A review of species diversity and distribution of Culicoides Latreille, 1809 (Diptera:...

A review of species diversity and distribution of Culicoides

Latreille, 1809 (Diptera: Ceratopogonidae) in Turkey

BILAL DIK1, SUKRAN YAGCI2 & YVONNE-MARIE LINTON3

1Selcuk University, Faculty of Veterinary Medicine, Department of Parasitology, Konya, Turkey,2Ankara University, Faculty of Veterinary Medicine, Department of Parasitology, Ankara, Turkey,

and 3Department of Entomology, Natural History Museum, Cromwell Road, London, UK

(Accepted 29 September 2006)

AbstractThis 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. festivipennisKieffer, 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. saevusKieffer, and C. shaklawensis Khalaf, whereas C. denisoni Boorman, C. dewulfi Goetghebuer, C. fagineusEdwards, 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 TurkishCulicoides 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 ruminants

including 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 follows

that the disease is present only where populations of competent vectors exist. Range

expansion of the major Old World vector, Culicoides imicola Kieffer, is believed to be a

key factor in the changes in bluetongue epidemiology in the Mediterranean basin

(Mellor and Wittman 2002). Culicoides imicola s.s. has expanded from Afrotropical zones

and now exists in stable populations in countries surrounding the Mediterranean,

including Turkey, below 40uN latitude. The first outbreak of bluetongue in Turkey

(serotype 4) was reported from Aydın province in western Turkey in 1977. The disease

overwintered and the outbreak lasted through to 1981 (Yonguc et al. 1982; Jennings et al.

Correspondence: Bilal Dik, Selcuk University, Faculty of Veterinary Medicine, Department of Parasitology, 42031 Campus,

Konya, Turkey. Email: [email protected]

Published 4 December 2006

Journal of Natural History, 2006; 40(32–34): 1947–1967

ISSN 0022-2933 print/ISSN 1464-5262 online # 2006 Taylor & Francis

DOI: 10.1080/00222930601046634

1983). The Imicola Group comprises some eight described species (with an additional four

remaining to be formally described), including C. imicola s.s., the major Afrotropical and

Mediterranean vector of bluetongue (Meiswinkel and Linton 2003). Despite several

molecular 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 detected

to date (Sebastiani et al. 2001; Linton et al. 2002; Dallas et al. 2003), suggesting that

the 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 the

Mediterranean Basin and were short and sporadic. In contrast, from 1998 an

unprecedented continuous outbreak of bluetongue has affected central Europe and the

countries of the Mediterranean Basin resulting in the deaths of over 800,000 sheep, and

making this the longest and most economically devastating outbreak of bluetongue in living

history. 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 Italian

islands of Sicily and Sardinia), Kosovo, Macedonia, Morocco, the Spanish islands of

Majorca and Menorca, Tunisia, Turkey, and Yugoslavia (see OIE World Organisation for

Animal Health website, http://www.oie.int).

Common European farmyard species including the C. obsoletus and C. pulicaris species

complexes have long been suspected to act as arbovirus vectors due to their widespread

abundance, and associated high densities around domestic livestock. Members of the C.

obsoletus group are almost impossible to differentiate as adult females and thus references in

the 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-2

from non-engorged parous C. obsoletus females caught alongside C. imicola, BTV-2 and

BTV-9 serotypes were isolated from mixed pools of C. obsoletus and C. scoticus collected

from bluetongue outbreak zones in Italy, where no C. imicola was reported (Savini et al.

2005). Carpenter et al. (2006) showed differential bluetongue vector capacity in

populations of C. obsoletus s.l. and Culicoides pulicaris s.l. in the UK, but showed that in

the 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 the

obvious pressures to identify the vectors of the ongoing bluetongue outbreak, this paper

attempts to succinctly review published works (written both in English and Turkish) to

comprehensively document the species composition and distribution of Culicoides biting

midges 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 outbreak

is very scanty. The first documented records of Culicoides in Turkey came in the form of two

new species descriptions by Kieffer (1918): C. albonotatus Kieffer later became a junior

synonym of C. fascipennis (Staeger), whilst C. nadayanus Kieffer was subsequently

synonomized 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 potential

biomedical importance and systematics of the genus Culicoides but he did not report which

species were present in Turkey. In later studies of blood-sucking flies, Mimioglu (1961)

reported collecting a number of Culicoides species from southeastern Turkey, but did not

identify 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 in

high numbers on a horse in Kusadası on the Aegean coast.

Serious efforts to document and identify Culicoides species in Turkey began with Navai’s

PhD thesis (1977), where she documented the presence of 19 Culicoides species from the

Aegean (AE), Mediterranean (ME) and South-Eastern Anatolian (SO) Regions in Turkey

(Table I; Figure 1). With the exception of C. circumscriptus, all 18 others comprised new

country 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) (Table I). Although a description is written in the original text (Navai 1977,

p 30), Navai inadvertently missed out the single male specimen of C. dewulfi found in

Adana, Turkey from her summary table of species distributions (Navai 1977, p 121–122,

Table 6) and this error has been perpetuated by all later authors who cite, incorrectly, that

18 rather than 19 species were found in this study (e.g. Jennings et al. 1983).

