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A review of species diversity and distribution of Culicoides Latreille, 1809 (Diptera: Ceratopogonidae) in Turkey

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This paper reviews the species composition and distribution of Culicoides biting midges in Turkey for the first time. The Culicoides fauna of Turkey is diverse, with 57 reported species collected in 54 localities across the Marmara, Aegean,
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  A review of species diversity and distribution of   Culicoides Latreille, 1809 (Diptera: Ceratopogonidae) in Turkey BILAL DIK  1 , S¸U¨ KRAN YAG˘ CI 2 & YVONNE-MARIE LINTON 3 1 Selc¸uk University, Faculty of Veterinary Medicine, Department of Parasitology, Konya, Turkey, 2  Ankara University, Faculty of Veterinary Medicine, Department of Parasitology, Ankara, Turkey,and   3 Department of Entomology, Natural History Museum, Cromwell Road, London, UK  (  Accepted 29 September 2006) Abstract This paper reviews the species composition and distribution of   Culicoides  biting midges in Turkey forthe first time. The  Culicoides  fauna of Turkey is diverse, with 57 reported species collected in 54localities across the Marmara, Aegean, Mediterranean, and Central, Eastern and SoutheasternAnatolian Regions of Turkey. No records are available for the Black Sea Region. The mostwidespread species include  Culicoides cataneii   Clastrier,  C. circumscriptus  Kieffer,  C. festivipennis Kieffer,  C. gejgelensis  Dzhafarov,  C. longipennis  Khalaf,  C. maritimus  Kieffer,  C. nubeculosus  (Meigen), C. obsoletus  (Meigen),  C. odiatus  Austen,  C. pulicaris  (Linnaeus),  C. puncticollis  (Becker),  C. saevus Kieffer, and  C. shaklawensis  Khalaf, whereas  C. denisoni   Boorman,  C. dewulfi   Goetghebuer,  C. fagineus Edwards,  C. minutissmus  (Zetterstedt),  C. montanus  Schakirzjanova,  C. semimaculatus  Clastrier,  C.slovacus  Orszagh, and  C. turanicus  Gutsevich and Smatov are represented from only one locality. Onlysingle specimens represent the country records of   C. dewulfi   and  C. seifadinei  . The potential of Turkish Culicoides  in zoonotic arbovirus, protozoa, and nematode transmission is discussed. Keywords:  Biting midges,  Culicoides  species, distribution, faunal list, Turkey, vector  Introduction Bluetongue is an infectious, non-contagious, and often lethal disease in domestic ruminantsincluding sheep, goats, and cattle that is endemic in tropical latitudes worldwide.Bluetongue is transmitted via the bites of some  Culicoides  biting midges and thus it followsthat the disease is present only where populations of competent vectors exist. Rangeexpansion of the major Old World vector,  Culicoides imicola  Kieffer, is believed to be akey factor in the changes in bluetongue epidemiology in the Mediterranean basin(Mellor and Wittman 2002).  