors of African horse sick horse African of vectors proven are Meiswinkel Kieffer was detected for the first time in Senegal Senegal in time first the for detected was Kieffer 10.1016/j.actatropica.2015.06.012 et al.et Comment citer cedocument: Reoviridae and Obvrs rnmsin hs-edn pten die pattern, host-feeding transmission, Orbivirus , et al.et , 1997; Venter 1997; , . pseudopallidipennis C. t al. et Culicoides oxystoma oxystoma Culicoides ) transmitted by small hematophagous insects of the of insects hematophagous small by transmitted ) , 2000; Meiswinkel & Paweska, 2003) and of bluetong of and 2003) Paweska, & Meiswinkel 2000; ,

21) Frhroe tee tde cletd p to up collected studies these Furthermore, 2015). , Culicoides Culicoides et al.et Culicoides Culicoides , 2000; Mellor & Hamblin, 2004). Little is is Little 2004). Hamblin, & Mellor 2000; , 7 in Senegal, extensive investigations have investigationshave extensive Senegal, in 7 es on horse and sheep and to study their their study to and sheep and horse on es after sunrise and sunset, while sunset, and sunrise after by transmitted biviruses species in West Africa, in particular those those particular in Africa, West in species y was to compare and quantify the host host the quantify and compare to was y i otra o AS n 07 i i also is it 2007; in AHS of outbreak tic e and sheep was 80 for 80 was sheep and e h Nae area(Diarra Niayes the . oxystoma C. ) had a preference for horse when when horse for preference a had ) ruminants respectively. Since the last last the Since respectively. ruminants and species of the sub-genus the of species and mpedes the development of efficient efficient of development the mpedes e endemic diseases in West Africa; Africa; West in diseases endemic e ctedly, species of the subgenus subgenus the of species ctedly, Culicoides imicola imicola Culicoides species biting species was a nuisance nuisance a was species biting

had continuous activity activity continuous had novd oal i the in locally involved in 2011 (Bakhoum 2011 in ness virus (AHSV) (AHSV) virus ness Culicoides C. oxystoma C. t al. et l host-seeking host-seeking l ife and Kieffer C. imicola imicola C. 21) a 2014), , Avaritia genus genus biting biting and and 41 41 et et ue ue

Version postprint Lancelot, R.,Gimonneau, G.,Garros, C.,Bakhoum, M.T.,Faye,O., Baldet,T.,Balenghien, T. (2015). African horse sickness and bluetongue viruses in Senegal. Acta Tropica, 149, 239-245. DOI : Host preferences and circadian rhythm of Culicoides (Diptera: Ceratopogonidae), vectors of The study was conducted at the Thiès national stud stud national Thiès the season rain the of middle the in 2013 September, at28 conducted was study The methods Materials and comparingtheir attraction horse to and sheep and d of arboviruses, of pref host describes study present The Africa. in is about data current fragmentary how illustrates This sunriseand the other (El close Sinnary sunset to are far so studied significance (Itoua dubitatus kumbaensis in zoo-anthropophilic are Africa Central in studied seasons. abundance during and areas some in humans occurs activity feeding peak and anthropophilic its Itoua a 1977) (Auriault, Gabon 1953), (Nicholas, Cameroon genus the of species African c been has research little Africa, South of Outside 1984). kingi Culicoides vir disease haemorrhagic epizootic the transmitting (Kurogi Japan in virus Akabane (PrasadIndia al.et Seneg in AHSV the of transmission the to contribute of those to equivalent horse that highlighted and 53) to 34 from Senegal Culicoides Fall, M. (Auteurdecorrespondance), Fall,A.G.,Seck, M.T.,Bouyer, J.,Diarra, M., 1) Study Area Study 1) , 2015). , t al. et t al. et rmr Rbot-ite ad eéol and Delécolle and Rebholtz-Hirtzel Kremer, species (this increased the number of described described of number the increased (this species , 1987) and primarily related to to related primarily and 1987) , alt Kee, oce ad Bach and Mouchet Kremer, Callot, 18) Otie oten fia te ny African only the Africa, southern Outside 1987). , Culicoides oxystomaCulicoides t al. et has been found in the field to be infected by EHDV by infected be to field the in found been has Culicoides 19) a ivle i te rnmsin f bovine of transmission the in involved as 1999), , 10.1016/j.actatropica.2015.06.012 Comment citer cedocument: that are potential vectors of the AHSV and BTV in in BTV and AHSV the of vectors potential are that Culicoides C. kingi C. . imicola C. has been reported as a putative vector for BTV in in BTV for vector putative a as reported been has t al. et

in Sudan which displays two biting peaks: one afte one peaks: biting two displays which Sudan in . The only in-depth investigations were conducted i conducted were investigations in-depth only The . 18; Yanase 1987; , . It may be that that be may It . Culicoides kingi kingi Culicoides uiods grahamii Culicoides et al. Clcie fulvithorax Culicoides , erences, as key elements in the transmission transmission the in elements key as erences, onducted on the biology and ecology of the the of ecology and biology the on onducted at sunrise and sunset, causing a nuisance to to a nuisance causing and sunset, at sunrise eterminingtheir circadian rhythm. the life history and ecology of ecology and history life the us (EHDV) in Israel (MoragIsrael in (EHDV) us their feeding behaviour, e.g. e.g. behaviour, feeding their . This stud farm was located in a forested forested a in located was farm stud This . al, and more broadly in West Africa(Fall West in broadly more and al, , 1985). , nd Congo (Vattier-BernardCongo nd uiods trifasciellus Culicoides t al. et However, most most However, am ewe 2 Ags and August 29 between farm C. oxystoma C. Austen reaches abundances on on abundances reaches Austen 20) n i ssetd of suspected is and 2005) , Culicoides Culicoides Austen in Sudan (Mellor Sudan in species of veterinary veterinary of species Austen arboviruses such as as such arboviruses and Culicoides Culicoides species found in in found species . . This species is is species This et al.et C. kingi kingi C. Goetghebuer et al.et , Culicoides Culicoides , Senegal by by Senegal Culicoides Culicoides Culicoides northern northern , 2012). , species species , 1986; 1986; , et al.et also n n r r , ,