Culicoides surveillance was undertaken in the Aegean (Aydın, Cakmak, Nazilli, and

Salihaga; and Mediterranean Region (Antalya) in direct response to the bluetongue

outbreak 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 five

were previously unreported in Turkey (C. dzhafarovi Remm, C. gejgelensis Dzhafarov, C.

newsteadi Austen, C. subneglectus Vimmer, and C. vidourlensis Callot, Kremer, Molet and

Bach) (Table I) (Jennings et al. 1983). Dik (1989) collected 14,098 Culicoides comprising

35 species around the city of Konya, in the Central Anatolian Region (CE, Figure 1).

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 Downes

and Kettle, C. shaklawensis Khalaf, C. simulator Edwards, C. tauricus Gutsevich, C.

truncorum Edwards, and C. vexans (Staeger) (Table I) (Dik 1989). Collecting in southern

Turkey, 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 (Burgu

et al. 1992), and C. denisoni Boorman (Dik 1993) (Table I). In 1994, Yılmaz reported 42

species from the Elazıg province (Eastern Anatolian Region (EA), Figure 1)—the highest

diversity 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 (Table I). Dik (1996) reported C. salinarius Kieffer

and C. turanicus Edwards as new country records amongst 31 species collected from the

Aegean Region (AE) of western Turkey (Aydın, Denizli, Izmir, Kutahya, and Mugla

provinces), 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; Yagcı et al. 1999; Eren and

Inci 2002; Tilki and Dik 2003; Uslu 2003).

Culicoides species Locality Map Specimens Source

C. achrayi Kettle and

Lawson, 1955

Baskil EA 7 122R, 13„ Yılmaz 1994

Elazıg EA 22 1R Yılmaz 1994

Kazan CE 34 3R Eren et al. 1995

Kadınhanı CE 31 1R Dik 1989

Keban EA 35 64R, 45„ Yılmaz 1994

Kovancılar EA 37 40R, 8„ Yılmaz 1994

Maden EA 40 1R Yılmaz 1994

Sivrice EA 50 1R Yılmaz 1994

C. azerbajdzhanicus

Dzhafarov, 1962





C. badooshensis Khalaf, 1961 Elazıg EA 22 1R, 1„ Yılmaz 1994


Maden EA 40 2„ Yılmaz 1994

Salihaga AE 46 1R Dik 1996

Soke AE 51 1R Dik 1996

C. bulbostylus Khalaf, 1961 Diyarbakır SO 20 6R, 11„ Navai 1977


C. cataneiia Clastrier, 1957 Adana ME 1 1R Dik 1993

Aksehir CE 2 2R Dik 1989


Beysehir CE 10 1R Dik 1989


Gemlik MA 25 3R Eren and Inci 2002

Golbası CE 27 5R Eren et al. 1995

Hadim CE 28 2R Dik 1989




Konya CE 36 7R, 1„ Uslu 2003




Simav AE 49 1R Dik 1996

Umurlu AE 54 4R Yagcı et al. 1999

S. Turkeya ME ?b Burgu et al. 1992

C. circumscriptusa Kieffer, 1918 Adana ME 1 1R; 21R, 4„ Navai 1977; Dik 1993

Syn: C. nadayanus Aksehir CE 2 170b Dik 1989

Kieffer, 1918 Anamur ME 3 4R, 2„ Dik 1993

Syn: C. edwardsi Ankara CE 4 3b Jennings et al. 1983

Goetghebuer, 1921 Antalya ME 5 129b; 3R Jennings et al. 1983;

Syn: C. algarum Dik 1993

Kieffer, 1924 Baskil EA 7 283R, 26„ Yılmaz 1994

Syn: C. pictidorsum (as variety of Bergama AE 8 21R, 9„ Dik 1996

C. salicola) Kieffer, 1924 Beysehir CE 10 9b Dik 1989

Syn: C. albonotatus Bornova AE 11 31R, 17„; 44R, Navai 1977; Dik 1996

Vimmer, 1932 53„

1950 B. Dik et al.


Syn: C. albosignatus Bozkır CE 12 32b Dik 1989

Vimmer, 1932 Cigli AE 16 10R, 2„ Navai 1977

Syn: C. polymaculatus Cihanbeyli CE 14 73b Dik 1989

Vimmer, 1932 Cumra CE 10 133b Dik 1989

Syn: C. pulcher Denizli AE 19 2R Dik 1996

Zihali-Sebess, 1934 Elazıg EA 22 61R, 48„ Yılmaz 1994

Syn: C. kirovabadicus Eregli CE 24 15b Dik 1989

Dzhafarov, 1964 Gemlik MA 25 125R, 26„ Eren and Inci 2002

Gokcekısık CE 26 1R Kieffer 1918

Golbası CE 27 61R, 9„ Eren et al. 1995

Hadim CE 28 5b Dik 1989

Iskenderun ME 29 5R Tilki and Dik 2003

Izmir AE 30 51R, 77„ Navai 1977

Karaman CE 33 25b Dik 1989

Kazan CE 34 320R, 20„ Eren et al. 1995



Konya CE 36 7b; 409b; 736R,

614„

Jennings et al. 1983;