Culicoides imicola  s.s. has expanded from Afrotropical zonesand now exists in stable populations in countries surrounding the Mediterranean,including Turkey, below 40 u N latitude. The first outbreak of bluetongue in Turkey(serotype 4) was reported from Aydın province in western Turkey in 1977. The diseaseoverwintered and the outbreak lasted through to 1981 (Yonguc¸ et al. 1982; Jennings et al. Correspondence: Bilal Dik, Selc¸uk University, Faculty of Veterinary Medicine, Department of Parasitology, 42031 Campus,Konya, Turkey. Email: bdik@selcuk.edu.trPublished 4 December 2006  Journal of Natural History , 2006; 40(32–34): 1947–1967 ISSN 0022-2933 print/ISSN 1464-5262 online # 2006 Taylor & FrancisDOI: 10.1080/00222930601046634  1983). The Imicola Group comprises some eight described species (with an additional fourremaining to be formally described), including  C. imicola  s.s., the major Afrotropical andMediterranean vector of bluetongue (Meiswinkel and Linton 2003). Despite severalmolecular studies on the composition of this complex in the Mediterranean Basin(including Italy, Greece, north Africa and Israel), only  C. imicola  s.s. has been detectedto date (Sebastiani et al. 2001; Linton et al. 2002; Dallas et al. 2003), suggesting thatthe species acting as a vector of bluetongue in Turkey is also likely to comprise only C. imicola  s.s.Prior to the 1980s outbreaks of bluetongue in Europe were restricted to theMediterranean Basin and were short and sporadic. In contrast, from 1998 anunprecedented continuous outbreak of bluetongue has affected central Europe and thecountries of the Mediterranean Basin resulting in the deaths of over 800,000 sheep, andmaking this the longest and most economically devastating outbreak of bluetongue in livinghistory. Countries affected in this outbreak include: Algeria, Bulgaria, Bosnia-Herzegovina,Cyprus, Croatia, the French island of Corsica, Greece (and the Greek islands of Kos,Rhodes, Chios, Evia, Lesbos, Skiathos, Skopelos, and Samos), Israel, Italy (and the Italianislands of Sicily and Sardinia), Kosovo, Macedonia, Morocco, the Spanish islands of Majorca and Menorca, Tunisia, Turkey, and Yugoslavia (see OIE World Organisation forAnimal Health website, http://www.oie.int).Common European farmyard species including the  C. obsoletus  and  C. pulicaris  speciescomplexes have long been suspected to act as arbovirus vectors due to their widespreadabundance, and associated high densities around domestic livestock. Members of the  C.obsoletus  group are almost impossible to differentiate as adult females and thus references inthe literature to  C. obsoletus  almost always refer to the  C. obsoletus  group, which includes  C.chiopterus  (Meigen),  C. dewulfi   Goetghebuer,  C. montanus  Shakirzjanova,  C. obsoletus (Meigen),  C. scoticus  Downes and Kettle, and up to two further as yet undescribed species(Gomulski et al. 2005). At the same time that De Liberato et al. (2005) isolated BTV-2from non-engorged parous  C. obsoletus  females caught alongside  C. imicola , BTV-2 andBTV-9 serotypes were isolated from mixed pools of   C. obsoletus  and  C. scoticus  collectedfrom bluetongue outbreak zones in Italy, where no  C. imicola  was reported (Savini et al.2005). Carpenter et al. (2006) showed differential bluetongue vector capacity inpopulations of   C. obsoletus  s.l. and  Culicoides pulicaris  s.l. in the UK, but showed that inthe most susceptible populations of infection prevalence was comparable with that of   C.imicola , using the same viral strain and feeding method.Given the socioeconomic and veterinary importance of the genus  