to enter, to engorge or not on animal, and avoidin and animal, on not or engorge to enter, to ee oh bnat (Diarra abundant both were . (2015).The animal-baited trap consists of a net b net a of consists trap animal-baited (2015).The . Culicoides Culicoides r pasturage and a cattle herd was grazing at at grazing was herd cattle a and pasturage r ted from Dakar in the south to the Senegal Senegal the to south the in Dakar from ted depressions between dunes that flooded flooded that dunes between depressions g 24 x 2 x 3 = 3 hours each. 144 x 2 g x 24 e year before the start of the experiment. experiment. the of start the before year e infall rarely exceeds 500 mm/year with a a with mm/year 500 exceeds rarely infall eaner.Each 24-h period was spread over over spread was period 24-h eaner.Each two locations separated by a distance of of distance a by separated locations two found there together with a number of of number a with together there found he switch of animals between the two two the between animals of switch he g each session, midges were collected collected were midges session, each g uare design. One horse and two sheep sheep two and horse One design. uare and 30 kg each. The baited traps used used traps baited The each. kg 30 and between 110 and 120 kg. The sheep sheep The kg. 120 and 110 between cinity is conducive to a high relative relative high a to conducive is cinity the distance from the sea and time of of time and sea the from distance the mise between-trap interactions. Other Other interactions. between-trap mise ) to midday (day 2). The two 24-h 24-h two The 2). (day midday to ) abundance, and this site was selected was site this and abundance, mercial garden crops and fruit are are fruit and crops garden mercial dges trapped inside the tents were were tents the inside trapped dges m) with an open space of 15 cm cm 15 of space open an with m) t al. et , 2014).The city of of city 2014).The , g the the g ox ox Version postprint Lancelot, R.,Gimonneau, G.,Garros, C.,Bakhoum, M.T.,Faye,O., Baldet,T.,Balenghien, T. (2015). African horse sickness and bluetongue viruses in Senegal. Acta Tropica, 149, 239-245. DOI : Host preferences and circadian rhythm of Culicoides (Diptera: Ceratopogonidae), vectors of Culicoides 1,259 of total A preference Host humiditywere higher and (about 37%) 9°C than inter Intra-se sessions. three the for 85.6% to 47.0 from 5 from varied humidity and session third the 33.6°C 3 to 26.4 from session, collection first the 32.8°C last the during sunny and sessions collection first se rainfall the during out carried were Collections Results data All analyses were performed using statistica R (2013) andwas Schielzeth used as an overall f test (AIC). criterion information Akaike the and model, con the ratio test, likelihood a on was model based effec fixed as sheep) (horse, host the and location day trapping the Ga used We adaptive log-likelihood. maximized an providing method a with fitted model of abundance Unadjusted co engorgedfemales by number the of total females col were rates Engorgement weight. host for adjusted spe by compared were hosts respective on Abundances and90% stored alcohol. in spec nu The not. or as gravid and unengorged, categorized or engorged were females and sex, and species tec (1968) Marston and Wirth the with accordance in specime needed, When 1994). Brunhes, & Cornet 1991; Meiswinkel 1989; Boorman, 1979; Dipeolu, & (Boorman morphothe usingDV4) Stemi stereomicroscope(Zeiss, temperatur low by of killed identification were collected insects The Fall, M. (Auteurdecorrespondance), Fall,A.G.,Seck, M.T.,Bouyer, J.,Diarra, M., 4) Statistical analysis analysis Statistical 4) were collected in the horse-baited trap, i.e. 96.5 i.e. trap, horse-baited the in collected were Culicoides Culicoides 10.1016/j.actatropica.2015.06.012 Comment citer cedocument: specimens were collected, of which 54 were males. males. were 54 which of collected, were specimens Culicoides pce rle o a eaiain f ig patterns wing of examination an on relied species