Dik 1989; Uslu 2003

Kuyucak AE 39 4R Dik 1996

Maden EA 40 10R, 3„ Yılmaz 1994

Mugla AE 42 2R Dik 1996

Pirinclik SO 45 7R, 9„ Navai 1977

Salihaga AE 46 2b; 62R, 5„ Jennings et al. 1983;

Dik 1996

Serik ME 47 37R, 6„ Dik 1993

Seydisehir CE 48 107b Dik 1989

Simav AE 49 37R, 2„ Dik 1996

Sivrice EA 50 11R, 1„ Yılmaz 1994


Tarsus ME 52 15R, 5„ Dik 1993

Tire AE 53 1R Navai 1977

Umurlu AE 54 54R, 4„ Yagcı et al. 1999


C. denisoni Boorman, 1988 Serik ME 47 3R Dik 1993

C. dewulfi Goetghebuer, 1936 Adana ME 1 1„ Navai 1977

Syn: C. pseudochipterus

Downes and Ketle, 1952

C. duddingstoni Kettle Beysehir CE 10 1„ Dik 1989

and Lawson, 1955 Eregli CE 24 2„ Dik 1989

Karaman CE 33 1„ Dik 1989

Salihaga AE 46 1R, 1„ Dik 1996

Simav AE 49 1„ Dik 1996

C. dzhafarovi Remm, 1967 Adana ME 1 4R Dik 1993

Syn: C. dzhafavovi Callot, Anamur ME 3 2R Dik 1993

Kremer, Molet and

Bach, 1968

Antalya ME 5 13b; 108R Jennings et al. 1983;

Dik 1993




Cihanbeyli CE 14 20R Dik 1989

Elazıg EA 22 227R, 112„ Yılmaz 1994

Eregli CE 24 8R Dik 1989

Table I. Continued.










Mezitli ME 41 2R Dik 1993

Salihaga AE 46 1b; 5R Jennings et al. 1983;

Dik 1996

Serik ME 47 13R Dik 1993

Seydisehir CE 48 7R Dik 1989



Tarsus ME 52 16R Dik 1993


C. fagineus Edwards, 1939 Hadim CE 28 1R, 1„ Dik 1989

C. fascipennis (Staeger, 1839) Beysehir CE 10 1R Dik 1989

Syn: C. distictus Kieffer, Dinek SO 20 1R Kieffer 1918

1916 Serik ME 47 1R Dik 1993

Syn: C. albonotatus Kieffer, 1918

Syn: C. turficola Kieffer, 1925

C. festivipennis Kieffer, 1914 Antalya ME 5 3„ Jennings et al. 1983

Syn: C. odibilis Austen, Aksehir CE 2 7b Dik 1989

1921 Baskil EA 7 33R, 48„ Yılmaz 1994

Syn: C. winnertzi Bornova AE 11 8R, 7„; 2R Navai 1977; Dik 1996

Edwards, 1926 Bozkır CE 12 1b Dik 1989

Diyarbakır SO 21 1R Navai 1977


Eregli CE 24 1b Dik 1989







Konya CE 36 4b; 360R, 270„ Dik 1989; Uslu 2003



Pirinclik SO 45 2R Navai 1977

Simav AE 49 22R, 39„ Dik 1996




C. flavipulicaris Dzhafarov,

1964





Table I. Continued.

1952 B. Dik et al.


C. furcillatus Callot,

Kremer and Paradis, 1962


Bornova AE 11 1„ Navai 1977





C. gejgelensisa Dzhafarov,

1964

Antalya ME 5 2„, 2R Jennings et al. 1983;

Dik 1993



Bergama AE 8 2R Dik 1996


Bozkır CE 12 2R Dik 1989



Gemlik MA 25 51R, 3„ Eren and Inci 2002






Konya CE 36 114R, 70„ Uslu 2003













C. heliophilus Edwards, 1921 Aksehir CE 2 1R Dik 1989




Keban EA 35 13R Dik 1989



C. ibericus Dzhafarov, 1964 Antalya ME 5 1R; 42R Jennings et al. 1983;

Dik 1993

Baskil EA 7 4R Yılmaz 1994

Bornova AE 11 1R Navai 1977



Keban EA 35 1R Yılmaz 1994


C. imicolaa Kieffer, 1913 Adana ME 1 15R, 2„ Dik 1993

Syn: C. pallidipennis Carter,

Ingram and Macfie 1920

Anamur ME 3 5R, 1„ Dik 1993


Dik 1993

Table I. Continued.