Culicoides  and theobvious pressures to identify the vectors of the ongoing bluetongue outbreak, this paperattempts to succinctly review published works (written both in English and Turkish) tocomprehensively document the species composition and distribution of   Culicoides  bitingmidges in Turkey for the first time. Results and discussion Species composition Early literature on the  Culicoides  fauna of Turkey prior to the 1977–81 bluetongue outbreakis very scanty. The first documented records of   Culicoides  in Turkey came in the form of twonew species descriptions by Kieffer (1918):  C. albonotatus  Kieffer later became a juniorsynonym of   C. fascipennis  (Staeger), whilst  C. nadayanus  Kieffer was subsequentlysynonomized with  C. circumscriptus  Kieffer. A single male specimen of   Culicoides parroti  1948  B. Dik et al.  Kieffer from Turkey was reported in a textbook of British haematophagous insects(Edwards et al. 1939). Later, Oytun (1945) wrote a short paper highlighting the potentialbiomedical importance and systematics of the genus  Culicoides  but he did not report whichspecies were present in Turkey. In later studies of blood-sucking flies, Mimiog˘lu (1961)reported collecting a number of   Culicoides  species from southeastern Turkey, but did notidentify them to species. In 1965, Unat reconfirmed the presence of   C. circumscriptus  and  C. parroti   and Leclercq (1966) reported  C. punctatus  (Meigen) for the first time, feeding inhigh numbers on a horse in Kus¸adası on the Aegean coast.Serious efforts to document and identify  Culicoides  species in Turkey began with Navai’sPhD thesis (1977), where she documented the presence of 19  Culicoides  species from theAegean (AE), Mediterranean (ME) and South-Eastern Anatolian (SO) Regions in Turkey(TableI; Figure1). With the exception of   C. circumscriptus , all 18 others comprised newcountry records as follows:  C. bulbostylus  Khalaf,  C. dewulfi   Goetghebuer,  C. festivipennis Kieffer (as  C. odibilis  Austen),  C. furcillatus  Callot, Kremer and Paradis,  C. ibericus Dzhafarov,  C. kurensis  Dzhafarov,  C. longipennis  Khalaf,  C. maritimus  Kieffer,  C.minutissmus  (Zetterstedt) (as  C. tugaicus  Dzhafarov),  C. montanus  Schakirzjanova,  C.nubeculosus  (Meigen),  C. obsoletus  (Meigen),  C. odiatus  Austen,  C. pictipennis  (Staeger), C. pulicaris  (Linnaeus),  C. puncticollis  (Becker),  C. saevus  Kieffer, and  C. schultzei  (Enderlein) (TableI). Although a description is written in the srcinal text (Navai 1977,p30), Navai inadvertently missed out the single male specimen of   C. dewulfi   found inAdana, Turkey from her summary table of species distributions (Navai 1977, p121–122,Table6) and this error has been perpetuated by all later authors who cite, incorrectly, that18 rather than 19 species were found in this study (e.g. Jennings et al. 1983). Culicoides  surveillance was undertaken in the Aegean (Aydın, C¸akmak, Nazilli, andSalihag˘a; and Mediterranean Region (Antalya) in direct response to the bluetongueoutbreak of 1978–81 (Jennings et al. 1983). Light traps set in the outbreak zone revealed  C.imicola  for the first time, amongst 18 species collected. Besides  C. imicola , a further fivewere previously unreported in Turkey ( C. dzhafarovi   Remm,  C. gejgelensis  Dzhafarov,  C.newsteadi   Austen,  C. subneglectus  Vimmer, and  C. vidourlensis  Callot, Kremer, Molet andBach) (TableI) (Jennings et al. 1983). Dik (1989) collected 14,098  Culicoides  comprising35 species around the city of Konya, in the Central Anatolian Region (CE, Figure1).Seventeen of these were new country records as follow:  C. achrayi   Kettle and Lawson,  C.cataneii   Clastrier,  C. duddingstoni   Kettle and Lawson,  C. fagineus  Edwards,  C. flavipulicaris Dzhafarov,  C. heliophilus  Edwards,  C. kibunensis  Tokunaga,  C. pallidicornis  Kieffer,  C. picturatus  Kremer and Deduit,  C. pumilus  (Winnertz),  C. riethi   Kieffer,  C. scoticus  Downesand Kettle,  C. shaklawensis  Khalaf,  C. simulator   Edwards,  C. tauricus  Gutsevich,  C.truncorum  Edwards, and  C. vexans  (Staeger) (TableI) (Dik 1989). Collecting in southernTurkey, Burgu et al. (1992) and Dik (1993) reported 13 and 22 species, respectively,including new country records for  C. sahariensis  Kieffer and  C. subneglectus  Vimmer (Burguet al. 1992), and  C. denisoni   Boorman (Dik 1993) (TableI). In 1994, Yılmaz reported 42species from the Elazıg˘ province (Eastern Anatolian Region (EA), Figure1)—the highestdiversity in any publication on Turkish  Culicoides  —including seven new country records for C. azerbajdzhanicus  Dzhafarov,  C. badooshensis  Khalaf,  C. kolymbiensis  Boorman,  C.reconditus  Campbell and Pelham-Clinton,  C. sejfadinei   Dzhafarov,  C. semimaculatus Clastrier, and  C. slovacus  Orszagh (TableI). Dik (1996) reported  C. salinarius  Kiefferand  C. turanicus  Edwards as new country records amongst 31 species collected from theAegean Region (AE) of western Turkey (Aydın, Denizli, I˙zmir, Ku¨tahya, and Mug˘laprovinces), completing the current Turkish species list of 57 species. Dik (1997) discussed Species diversity and distribution of   Culicoides 1949  Table I. Faunal list and known distribution of biting midges of the genus  Culicoides  (Diptera: Ceratopogonidae) of Turkey based on published data (Kieffer 1918; Edwards et al. 1939; Leclercq 1966; Navai 1977; Jennings et al.1983; Dik 1989; Burgu et al. 1992; Dik 1993, 1996; Yılmaz 1994; Eren et al. 1995; Yag˘cı et al. 1999; Eren andI˙nci 2002; Tilki and Dik 2003; Uslu 2003). Culicoides  species Locality Map Specimens Source C. achrayi   Kettle andLawson, 1955Baskil EA 7 122 R , 13 „  Yılmaz 1994Elazıg˘ EA 22 1 R  Yılmaz 1994Kazan CE 34 3 R  Eren et al. 1995Kadınhanı CE 31 1 R  Dik 1989Keban EA 35 64 R , 45 „  Yılmaz 1994Kovancılar EA 37 40 R , 8 „  Yılmaz 1994Maden EA 40 1 R  Yılmaz 1994Sivrice EA 50 1 R  Yılmaz 1994 C. azerbajdzhanicus Dzhafarov, 1962Baskil EA 7 47 R , 33 „  Yılmaz 1994Elazıg˘ EA 22 3 R  Yılmaz 1994Keban EA 35 43 R , 76 „  Yılmaz 1994Kovancılar EA 37 18 R , 43 „  Yılmaz 1994 C. badooshensis  Khalaf, 1961 Elazıg˘ EA 22 1 R , 1 „  Yılmaz 1994Kovancılar EA 37 20 R , 13 „  Yılmaz 1994Maden EA 40 2 „  Yılmaz 1994Salihag˘a AE 46 1 R  Dik 1996So¨ke AE 51 1 R  Dik 1996 C. bulbostylus Khalaf  , 1961 Diyarbakır SO 20 6 R , 11 „  Navai 1977Salihag˘a AE 44 2 R  Dik 1996 C. cataneii  a Clastrier, 1957 Adana ME 1 1 R  Dik 1993Aks¸ehir CE 2 2 R  Dik 1989Baskil EA 7 21 R , 1 „  Yılmaz 1994Beys¸ehir CE 10 1 R  Dik 1989Elazıg˘ EA 