pce ws oeld sn a oso mixed-effect Poisson a using modelled was species orgoodness of fit. session. Temperatures varied from 23.2 to to 23.2 from varied Temperatures session. 4.8°C the second session, and from 25.2 to to 25.2 from and session, second the 4.8°C fidence intervals for parameters in the fitted the fitted in parameters fidencefor intervals l packages(R_Core_Team, l 2014). ason. Weather was cloudy during the two two the during cloudy was Weather ason. ssion amplitudes of both temperature and and temperature both of amplitudes ssion lected. ts. Selection of effects in the abundance abundance the in effects of Selection ts. -session amplitudes (1-3°C and amplitudes -session 1-9%). The procedure proposed by Nakagawa Nakagawa by proposed procedure The 5.1 to 90.6%, from 49.3 to 84.6% and and 84.6% to 49.3 from 90.6%, to 5.1 imens were placed in Eppendorf tubes tubes Eppendorf in placed were imens logical keys for the Afrotropical region region Afrotropicalthe keysfor logical (1 to 6) as a random effect, and the the and effect, random a as 6) to (1 hnique. mputed by dividing the number of of number the dividing by mputed ns were dissected and slide-mounted slide-mounted and dissected were ns lpru o pru (ye 1969), (Dyce, parous or lliparous s-emt apoiain o the to approximation uss-Hermite cies using the raw data and data data and data raw the using cies e and identified. Morphological Morphological identified. and e , 1989; Glick, 1990; Meiswinkel, Meiswinkel, 1990; Glick, 1989; , % of overall collections, vs. 44 in 44 vs. collections, overall of % Culicoides were counted by by counted were In total, 1,215 1,215 total, In under a a under Version postprint Lancelot, R.,Gimonneau, G.,Garros, C.,Bakhoum, M.T.,Faye,O., Baldet,T.,Balenghien, T. (2015). African horse sickness and bluetongue viruses in Senegal. Acta Tropica, 149, 239-245. DOI : Host preferences and circadian rhythm of Culicoides (Diptera: Ceratopogonidae), vectors of between thesites. two co those and horse the on collected females between fixed the For effect. host the by explained (94.2%) ma the whereas (97.0), high very was R² conditional of abundance the predict To sites. two t as much as twice weighing horse (the sheep the on c females between 80 of ratio a predicted model the (marginal marginal the whereas and fixed both by explained variance of (percentage day trapping the and effects, fixed the as host the of abundance the predict To (Figure98% 1); from of to 96 females were collecte for trap sheep-baited the a were figures weight-adjusted host the and raw the sig varied caughtfemales of number Theother). the Overall, identified.The incidental was collection their and baits sheep and Macfieand and Ingram Carter, and Macfie and Kettle, and Khamala for sheep from ranged species these for rate engorgement The 97.8% for accounted species 4 these together, Taken and (4.3%) specimens namely group, Imicola the The (73.7%). specimens 928 with collections, the in w 8 only oxystoma Culicoides while trap, horse-baited the in found were iden We 1). (Table 3.5% i.e. trap, sheep-baited the Fall, M. (Auteurdecorrespondance), Fall,A.G.,Seck, M.T.,Bouyer, J.,Diarra, M., Culicoides Culicoides C. oxystoma C. R ² = 64.6%), and mainly (96.0%) explained by the hos the by explained (96.0%) mainly and 64.6%), = ² Culicoides Culicoides moreli moreli Culicoides numbers were fairly balanced between sites (593 in in (593 sites between balanced fairly were numbers , the only representative species of the Schultzei Schultzei the of species representative only the , 10.1016/j.actatropica.2015.06.012 Culicoides nivosus nivosus Culicoides (Table 1). The other species – – species other The 1). (Table Comment citer cedocument: Culicoides pseudopallidipennis pseudopallidipennis Culicoides R (ecnae f aine xlie b fxd effect fixed by explained variance of (percentage ² population was relatively population young a with nulliparous C. oxystoma, C. imicola, C. bolitinos C. imicola, C. oxystoma, C. C. oxystoma C. C. imicola imicola C. Culicoides leucostictus leucostictus Culicoides Clastrier were uncommon. Finally, uncommon. were Clastrier

C. imicola imicola C. females, we selected the full model with the site site the with model full the selected we females, with 214 specimens (16.9%), (16.9%), specimens 214 with De Meillon, Meillon, De as the random effect. The conditional conditional The effect. random the as since only gravid females or males were were males or females gravid only since d on this host (Table host 1). this on d Both sessions. trapping between nificantly effect, this model predicted a ratio of 26 26 of ratio a predicted model this effect, females, we selected the full model. The The model. full the selected we females, lways much greater for the horse than for for than horse the for greater much lways ollected on the horse and those collected collected those and horse the on ollected random effects) was very high (99.6%), (99.6%), high very was effects) random medium-abundance species belonged to to belonged species medium-abundance 40 to 50% on the horse and was 20% on on 20% was and horse the on 50% to 40 tified 11 different species, all of which which of all species, different 11 tified he ewes) and a ratio of 2.5 between the the between 2.5 of ratio a and ewes) he llected on the sheep and a ratio of 2.2 2.2 of ratio a and sheep the on llected f the of rginal R² was high (63.8), and mainly mainly and (63.8), high was R² rginal C. trifasciellus C. Kieffer were not attracted by the horse horse the by attracted not were Kieffer Culicoides nigripennis Culicoidesnigripennis Clastrier with 34 specimens (2.7%). (2.7%). specimens 34 with Clastrier ere found in the sheep-baited trap. trap. sheep-baited the in found ere Culicoides and t effect. For the fixed effects, fixed the For effect. t , group, was predominant was group, . pseudopallidipennis C. Culicoides translucens translucens Culicoides Culicoides accraensis accraensis Culicoides C. bolitinos C. collected (Table 1). 1). (Table collected one site and 600 in 600 and site one rate of 70%. atr Ingram Carter, s) was high high was s) with 55 55 with and and R ² ²

bnacs n ah rpig eso wr correlated were session trapping each in abundances of abundance pseudopallidipennis C. overall the shows 2 Figure rhythms Circadian gravid of females. (bfR):engorgementpercentage;N:engorgedfemales; numb F: abundance; of percentages cumulative (C%): 1. Table sheep, on which were always low. sheep two were used against one horse) was applied collectedsimil each quite on look Both plots host. bolitinos Culicoides imicola, Culicoides Figure1: Fall, M. (Auteurdecorrespondance), Fall,A.G.,Seck, M.T.,Bouyer, J.,Diarra, M., species

Numberof Raw abundance weight-adjusted and host abundance o OA TOTAL Total Rank Culicoides 10.1016/j.actatropica.2015.06.012 11 10 eae oe te il eades f ot Fr each For host. of regardless diel the over females 9 8 7 6 5 4 3 2 1 Comment citer cedocument: 100.0 100.0 (C%) 99.9 99.7 99.4 99.1 98.7 97.8 95.1 90.7 73.7 collected during the trapping 6 days horse on and 1,205

212 881 11 33 55 F F 1 0 2 3 3 4 , and , number of nulliparous females; P: number of parousofnumbernulliparous of numberP: females; r f eae; P: aos ae M nme o males of number M: rate; parous (P): females; of er 30.4 16.1 12.8 35.8 5.6 (P) ------Culicoides pseudopallidipennis Culicoides . oxystoma C. aras weight-correction as (which limited is 4 54 47 M 0 1 0 1 1 1 0 1 0 2 on the on numbers of

for nulliparous, parous, gravid and and gravid parous, nulliparous, for Horse-baitedtrap 1,174 206 867 11 32 53 F F 0 1 1 2 0 1 , , . imicola C. bf F F bf 519 381 f 14 22 99 0 0 0 0 0 0 3 Culicoides oxystoma, Culicoides (bfR) 44.2 43.8 41.5 48.0 43.9 Culicoides ------, , species, observed observed species, C. bolitinos C. females 448 308 17 26 91 N 0 0 0 0 0 0 6 females; G: numberG: females; sheep baits collected bF nme of number bfF: ; 200 176 14 P P 0 1 0 2 0 0 2 1 4 and , G 7 0 0 1 0 0 1 1 0 1 2 2 1 41 36