Syn: C. iraqensis Khalaf,

1957

Aydın AE 6 13b Jennings et al. 1983

Bornova AE 11 1R Dik 1996

Syn: C. minutus Sen and

Das Gupta, 1959

Cakmak AE 15 16b Jennings et al. 1983

Iskenderun ME 29 53R, 3„ Tilki and Dik 2003

Syn: C. pseudoturgidus

Das Gupta, 1962

Mezitli ME 41 23R, 1„ Dik 1993

Nazili AE 44 13b Jennings et al. 1983

Salihaga AE 46 479b Jennings et al. 1983




C. kibunensis Tokunaga, 1937 Baskil EA 7 48R, 43„ Yılmaz 1994

Syn: C. cubitalis

Edwards, 1939



Syn: C. ponkikiri Kono

and Takahasi, 1940



Syn: C. sitinohensis

Okada, 1941



Konya CE 36 3R Uslu 2003



Salihaga AE 46 3R, 2„ Dik 1996


C. kolymbiensis Boorman, 1988 Baskil EA 7 110R, 78„ Yılmaz 1994




C. kurensis Dzhafarov, 1960 Antalya ME 5 348b Jennings et al. 1983

Bespınar SO 9 12R Navai 1977

Pirinclik SO 45 5„ Navai 1977


C. longipennisa Khalaf, 1957 Adana ME 1 2R; 2R Navai 1977; Dik 1993

Syn: C. flavisimilis

Dzhafarov, 1964

Anamur ME 3 4R Dik 1993


Dik 1993


Bornova AE 11 5R; 2R Navai 1977; Dik 1996


Cihanbeyli CE 14 1b Dik 1989










Maden EA 40 77R, 48„ Yilmaz 1994

Nazilli AE 44 4b Jennings et al. 1983


Dik 1996

Serik ME 47 25R, 1„ Dik 1993

Simav AE 49 20R, 8„ Dik 1996

Table I. Continued.

1954 B. Dik et al.






C. maritimus Kieffer, 1924 Ankara CE 4 1b Jennings et al. 1983

Syn: C. submaritimus

Dzhafarov, 1962

Antalya ME 5 51b Jennings et al. 1983



Bornova AE 11 10R, 4„ Navai 1977

Bozkır CE 12 22b Dik 1989

Cumra CE 18 23b Dik 1989


Kadınhanı CE 31 2b Dik 1989


Konya CE 36 171b; 6„ Dik 1989; Uslu 2003





C. minutissmus (Zetterstedt), 1855 Bornova AE 11 2R, 9„ Navai 1977

Syn: C. nanulus Kieffer, 1919

Syn: C. albihalter Kieffer, 1919

Syn: C. bychowskyi Dzhafarov, 1964

Syn: C. tugaicus Dzhafarov, 1960

C. montanus Schakirzjanova, 1962 Diyarbakır SO 21 3R Navai 1977

C. newsteadi Austen, 1921 Aksehir CE 2 6b Dik 1989

Syn: C. biclavatus Kieffer, 1924 Ankara CE 4 1b Jennings et al. 1983

Syn: C. halophilus Kieffer, 1924 Antalya ME 5 67b; 1R Jennings et al. 1983;

Syn: C. edwardsi (as variety of

C. pulicaris) Goetghebuer, 1933

Dik 1993


Syn: C. edwardsianus

(as variety of C. pulicaris)

Goetghebuer, 1933

Beysehir CE 10 19b Dik 1989











Konya CE 36 2b Jennings et al. 1983









Table I. Continued.



C. nubeculosus(Meigen), 1830 Adana ME 1 405R, 62„ Dik 1993

Syn: C. puncticollis

Goetghebuer, 1912

Antalya ME 5 3R Dik 1993

Bergama AE 8 1R, 4„ Dik 1996

Syn: C. punctaticollis

Goetghebuer, 1912





Denizli AE 19 1R Dik 1996











Simav AE 49 71R, 26„ Dik 1996



C. obsoletusa (Meigen), 1818 Adana ME 1 1R Dik 1993

Syn: Ceratopogon varius

(Winnertz), 1852

Aksehir CE 2 7b Dik 1989

Antalya ME 5 1R; 2R Jennings et al. 1983;

Syn: C. obscuripes (as variety

of C. varius) Santos Abreu, 1918

Dik 1993

Aydın AE 6 1R Jennings et al. 1983

Syn: C. lacteinervis Kieffer, 1919 Baskil EA 7 5R, 2„ Yılmaz 1994

Syn: C. rivicola Kieffer, 1921 Bornova AE 11 3R, 1„ Navai 1977

Syn: C. clavatus Kieffer, 1921 Beysehir CE 10 1b Dik 1989

Syn: C. heterocerus Kieffer, 1921 Elazıg EA 22 3R Yılmaz 1994

Syn: C. pegobius Kieffer, 1922 Eregli CE 24 1b Dik 1989

Syn: C. kabyliensis Kieffer, 1922 Gemlik MA 25 10R Eren and Inci 2002

Syn: C. concitus Kieffer, 1922 Golbası CE 27 46R, 3„ Eren et al. 1995

Syn: C. intermedius Okada, 1941 Iskenderun ME 29 3R Tilki and Dik 2003

Syn: C. intermedius

(as variety of C. obsoletus)

Okada, 1941




Syn: C. sintrensis

Cambournac, 1956


Kovancılar EA 37 10R Yılmaz 1994

Syn: C. seimi Shevchenko, 1967 Kuyucak AE 39 3R Dik 1996



Nazilli AE 44 1R Jennings et al. 1983

Salihaga AE 46 2R; 16R, 1„ Jennings et al. 1983;

Dik 1996



Simav AE 49 12R, 1„ Dik 1996




Table I. Continued.