22 3 R  Yılmaz 1994Gemlik MA 25 3 R  Eren and I˙nci 2002Go¨lbas¸ı CE 27 5 R  Eren et al. 1995Hadim CE 28 2 R  Dik 1989Kadınhanı CE 31 1 R  Dik 1989Kazan CE 34 8 R  Eren et al. 1995Keban EA 35 29 R , 6 „  Yılmaz 1994Konya CE 36 7 R , 1 „  Uslu 2003Kovancılar EA 37 14 R , 4 „  Yılmaz 1994Maden EA 40 6 R  Yılmaz 1994So¨ke AE 51 1 R  Dik 1996Simav AE 49 1 R  Dik 1996Umurlu AE 54 4 R  Yag˘cı et al. 1999S. Turkey a ME ? b Burgu et al. 1992 C. circumscriptus a Kieffer, 1918 Adana ME 1 1 R ; 21 R , 4 „  Navai 1977; Dik 1993Syn:  C. nadayanus  Aks¸ehir CE 2 170 b Dik 1989Kieffer, 1918 Anamur ME 3 4 R , 2 „  Dik 1993Syn:  C. edwardsi   Ankara CE 4 3 b  Jennings et al. 1983Goetghebuer, 1921 Antalya ME 5 129 b ; 3 R  Jennings et al. 1983;Syn:  C. algarum  Dik 1993Kieffer, 1924 Baskil EA 7 283 R , 26 „  Yılmaz 1994Syn:  C. pictidorsum  (as variety of Bergama AE 8 21 R , 9 „  Dik 1996 C. salicola ) Kieffer, 1924 Beys¸ehir CE 10 9 b Dik 1989Syn:  C. albonotatus  Bornova AE 11 31 R , 17 „ ; 44 R , Navai 1977; Dik 1996Vimmer, 1932 53 „ 1950  B. Dik et al.  Culicoides  species Locality Map Specimens SourceSyn:  C. albosignatus  Bozkır CE 12 32 b Dik 1989Vimmer, 1932 C¸ig˘li AE 16 10 R , 2 „  Navai 1977Syn:  C. polymaculatus  Cihanbeyli CE 14 73 b Dik 1989Vimmer, 1932 C¸umra CE 10 133 b Dik 1989Syn:  C. pulcher   Denizli AE 19 2 R  Dik 1996Zihali-Sebess, 1934 Elazıg˘ EA 22 61 R , 48 „  Yılmaz 1994Syn:  C. kirovabadicus  Ereg˘li CE 24 15 b Dik 1989Dzhafarov, 1964 Gemlik MA 25 125 R , 26 „  Eren and I˙nci 2002Go¨kc¸ekısık CE 26 1 R  Kieffer 1918Go¨lbas¸ı CE 27 61 R , 9 „  Eren et al. 1995Hadim CE 28 5 b Dik 1989I˙skenderun ME 29 5 R  Tilki and Dik 2003I˙zmir AE 30 51 R , 77 „  Navai 1977Karaman CE 33 25 b Dik 1989Kazan CE 34 320 R , 20 „  Eren et al. 1995Keban EA 35 112 R , 43 „  Yılmaz 1994Kovancılar EA 37 764 R , 385 „  Yılmaz 1994Konya CE 36 7 b ; 409 b ; 736 R ,614 „  Jennings et al. 1983;Dik 1989; Uslu 2003Kuyucak AE 39 4 R  Dik 1996Maden EA 40 10 R , 3 „  Yılmaz 1994Mug˘la AE 42 2 R  Dik 1996Pirinc¸lik SO 45 7 R , 9 „  Navai 1977Salihag˘a AE 46 2 b ; 62 R , 5 „  Jennings et al. 1983;Dik 1996Serik ME 47 37 R , 6 „  Dik 1993Seydis¸ehir CE 48 107 b Dik 1989Simav AE 49 37 R , 2 „  Dik 1996Sivrice EA 50 11 R , 1 „  Yılmaz 1994So¨ke AE 51 8 R  Dik 1996Tarsus ME 52 15 R , 5 „  Dik 1993Tire AE 53 1 R  Navai 1977Umurlu AE 54 54 R , 4 „  Yag˘cı et al. 1999S. Turkey a ME ? b Burgu et al. 1992 C. denisoni   Boorman, 1988 Serik ME 47 3 R  Dik 1993 C. dewulfi   Goetghebuer, 1936 Adana ME 1 1 „  Navai 1977Syn:  C. pseudochipterus Downes and Ketle, 1952 C. duddingstoni   Kettle Beys¸ehir CE 10 1 „  Dik 1989and Lawson, 1955 Ereg˘li CE 24 2 „  Dik 1989Karaman CE 33 1 „  Dik 1989Salihag˘a AE 46 1 R , 1 „  Dik 1996Simav AE 49 1 „  Dik 1996 C. dzhafarovi   Remm, 1967 Adana ME 1 4 R  Dik 1993Syn:  C. dzhafavovi   Callot, Anamur ME 3 2 R  Dik 1993Kremer, Molet andBach, 1968Antalya ME 5 13 b ; 108 R  Jennings et al. 1983;Dik 1993Aks¸ehir CE 2 5 R  Dik 1989Baskil EA 7 601 R , 263 „  Yılmaz 1994Beys¸ehir CE 10 6 R  Dik 1989Cihanbeyli CE 14 20 R  Dik 1989Elazıg˘ EA 22 227 R , 112 „  Yılmaz 1994Ereg˘li CE 24 8 R  Dik 1989Table I. Continued. Species diversity and distribution of   Culicoides 1951
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