M 1 0 0 1 1 1 0 0 0 1 Sheep- 14 31 F F 0 0 1 1 3 3 0 1 2 6

baited trapbaited bf F

9 0 0 2 1 1 1 1 3 Version postprint Lancelot, R.,Gimonneau, G.,Garros, C.,Bakhoum, M.T.,Faye,O., Baldet,T.,Balenghien, T. (2015). African horse sickness and bluetongue viruses in Senegal. Acta Tropica, 149, 239-245. DOI : Host preferences and circadian rhythm of Culicoides (Diptera: Ceratopogonidae), vectors of the Ceratopogonidae another identified we Additionally, sunriseand sunset. represents line the average of observations. The ve pseudopallidipennis C. numberscollected renders validate to difficult it of sunset. immedia peaks activity with times, all at collected st physiological the in differences with associated no was there that suggesting thus females, engorged Figure2: Fall, M. (Auteurdecorrespondance), Fall,A.G.,Seck, M.T.,Bouyer, J.,Diarra, M., . bolitinos C. Lasiohelae Culicoides imicola imicola Culicoides Circadianactivity of female sub-genus that was remarkably aggressive towards t towards aggressive remarkably was that sub-genus and C. pseudopallidipennis C. 10.1016/j.actatropica.2015.06.012 , collected , host-baited traps in regardless of the Comment citer cedocument: was nocturnal and its activity peaked just after su after just peaked activity its and nocturnal was

Culicoides oxystoma Culicoides peaked just after sunset and sunrise but the low low the but sunrise and sunset after just peaked this result. this rticalgrey of the time illustrate lines atus of females. females. of atus tely after sunrise, and immediately after after immediately and sunrise, after tely activity difference related to time of day day of time to related difference activity species of the of species , , C. imicola C. Forcipomyia Culicoides oxystoma oxystoma Culicoides he hosts, particularly the the particularly hosts, he host. The black, host. broken , , C. bolitinos C. nset. The activity activity The nset. genus and of of and genus , and , was was Version postprint Lancelot, R.,Gimonneau, G.,Garros, C.,Bakhoum, M.T.,Faye,O., Baldet,T.,Balenghien, T. (2015). African horse sickness and bluetongue viruses in Senegal. Acta Tropica, 149, 239-245. DOI : Host preferences and circadian rhythm of Culicoides (Diptera: Ceratopogonidae), vectors of for horse as compared to sheep. Similar host prefer host Similar sheep. to compared as horse for of preference host a showed (Diarra region the in reported been previously of predominance The Discussion sunriseand sunset. observations the of mean the represents line broken collected females of number overall i.e. subgenus, Figure 3: wasmarkedly peak diurnal and its of activity th is T 70.3%. of rate engorgement an with (12.4%), sheep 644 comp as 80.2%, ofrate engorgement an with (87.6%), collected, were specimens 735 of total A level. to unable were we and collected was male No horse. Fall, M. (Auteurdecorrespondance), Fall,A.G.,Seck, M.T.,Bouyer, J.,Diarra, M., icda atvt o fmls eogn t te unkn the to belonging females of activity Circadian 10.1016/j.actatropica.2015.06.012 C. oxystoma C. Comment citer cedocument: C. oxystoma oxystoma C. and and

C. imicola C. and Culicoides Culicoides

t al. et epre-sunset period (Figure 3). in UV-light traps and horse-baited traps has has traps horse-baited and traps UV-light in in each catch regardless of host. The black, The host. of regardless catch each in . The vertical grey lines illustrate time of of time illustrate lines grey vertical The . ence for horse was found by Viennet Viennet by found was horse for ence ared with 91 specimens collected on the the on collected specimens 91 with ared his species of the of species his 21; Fall 2014; , of which were found on the horse horse the on found were which of dniy h seies o h species the to specimens the identify species from the the from species t al. et w o the of own Lasiohelea Lasiohelea , 2015).This study study 2015).This , Avaritia

Lasiohelea Lasiohelea sub-genus sub-genus subgenus subgenus et et Version postprint Lancelot, R.,Gimonneau, G.,Garros, C.,Bakhoum, M.T.,Faye,O., Baldet,T.,Balenghien, T. (2015). African horse sickness and bluetongue viruses in Senegal. Acta Tropica, 149, 239-245. DOI : Host preferences and circadian rhythm of Culicoides (Diptera: Ceratopogonidae), vectors of rvosy osdrd sn lgt rp a hgl a highly as traps light using considered previously al. on subschultzei Fall by made observations with of predominance The Raich 1974; for attractiveness host dioxide carbon of quantity higher to corresponding impunctatus (Nelson America northern in complex Variipennis the of rate guttipennis engorgement on influence for m/s three activity all odour Almost activity: insect the with interfere disrupt also can Wind 2013). Verhulst, & (Dow i mosquitoes on conducted as colour, its or odours specific other its (CO2) i host, the of size the on dependent be can insects (Mellor regions other in and 1987) (Co Africa Sub-Saharan in nights moonless on higher i catches that reported classically is it Moreover, s of number the region, Afro-tropical the in higher so as that reported (1977) Walker and (1969) Cornet b host the to inherent factors on only not depended days. between varied collected midges of number The collected. for horse of attractiveness greater with connected th suggested sheep the and horse the between weight largest the far by being horse (the attractiveness no a was there that or hosts, other than attractive reac however not did authors The region. Palearctic al. Fall, M. (Auteurdecorrespondance), Fall,A.G.,Seck, M.T.,Bouyer, J.,Diarra, M., 19; Mushi 1996; , for (2012) Culicoides Cqilt (upry & unr 17) Cro diox Carbon 1973). Turner, & (Humphreys Coquillett et al. Cornet and Brunhes was consistently collected in ve in collected consistently was Brunhes and Cornet othbe i Soln (Bhasin Scotland in Goetghebuer associated with livestock collected by light trap light by collected livestock with associated C. imicola C. Culicoides t al. et , 1997). , 10.1016/j.actatropica.2015.06.012 C. oxystoma C. Culicoides Comment citer cedocument: 19) n i wsen fia or td) hra t whereas study) (our Africa western in and 1998) , in Kenya (Walker, 1977). Host colour does not see not does colour Host 1977). (Walker, Kenya in pce o vtrnr sgiiac uig host-bait using significance veterinary of species et al.et t al.et o ot (upry & unr 17; anr Turne & Tanner 1973; Turner, & (Humphreys hosts to in the horse-baited trap in the Niayes region was region Niayes the in trap horse-baited the in