1956 B. Dik et al.


C. odiatusa Austen, 1921 Adana ME 1 25R 7„ Dik 1993

Syn: C. niger (as variety of

C. pallidicornis) Root and

Hoffman, 1937


Anamur ME 3 5R,1„ Dik 1993


Syn: C. indistinctus Khalaf, 1961 Dik 1993

Syn: C. lailae Khalaf, 1961 Aydın AE 6 14b Jennings et al. 1983

Syn: C. kureksthaicus

Dzhafarov, 1962


Bergama AE 8 5R Dik 1996

Syn: C. conicus Remm

and Zhagolev, 1968



Bornova AE 11 22R, 1„; 1R Navai 1977; Dik 1996


Cigli AE 16 1R Navai 1977



Denizli AE 19 4R Dik 1996

Diyarbakır SO 21 1„ Navai 1977













Pirinclik SO 45 3R Navai 1977


Dik 1996

Serik ME 47 19R, 2„ Dik 1993






Tire AE 53 8R, 1„ Navai 1977


C. pallidicornis Kieffer, 1919 Baskil EA 7 283R, 25„ Yılmaz 1994

Syn: C. susae Kieffer, 1919 Elazıg EA 22 3R, 1„ Yılmaz 1994

Syn: C. dileucus Kieffer, 1921 Keban EA 35 172R, 174„ Yılmaz 1994

Syn: C. brunneiscutellatus

(as variety of C. pallidicornis)

Zilahi-Sebess, 1933




Syn: C. bruneoscutellatus

(as variety of C. pallidicornis)

Zilahi-Sebess, 1934


Syn: C. niger Root and

Hoffman, 1937

C. parrotic Kieffer, 1922 Ankara CE 4 1„ Edwards et al. 1939



Table I. Continued.





Nazilli AE 44 1R Jennings et al. 1983




C. pictipennis (Staeger), 1839 Baskil EA 7 1„ Yılmaz 1994

Syn: Ceratopogon arcuatus

(Winnertz), 1852


Cigli AE 16 2R Navai 1977

Syn: C. guttularis Kieffer, 1919 Elazıg EA 22 12R, 4„ Yılmaz 1994

Syn: C. maculatus

(as variety of C. pictipennis)

Zilahi-Sebess, 1936




Syn: C. subgrisescens

Dzhafarov, 1964

Tire AE 53 1R, 2„ Navai 1977

Syn: C. achkamalicus

Dzhafarov, 1964

Syn: C. luganicus

Shevchenko, 1972

C. picturatus Kremer and

Deduit, 1961


Baskil EA 7 365R, 13„ Yilmaz 1994








C. pulicarisa (Linnaeus), 1758 Anamur ME 3 1R Dik 1993

Syn: C. setosinervis Kieffer, 1913 Aksehir CE 2 78b Dik 1989

Syn: C. pullatus Kieffer, 1915 Baskil EA 7 27R, 5„ Yılmaz 1994

Syn: C. stephensi Carter, 1916 Beysehir CE 10 3b Dik 1989

Syn: C. cinerellus Kieffer, 1919 Bornova AE 11 16R, 10„ Navai 1977

Syn: C. quinquepunctatus

Goetghebuer, 1921

Cigli AE 16 7R 3„ Navai 1977


Syn: C. flaviplumus Kieffer, 1924 Elazıg EA 22 11R Yılmaz 1994

Syn: C. sawamotoi Kono and

Takahasi, 1940





Konya CE 36 7b; 1R Dik 1989; Uslu 2003








Soke AE 51 1„ Dik 1996



Table I. Continued.

1958 B. Dik et al.


C. pumilus (Winnertz), 1852 Antalya ME 5 1R Dik 1993







Keban EA 35 1261R, 1000„ Yılmaz 1994





C. punctatus (Meigen), 1804 Ankara CE 4 3b Jennings et al. 1983

Syn: C. punctatus Latreille, 1809 Antalya ME 5 38b; 3R Jennings et al. 1983;

Syn: C. ocellaris Kieffer, 1921 Dik 1993

Syn: C. kasachstanicus

(as subspecies of C. pulicaris)

Shakirzjanova, 1963




Syn: C. remmi

Damian-Georgescu, 1972


Bornova AE 11 2R Dik 1996














Konya

Kovancılar

CE 36 1b; 272b Jennings et al. 1983;

Dik 1989

Kusadası EA 37 132R, 16„ Yılmaz 1994

Kuyucak AE 38 Numerous R Leclercq 1966

Maden AE 39 3R Dik 1996

Salihaga EA 40 10R, 3„ Yılmaz 1994

Serik AE 46 9b; 13R Jennings et al. 1983;

Dik 1996

Seydisehir ME 47 6R Dik 1993

Simav CE 48 317b Dik 1989

Sivrice AE 49 4R Dik 1996

Umurlu EA 50 1002R, 73„ Yılmaz 1994

AE 54 7R, 1„ Yagcı et al. 1999

C. puncticollisa (Becker, 1903) Adana ME 1 6R, 3„; 7R Jennings et al. 1983;

Syn: Ceratopogon algecirensis (as

form of pulicaris)(Strobl), 1900

Dik 1993


Syn: Ceratopogon algecirensis (as

form of pulicaris)(Strobl), 1900



Syn: C. impressus Kieffer, 1918 Bespınar SO 9 10R, 5„ Navai 1977

Syn: C. distigma Kieffer, 1922 Bornova AE 11 1„; 1R Navai 1977; Dik 1996

Syn: C. donatieni Kieffer, 1922 Cigli AE 16 2R, 1„ Jennings et al. 1983

Table I. Continued.



Syn: C. sciniphes Kieffer, 1925 Cihanbeyli CE 14 624b Dik 1989

Syn: C. bipunctatus Vimmer, 1932 Cumra CE 18 60b Dik 1989

Syn: C. tripunctatus Vimmer, 1932 Elazıg EA 22 17R, 4„ Yılmaz 1994

Syn: C. wenigi Vimmer, 1932 Eregli CE 24 25b Dik 1989

Syn: C. flavitarsis Vimmer, 1932 Golbası CE 27 2R, 2„ Eren et al. 1995

Syn: C. griseovittatus Vimmer,

1932



Syn: C. luteosignatus Vimmer,

1932



Syn: C. vavrai Vimmer, 1932 Konya CE 36 137R, 35„ Uslu 2003


Konya CE 36 44b Jennings et al. 1983




Simav AE 49 220R, 78„ Dik 1996





C. reconditus Campbell and

Pelham- Clinton, 1960



Syn: C. riouxi Callot and

Kremer, 1961





C. riethi Kieffer, 1914 Bergama AE 8 1R Dik 1996

Syn: C. cordatus Kieffer, 1921 Bozkır CE 12 19b Dik 1989

Syn: C. crassiforceps Kieffer, 1924 Cihanbeyli CE 14 41b Dik 1989





Konya CE 36 7327b; 8R, 43„ Dik 1989; Uslu 2003

Mut ME 43 1„ Dik 1996




C. saevus Kieffer, 1922 Adana ME 1 2R Dik 1993

Syn: C. drenskii Zilahi-Sebess,

1934



Syn: C. puncticeps Goetghebuer,

1934



Syn: C. micromaculithorax

Khalaf, 1957


Cigli AE 16 12R 3„ Navai 1977

Diyarbakır SO 21 4R Navai 1977





Konya CE 36 2R Dik 1989



Table I. Continued.

1960 B. Dik et al.



Mut ME 42 43R Dik 1993


Salihaga AE 46 21„ Jennings et al. 1983






C. sahariensisa Kieffer, 1923 Mugla AE 42 1R Dik 1996

Syn: C. baghdadensis Khalaf,

1957

Simav AE 49 3R, 2„ Dik 1996


Syn: C. coluzzii Callot, Kremer

and Bailly-Choumara, 1970



C. salinarius Kieffer, 1914 Bornova AE 11 1R Dik 1996

Syn: C. halobius Kieffer, 1914 Konya CE 36 1R Uslu 2003

Syn: C. meinerti Kieffer, 1915

Syn: C. punctatidorsum Kieffer, 1924

C. schultzeiad (Enderlein), 1908 Adana ME 1 4R; 259R, 13„ Navai 1977; Dik 1993

Anamur ME 3 16R Dik 1993



Baskil EA 7 1„ Yılmaz 1994




Kuyucak AE 39 7R, 5„ Dik 1996







C. scoticus Downes and Kettle, 1952 Hadım CE 28 1R Dik 1989


C. sejfadinei Dzhafarov, 1958 Baskil EA 7 32R, 4„ Yılmaz 1994

Syn: C. flavidus Dzhafarov, 1959 Keban EA 35 1R, 1„ Yılmaz 1994




C. semimaculatus Clastrier, 1958 Maden EA 40 1R Yılmaz 1994

C. shaklawensisa Khalaf, 1957 Aksehir CE 2 6R Dik 1989

Syn: C. caspius Gutsevich, 1959 Baskil EA 7 22R, 13„ Yılmaz 1994




Keban EA 35 47R, 30„ Uslu 2003

Konya CE 36 119R, 140„ Uslu 2003




Table I. Continued.





C. simulator Edwards, 1939 Aksehir CE 2 44b Dik 1989









Konya CE 36 234b Dik 1989



C. slovacus Orszagh, 1969 Baskil EA 7 2R Yılmaz 1994

C. subfasciipennis Kieffer, 1919 Aksehir CE 2 64R Dik 1989

Syn: C. analis (as variety of C.

subfasciipennis) Kieffer, 1925

Antalya ME 5 6R, 1„ Jennings et al 1983








Konya CE 36 2R; 1R, 1„ Dik 1989; Uslu 2003







C. subneglectusa Vimmer, 1932 Baskil EA 7 1R, 2„ Yılmaz 1994






C. tauricus Gutsevich, 1959 Aksehir CE 2 4R Dik 1989

Antalya ME 5 1R Dik 1993


Bergama AE 8 1R, 1„ Dik 1996









C. truncorum Edwards, 1939 Baskil EA 7 17R, 1„ Yılmaz 1994

Syn: C. sylvarum Callot

and Kremer, 1961



Table I. Continued.

1962 B. Dik et al.

the morphology and ecological parameters of the Turkish fauna in relation to disease

transmission. Total numbers of reported species per study are given in relation to currently

accepted nomenclature (Borkent and Wirth 1997).