, 1957; Edman 1957; , t al. et 21) sn te ae rp Interestingly, trap. same the using (2015) uiods sanguisuga Culicoides , 2000). Host attractiveness to haematophagous haematophagous to attractiveness Host 2000). , was suppressed at wind speeds greater than than greater speeds wind at suppressed was n light trap or on human bait were generally generally were bait human on or trap light n host). In our study, the limited difference in in difference limited the study, our In host). t al. et pecimens collected by light trap increased. increased. trap light by collected pecimens n-linear relationship between weight and and weight between relationship n-linear et al.et t has been highlighted by many studies studies many by highlighted been has t bundant in the south and eastern Africa Africa eastern and south the in bundant ts body temperature, the carbon dioxide dioxide carbon the temperature, body ts abundant most 4 the on as night temperatures were somewhat somewhat were temperatures night as on released by the host, resulted in greater in resulted host, the by released h the conclusion that horse were more more were horse that conclusion the h ut also on weather conditions. Indeed, Indeed, conditions. weather on also ut rnet, 1969; Auriault, 1979; Itoua 1979; Auriault, 1969; rnet, , 1965; Mullens, 1995) and 1995) Mullens, 1965; , The numbers collected in baited traps traps baited in collected numbers The at this difference in abundance was was abundance in difference this at , 1974; Lardeux 1974; , lw eaaig rm h hs or host the from emanating flows , 2001). Also, greater host size, size, host greater Also, 2001). , in southern Africa (VenterAfrica southern in Cqilt and Coquillett ry small numbers in studies studies in numbers small ry ide attracted specimens of of specimens attracted ide et al.et Culicoides Culicoides his species was was species his ed traps in the the in traps ed , 2007; Takken 2007; , m to have any have to m Culicoides Culicoides Culicoides Culicoides Culicoides Culicoides species species in line line in et al.et et et r, r, , , Version postprint Lancelot, R.,Gimonneau, G.,Garros, C.,Bakhoum, M.T.,Faye,O., Baldet,T.,Balenghien, T. (2015). African horse sickness and bluetongue viruses in Senegal. Acta Tropica, 149, 239-245. DOI : Host preferences and circadian rhythm of Culicoides (Diptera: Ceratopogonidae), vectors of identified as possible vector of of vector belongi possible as identified midge day-feeding of species undescribed an this of species of role the regarding available is with day the during particular in sheep, and horse the to belonging females observed We light-trapthe area collections in (Diarra (Fall st previous a During sheep. on found were engorged, nivosus C. sp these for available are characters morphological (Kremer characteristic highly as such species other (Itoua zoo-anthropophilic undoubtedly i ascanto be firmdrawn conclusions collected, no trifasciellus Culicoides numbersof pre The AHSV. of vector a as considered is it site, nocturnal.Although transmission. AHSV against protect might night the during holdings closed into Meiswinkel 1997; (Barnard, findings of activity seeking host night-time The Africanthe countries, observations supplement m to ecosystems different in preferences host on needed g this in species the of status the Brunhes,1994), al. al.et w areas of in livestock the vicinity collectionsin Africa. South in suction direct al. expla might wa which areas, reputation forested in This investigations 1994). Brunhes, & (Cornet region Fall, M. (Auteurdecorrespondance), Fall,A.G.,Seck, M.T.,Bouyer, J.,Diarra, M., , 2013) and due to the taxonomic imbroglio pertaini imbroglio taxonomic the to due and 2013) , no were there showed (2012) et al.et , 2014). Following the detection of detection the Following 2014). , , 2015), no engorged female of this species was fou was species this of female engorged no 2015), , specimen – a male – was found on the horse whereas horse the on found was – male a – specimen C. bolitinos C. . bolitinos C. 10.1016/j.actatropica.2015.06.012 C. brosseti C. was only collected in the horse-baited trap. Due t Due trap. horse-baited the in collected only was , and , theof risk AHSV being a in give transmitted, Comment citer cedocument: t al. et Leishmania enrietti enrietti Leishmania bolitinos Culicoides os o se t ue os mnr a a avl deve larval a as manure horse use to seem not does and uiods oxystoma Culicoides . subschultzei C.

, 1975). Added to this, no taxonomic keys based on on based keys taxonomic no this, to Added 1975). , et al.et C. dubitatus C. et al.et et al. Lasiohelea C. oxystoma C. . imicola C. , 2000). As this species is exophilic, enter horses enter exophilic, is species this As 2000). , , 2014). , , 1987). Its taxonomic status is uncertain as for for as uncertain is status taxonomic Its 1987). , here it is present (Oempresent is it here roup needs to be clarified. Further research is is Further research clarified. be to needs roup subgenus in virus transmission. In Australia, Australia, In transmission. virus in subgenus among the insects collected on horses by by horses on collected insects the among sence of cattle near horses may increase the the increase may horses near cattle of sence ts feeding patterns. However, this species is is species feeding However, this ts patterns. pre-sunset peak of activity. No information information No activity. of peak pre-sunset , the male specimens of specimens male the , ecies. It should also be noted that only one one only that noted be also should It ecies. recorded in our study matched previous previous matched study our in recorded ade in this study. adethis in subgenus to cause major nuisance to the to nuisance major cause to subgenus