Although other authors have published Culicoides studies and added valuable data to

species distributions across Turkey (Table I; Figure 1), their studies did not report novel

Culicoides: Eren et al. (1995) (Ankara province, Central Anatolian Region (CE), 19 spp.),

Yagcı et al. (1999) (Aydin, Aegean Region (AE), 14 spp.), Eren and Inci (2002) (Bursa

province, Marmara Region (MA), 12 spp.), Tilki and Dik (2003) (Iskenderun,

Mediterranean Region (ME), 5 spp.), and Uslu (2003) (Konya province, Central

Anatolian Region (CE), 18 spp.) (Table I; Figure 1).

Species distribution and relative abundance

Culicoides sampling in Turkey has been sporadic and is far from comprehensive. Adult

Culicoides have been reported from six of the seven recognized Regions of Turkey

(Figure 1). No records are available on the Culicoides fauna of the Black Sea Region in the

north of the country. Distribution records included in this review cover the Central

Anatolian Region (15 localities in four of 15 provinces), Aegean Region (16 localities in five

of eight provinces), Mediterranean Region (11 localities in five of eight provinces), Eastern

Anatolian Region (six localities in one of 15 provinces) and Southeastern Anatolian









C. turanicus Gutsevich and

Smatov, 1971


C. vexans (Staeger), 1839 Aksehir CE 2 1R Dik 1989

Syn: Palpomyia pungens

(Kieffer, 1901)



Syn: C. perpungens Kieffer, 1919 Maden EA 40 1„ Yılmaz 1994

Syn: C. ajbassovi Shakirzjanova,

1962


C. vidourlensis Callot, Kremer,

Molet and Bach, 1968





Maden EA 40 1„ Yılmaz 1994


Serik ME 47 1Re Dik 1993


aBurgu et al. (1992) reported several species from the southern Turkish localities of Aydın, Antalya, Ceylanpınar,

Cukurova, Erdemli, and Turkoglu. Exact locality data and numbers/sex of samples were not detailed. bSex

unspecified. cLocality originally listed as Koktshe Kissik in Kieffer (1918). dSpecies identified as C. schultzei may

comprise a species complex. eIdentification verified after publication.

Table I. Continued.


Region (five localities in two of seven provinces), and a single locality (in one of 12

provinces) of the Marmara Region (Kieffer 1918; Edwards et al. 1939; Leclercq 1966;

Navai 1977; Jennings et al. 1983; Dik 1989, 1993, 1996; Burgu et al. 1992; Yılmaz 1994;

Eren et al. 1995; Yagcı et al. 1999; Eren and Inci 2002; Tilki and Dik 2003; Uslu 2003)

(Figure 1).

Culicoides circumscriptus, C. festivipennis, C. maritimus, and C. pulicaris are the most

widespread species, being found in all six provinces sampled, with C. cataneii, C. gejgelensis,

C. longipennis, C. nubeculosus, C. obsoletus, C. odiatus, C. puncticollis, C. saevus, and C.

shaklawensis being reported in five provinces, respectively (Table I). The least common

species are C. denisoni, C. dewulfi, C. fagineus, C. minutissmus, C. montanus, C. semima-

culatus, C. slovacus, and C. turanicus which are represented from only one locality (Table I).

Only a single male and a single female specimen represent C. dewulfi and C. semimaculatus,

respectively (Navai 1977; Yılmaz 1994). Culicoides azerbajdzhanicus and C. sejfadinei were

collected from four and five localities, respectively, all within the Eastern Anatolian Region

(Yılmaz 1994). Culicoides imicola has been confirmed in the Aegean (Aydın, Bornova,

Cakmak, Nazilli, Salihaga, and Umurlu) (Jennings et al. 1983; Dik 1993, 1996; Yagcı et al.

1999) and the Mediterranean (Adana, Anamur, Antalya, Iskenderun, Mezitli, and Tarsus)

(Burgu et al. 1992; Dik 1993; Tilki and Dik 2003) regions of Turkey. Although the species

was not detected elsewhere, care should be taken in the interpretation of this and other

species distributions, given the random sampling strategies reflected in this paper.

As the records of Culicoides presented here have been collected by various methods

(pootering, baffle traps, UV light traps, etc.), no inference of relative abundance can be

drawn. However, the following 19 species appear to be locally abundant at some sites in

Turkey: C. circumscriptus, C. dzhafarovi, C. festivipennis, C. gejgelensis, C. imicola, C.

kolymbiensis, C. longipennis, C. newsteadi, C. odiatus, C. pallidicornis, C. picturatus, C. pumilus,

C. punctatus, C. riethi, C. saevus, C. schultzei group, C. shaklawensis, C. subneglectus, and C.

vidourlensis (Table I). Little is known on the preferred breeding sites and other ecological

parameters of Culicoides species in Turkey.

Veterinary importance of Turkish Culicoides

Protozoa. Three Turkish Culicoides have been implicated in the transmission of zooparasitic

protozoa. Leucocytozoonosis is an economically important disease of poultry. In SE Asia,

C. circumscriptus and C. festivipennis (as C. odibilis) have been shown to transmit Leucocy-

tozoon caulleryi, although the latter species is not an effective vector (Morii and Kitaoka

1968). The transmission of Haemoproteus desseri and Trypanosoma bakeri to parrots, and

Hepatocystis brayi to squirrels via the bites of C. nubeculosus has been implicated experi-

mentally, but not confirmed in nature (Miltgen et al. 1976; Miltgen and Landau 1982).

Nematoda. At least two Turkish Culicoides species are proven vectors of Onchocerciasis to

domestic animals. Culicoides nubeculosus is an efficient vector of Onchocerca reticulata and O.

cervicalis to horses (Steward 1933; Moignoux 1952) and O. gutturosa to cattle (Bain 1979),

and C. oxystoma of the C. schultzei group transmits O. gibsoni to cattle (Buckley 1938).

Culicoides nubeculosus has also been shown to be capable of experimental transmission of the

Eufilarial nematodes, Eufilaria delicata and E. bartlettae, to blackbirds (Bain 1980).

Arboviruses. Culicoides imicola is clearly involved in bluetongue transmission in Turkey

(Jennings et al. 1983), but other common species including those in the C. obsoletus and C.

1964 B. Dik et al.

pulicaris species complexes may also play a criticial role in Turkey, as in other countries in

the Mediterranean Basin (De Liberato et al. 2005; Savini et al. 2005; Carpenter et al.

2006). Due to its high association with domestic livestock, members of the C. schultzei

group have also been implicated as potential bluetongue and African horse sickness virus

vectors in South Africa (Venter et al. 1996). In other regions of its range (Africa, Middle

East, and in other areas of Mediterranean Europe), Culicoides imicola is also a competent

vector of other arboviruses including African horse sickness virus, Akabane virus, Bovine

ephemeral fever, Equine encephalitis, and the Sabo and Shamonda viruses (Yonguc et al.

Figure 1. Outline map of Turkey detailing the collection sites of Culicoides listed in Table I. Collection sites are

listed numerically in alphabetical order and indicated on the map as follows: 1, Adana (36u589N, 35u229E); 2,

Aksehir (38u219N, 31u259E); 3, Anamur (36u049N, 32u499E); 4, Ankara (40u009N, 32u529E); 5, Antalya

(36u549N, 30u419E); 6, Aydın (37u499N, 27u499E); 7, Baskil (38u349N, 38u499E); 8, Bergama (39u079N,

27u109E); 9, Bespınar (37u509N, 41u359E); 10, Beysehir (37u419N, 31u439E); 11, Bornova (38u279N, 27u139E);

12, Bozkır (37u119N, 32u149E); 13, Ceylanpınar (36u509N, 40u039E); 14, Cihanbeyli (38u399N, 32u559E); 15,

Cakmak (37u479N, 29u009E); 16, Cigli (38u299N, 27u049E); 17, Cukurova (36u509N, 35u209E); 18, Cumra

(37u349N, 32u469E); 19, Denizli (37u509N, 29u089E); 20, Dinek (37u479N, 39u049E); 21, Diyarbakır (37u589N,

40u109E); 22, Elazıg (38u389N, 39u059E); 23, Erdemli (36u369N, 34u189E); 24, Eregli (37u319N, 34u019E); 25,

Gemlik (40u269N, 29u099E); 26, Gokcekısık (39u389N, 30u239E); 27, Golbası (39u489N, 32u489E); 28, Hadim

(36u599N, 32u279E); 29, Iskenderun (36u349N, 36u109E); 30, Izmir (38u279N, 27u109E); 31, Kadınhanı

(38u149N, 32u129E); 32, Kahramanmaras (37u389N, 36u489E); 33, Karaman (37u119N, 33u089E); 34, Kazan

(40u139N, 32u419E); 35, Keban (38u479N, 38u449E); 36, Konya (37u559N, 32u129E); 37, Kovancılar (38u439N,

39u519E); 38, Kusadası (37u519N, 27u159E); 39, Kuyucak (37u559N, 28u279E); 40, Maden (38u239N, 39u409E);

41, Mezitli (36u489N, 34u379E); 42, Mugla (37u139N, 28u169E); 43, Mut (36u389N, 33u269E); 44, Nazilli

(37u549N, 28u199E); 45, Pirinclik (38u129N, 49u209E); 46, Salihaga (37u549N, 29u049E); 47, Serik (36u559N,

31u069E); 48, Seydisehir (37u259N, 31u509E); 49, Simav (39u059N, 28u589E); 50, Sivrice (38u279N, 39u189E); 51,

Soke (37u459N, 27u249E); 52, Tarsus (36u559N, 34u539E); 53, Tire (38u059N, 27u449E); 54, Umurlu (37u519N,

27u579E).


1982; Sellers and Pedgley 1985; Dik 1988/89), and therefore could also be involved in local

transmission of other arboviruses to livestock in Turkey. Mellor et al. (1990) isolated

African Horse Sickness (AHS) virus serotype 4 from mixed C. obsoletus and C. pulicaris

pools in Spain during the 1988 AHS outbreak and C. pulicaris s.l. (including C. pulicaris s.s.

and C. punctatus, both present in Turkey) was shown to be an effective vector of bluetongue

(BTV-1 and BTV-4) in the laboratory (Jennings and Mellor 1988). Further studies on the

species composition and vector competencies of proven/potential vector complexes

(Imicola, Obsoletus, Pulicaris, and Schultzei species complexes) in Turkey is required.

Acknowledgements

The authors are grateful to Dr John Boorman (UK) and Mr Rudy Meiswinkel (Italy) for

taxonomic advice.

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