complex to the red kangaroo ( kangaroo red the to complex and different seasons, including in other other in including seasons, different and in the Afro-tropical region (Bakhoumregion Afro-tropical the in and n hs paet imth Scheffer mismatch. apparent this in hm from them udy performed with a horse-baited trap trap horse-baited a with performed udy is regarded as abundant in light trap trap light in abundant as regarded is ng to the Schultzei group (Cornet & & (Cornet group Schultzei the to ng ng to this subgenus was recently recently was subgenus this to ng s however based on taxonomic taxonomic on based however s C. pseudopallidipennis C. nd despite a high abundance in in abundance high a despite nd 3 females, 2 of which were were which of 2 females, 3 . imicola C. etal. n area. n o the low numbers low the o C. dubitatus C. , 2013; Satheesha 2013; , bites and then then and bites are also also are Macropus Macropus loping loping being et et et et

17 15 , 77-79. 77-79. , 171-176. , Culicoides b Y & aucan, . 21) is rcr of record First (2013) K. Labuschagne, & Y. eb, ue et écologique de écologique et ue ue et écologique de écologique et ue . ontinuous activity (mostly crepuscular), and and crepuscular), (mostly activity ontinuous midges populations in the Niayes area of of area Niayes the in populations midges PLoS ONE, PLoS the European Commission. the European Commission. ominance of ominance e frt dense. forêt en é control methods. Moreover, similar work work similar Moreover, methods. control (Carpenter d behaviour of this species would provide provide would species this of behaviour é e femelles. des té cation are the sole responsibility of the the of responsibility sole the are cation due to the pattern of AHSV and BTV BTV and AHSV of pattern the to due other other ence for Orbiviruses, notably for the the for notably Orbiviruses, for ence d that night active insects will play a a play will insects active night that d eering Committee as EDENext322 EDENext322 as Committee eering 8 , 1 - 8. 8. - 1 , -2010-single-stage grant 261504 261504 grant -2010-single-stage ent of operational methods for for methods operational of ent Culicoides Culicoides C. oxystoma C. zei group of of group zei t al. et Culicoides grahamiiCulicoides Culicoides grahamiiCulicoides air OSO, serie ORSTOM, Cahiers air OSO, serie ORSTOM, Cahiers , 2008). In particular, particular, In 2008). , species - particularly particularly - species s species and its its and species s Culicoides (vs. C. imicola C. (Austen), (Austen) Latreille ), ), Version postprint Lancelot, R.,Gimonneau, G.,Garros, C.,Bakhoum, M.T.,Faye,O., Baldet,T.,Balenghien, T. (2015). African horse sickness and bluetongue viruses in Senegal. Acta Tropica, 149, 239-245. DOI : Host preferences and circadian rhythm of Culicoides (Diptera: Ceratopogonidae), vectors of pseudopunctipennis (Diptera: Ceratopogonidae)(Diptera: descriptionthewithof Afrotropical (1989) R. Meiswinkel, Ho (2007) C. B. Bouchité, & P. Loayza, F., Lardeux, (19 midge M. Matumoto, & Y. Inaba, K., Akiba, H., Kurogi, EntomologieParasitologie,médicale et C. J. Delécolle, dubitatus & C. Rebholtz-Hirtzel, M., Trouil Kremer, & G. 127-134. Vattier-Bernard, M., Africa. Central of Ceratopogonidae) Cornet, A., Itoua, Blood-fe (1973) C. E. Ceratopogonidae). J. Turner, & G. J. Humphreys, Entomology, (1990) I. J. Glick, Senegal. of area Niayes the Sec hor African of vectors T., the midges, Ceratopogonidae) Balenghien, A., Fall, M., Diarra, M., Fall, Tropicaux, & A. Mannan, kingi El Atta Culicoides R., Muller, A., K. Sinnary, El nigripalpusCulex (1974) A. A. Schmid, & A. L. Webber, D., J. Edman, dissection. without a nulliparous of recognition The (1969) L. A. Dyce, Coq. F (1957) E. R. Bellamy, & C. W. Reeves, P., R. Dow, InternationalJournal Parasitology, for as Ceratopogonidae) (Diptera: midges incriminating Harris, C., D. Holt, B., Alexander, M., A. Dougall, Senegal. of area Niayes in the viruses potential Ceratopogonidae) midges, biting(Diptera: A.,Seck,M., Diop, Fall,A.,Fall, M., M., Diarra, EntomologiqueFrance,de (D espèce afro-tropicale région des la Révision dans 1908) (1994) (Enderleini, J. Brunhes, & M. Cornet, Entomologie Parasitologie médicale et serie ORSTOM, Les (1969) M. Cornet, 175-187. Pala northwestern and U.K. the in application their C (2008) J. S. Torr, & S. P. Mellor, S., Carpenter, species. Ceratopogoaidae) stu taxonomic A (1979) O. O. Dipeolu, & J. Boorman, importance. and veterinary medical their (1989) J. Boorman, 156. the midge biting governing the factors (2001) W. Mordue, Some & J. A. Luntz, Mordue A., Bhasin, (1997) H. stables. into Ceratopogonidae) J. B. Barnard, Fall, M. (Auteurdecorrespondance), Fall,A.G.,Seck, M.T.,Bouyer, J.,Diarra, M., AmericanJournal ofTropical Medicineand Hygiene, Culicoidesoxystoma . p (itr: eaoooia) e a éin éth région la de Ceratopogonidae) (Diptera: sp. n. 38 27 , 270-275. 270-275. , , 85-195. 85-195. , n oten Sudan. northern in when offered a choice of blood sources. sources. blood of choice a offered when Culicoides uiods impunctatus Culicoides JournalofMedical Entomology, JournalAustralianof the Entomological Society, in a village of the Andean valleys of Bolivia. Bolivia. of Andean the valleys of invillage a Culicoides Culicoides 10.1016/j.actatropica.2015.06.012 Comment citer cedocument: 92 inJapan. OccasionalPublications Entomologicalof the Societ Parasites & Vectors, & Parasites biting midges (Diptera: Ceratopogonidae) of Kenya. of Ceratopogonidae) (Diptera: midges biting , 149-164. 149-164. , Dpea Crtpgnde o te rba peninsul Arabian the of Ceratopogonidae) (Diptera: Onderstepoort JournalResearch, Onderstepoort ofVeterinary (Diptera: Ceratopogonidae) de l'Ouest Africain (1e Africain l'Ouest de Ceratopogonidae) (Diptera: Culicoides Veterinary Microbiology, Veterinary Cahiers ORSTOM, serie Entomologie médicale et Paras et médicale Entomologie serie ORSTOM, Cahiers Parasites & Vectors, & Parasites 41

13 13 , 571-579. 571-579. , eu dEeae t e éeie ééiar ds Pays des Vétérinaire Médecine de et d'Elevage Revue FaunaofSaudi Arabia, 233-236. 233-236. n Scotland. in Garros, C. : a redescription of of redescription a : 8 T., Sultan, A. H., Bates, P. A. P. Bates, H., A. Sultan, T., , 39. 39. , ontrol techniques for techniques ontrol , . Bue, J. Bouyer, M., k, ield tests of avian host preference of preference host avian of tests ield 10 closely alliedclosely Effect of host defences on the feeding pattern of pattern feeding the on defences host of Effect vectors of African horse sickness and bluetonguesicknessandhorse African of vectors nd parous nd pea Ceratopogonidae). iptera: st choice and human blood index of of index blood human and choice st earctic. se sickness virus - a host/vector contact study in study contact host/vector a - virus sickness se Nigerian adult of dy Field studies on efficacy of host odour baits for baits odour host of efficacy on studies Field 17) ecito due sèe nouvelle espèce d'une Description (1975) , 79-83. 79-83. , 7 Ioain f kbn vrs rm h biting the from virus Akabane of Isolation 87) usi, . . 18) h dunl ciiy of activity diurnal The (1985) H. S. Hussein, , 7 potential vectors of of vectors potential dn atvt o female of activity eding eia ad eeiay Entomology, Veterinary and Medical , 341-364. 341-364. , , et al.et , 6 de s 7 , 294-303. 294-303. , JournalofParasitology, e, . 18) The (1987) J. let, , 147. 147. , Medical and Veterinary Entomology,Veterinary and Medical 15 entry of of entry (2014) Seasonaldynamics(2014)of Culicoides Culicoides Malaria Journal,Malaria , 243-248. 243-248. , 10 C . ( . iopienne. , 160-224. 160-224. , . Aaii) imicola (Avaritia) C. e al. et , 8 Avaritia , 11-15. 11-15. , Culicoides (Diptera: Ceratopogonidae) (Diptera: paete à apparentées Culicoides (2015) Culicoides ) ) Leishmania air OSO, serie ORSTOM, Cahiers bolitinossp 64 , et al.et , y ofNigeria,y ultn e a Société la de Bulletin , 227-233. 227-233. , 6 Culicoides Culicoides

Culicoides , 14. 14. , 60 biting midges and midges biting Journal of Medical of Journal Latreille (Diptera:Latreille , 874-883. 874-883. , re note). re (2011) Evidence (2011) a with notes on on notes with a p. (Diptera: spp. ife, 1913 Kieffer, n Australia. in Culex tarsalisCulex . Nov. rearedNov.. 22 . shultzei C. (Diptera: Anopheles (Diptera: Culicoides (Diptera: 15 , 1-121. 1-121. , itologie Cahiers 147- , 22 C. , ,

Version postprint Lancelot, R.,Gimonneau, G.,Garros, C.,Bakhoum, M.T.,Faye,O., Baldet,T.,Balenghien, T. (2015). African horse sickness and bluetongue viruses in Senegal. Acta Tropica, 149, 239-245. DOI : Host preferences and circadian rhythm of Culicoides (Diptera: Ceratopogonidae), vectors of AnnualofEntomology, Review JournalResearch, ofVeterinary Entomology, Hostpreference(2013) Verhulst,N.O. & W. Takken, po midge in prevalence Parasitology, Veterinary virus sickness horse African Pa K., Labuschagne, al. J., G. Venter, G., E. Scheffer, buffaloes. with associated midges & M. M. Appannavar, G., K. Udupa, P., S. Satheesha, Entomology, Veterinary D. M. Ortega, & I. imicolaCulicoides Pena, J., M. Pro, P., Rawlings, inColora selection host Ceratopogonidae) (Diptera: R., Babion, F., Holbrook, M., Jacobson, T., Raich, and language Vienna,Computing, Austr Statistical Foundationfor A 3.1.1: version R (2014) R_Core_Team. IndianFarming, Bluetongue: (1999) Sushila. & Y. Malik, G., Prasad, Science, Veterinary Ceratopogonidae, (Diptera: species midge K., T. Kim, S., M. Kwon, Y., J. Chung, K., J. Oem, area. same in the vectors be may togetherBritishCameroons, the rain-forest of the ofbionomicsThe (1953) M. W. Nicholas, 56-57. Carbon(1965) L. R. Nelson, anattractanas dioxide models. linearmixed-effects and general A (2013) H. Schielzeth, & S. Nakagawa, Mogodits at horses Communications, Research with associated M Binta, G., Ceratopogonidae) R. Chabo, W., F. J. Isa, Z., E. Mushi, 310-315. response and activity Flight sonorensis (1995) A. B. Mullens, Israel. phylogeneticstatus and geographic distribution of E. Klement, Y., Bravermann, Y., Saroya, N., Morag, Culicoides (1984) M. D. Jennings, & R. Osborne, S., P. Mellor, si African horse Hamblin, S.C.(2004) & P. Mellor, (2000) M. Baylis, & J.Boorman, S., P. Mellor, inAfrica.South sickness for Evidence (2003) T. J. Paweska, & R. Meiswinkel, BulletinofEntomological Research, (2000) bolitinos K. Culicoides Labuschagne, & M. Baylis, R., Meiswinkel, Research, ofVeterinary to allied closely Afrotropical (1991) R. Meiswinkel, wildebee blue buffalo, african the of dung the from Fall, M. (Auteurdecorrespondance), Fall,A.G.,Seck, M.T.,Bouyer, J.,Diarra, M., 21) oprsn f w tapn mtos for methods trapping two of Comparison (2012) PLoS ONE, PLoS spp.Sudan.in the Dpea Crtpgnde i suhr California. southern in Ceratopogonidae) (Diptera: 58 , 433-453. 433-453. , 49 C 7 . ( . in Iberia in relation to the transmission of Afric transmissionof the to relation Iberiain in , e33610. e33610. , , 16-20. 16-20. , 14 (Diptera: Ceratopogonidae), a recently identifiedrecently Ceratopogonidae),a (Diptera: Avaritia , 91-94. 91-94. , 58 10.1016/j.actatropica.2015.06.012 11 185 Preventive Veterinary Medicine, Veterinary Preventive Comment citer cedocument: , 155-170. 155-170. , , 49-57. 49-57. , 22 ) ) , 265-273. 265-273. , imicola JournalofHygiene, Methods inEcology Methods and Evolution, , 295-297. 295-297. , 45 56 , 307- 340. 340. 307- , , 23-39. 23-39. , AnnalsofTropical Medicineand Parasitology, BuffaloBulletin, 90 Kieffer, 1913 (Diptera: Ceratopogonidae).(Diptera: 1913 Kieffer, Culicoides , 509-515. 509-515. ,

Culicoides austeniCulicoides Culicoides Culicoides : : C. 93 ckness. ckness. ( Blair, C. & Beaty, B. J. (1997) J. B. Beaty, & C. Blair, Lee, T. U. & Bae, Y. C. (2013) Abundance of biting of Abundance (2013) C. Y. Bae, & U. T. Lee, 33 , 621-628. 621-628. , t for t with notes on on noteswith G & aat, . . (1998) W. R. Kapaata, & G. . Culicoidesoxystoma an alarming disease to livestock industry in India in industry livestock to disease alarming an Avaritia Isolation of bluetongue and related viruses from viruses related and bluetongue of Isolation ia. do. simple method for obtaining R² from generalized from R² obtaining for method simple e P C, uln, . . Mcaha, . J. N. MacLachlan, A., B. Mullens, C., P. ge, s of blood-feeding of smosquitoes. , 400-406. 400-406. , a e field new a . 19) pta ad esnl itiuin of distribution seasonal and Spatial (1997) C. Culicoides Gtle, . 21) oeua identification, Molecular (2012) Y. Gottlieb, & Labuschagne, K. (2014) A study on on study A (2014) K. Labuschagne, ULR: http://www.R-project.org/ ULR: tbig n te rtcin f oss from horses of protection the and Stabling spp.) on cattle farms in Korea. Korea. in farms cattle on spp.) t n ctl i Suh Africa. South in cattle and st Culicoides biting midges: their role as arbovirus vectors.arbovirus as role their midges: biting JournalofMedical Entomology, to carbon-dioxide of of carbon-dioxide to 60 uain a Odrtpot Suh Africa. South Onderstepoort, at pulations Veterinary Research, Veterinary environment for statistical computing. R R computing. statistical for environment , 243-253. 243-253. , ) ) , vector of vector , ae Gbrn, Botswana. Gaborone, hane, miombo 4 iig igs n dtriain of determination and midges biting

, 133-142. 133-142. , C. grahamiiC. an horse sicknessvirus.horse an ora o Mdcl Entomology, Medical of Journal . JournalEntomology, ofEconomic Culicoides vector of African horse sickness.horse African of vector p nv, wdsra species widespread a nov., sp. Acanthocheilonemaperstans (Diptera: Ceratopogonidae)in and other species whichspecies other and vco f fia horse African of vector 35 Onderstepoort Journal Onderstepoort uiods variipennis Culicoides 47 Culicoides variipennisCulicoides , 445-466. 445-466. , Culicoides , 187-206. 187-206. , Annual Review ofAnnualReview . Onderstepoort 34 Medicaland , 247-249. 247-249. , ora of Journal Veterinary Culicoides (Diptera: et , 32 2 in . , ,

species for virus serotypes 3, 5 and 8. 8. and 5 3, forserotypes virus species . Culicoides Mosquito News,Mosquito Culicoides lemant, M. (1986) Les Ceratopogonidae (Diptera) du (Diptera) Ceratopogonidae Les (1986) M. lemant, , S., Yamakawa, M.Yamakawa, S., , tivities and host preferences of several of preferences host and tivities pce fr h Byntn eoye f equine of serotype Bryanston the for species . Aln, . Lneo, R. Lancelot, X., Allene, I., 61 drtpot ra Gueg Suh fia as Africa South Gauteng, area, nderstepoort e fmle de femelles des ne, . . Hwl, . . 19) Vector (1999) G. P. Howell, & H. E. enter, 13 species (Diptera: Ceratopogonidae) in Kenya. in Ceratopogonidae) (Diptera: species rcn os scns eieilg: vector epidemiology: sickness horse frican , 367-377. 367-377. , 34 , 393-400. 393-400. , ig ml iscs n irsoe lds in slides microscope on insects small ting , 66-70. 66-70. , d, . (1996) M. rds, 61 , 783-784. 783-784. , , et al.et , uiods grahamiiCulicoides (2005) Isolation of bovine of Isolation (2005) Medical and Veterinary Veterinary Medicaland rn Japan: 1985-2002. Japan: rn Culicoides e al. et , 63 , 315-325. 315-325. , 21) Host (2012) (Diptera: Culicoides biviruses. Austen,