Tabanidae (Diptera) of Saudi Arabia

Saudi Journal of Biological Sciences (2009) 16, 77 83 King Saud University Saudi Journal of Biological Sciences www.ksu.edu.sa www.sciencedirect.com ORIGINAL ARTICLE Tabanidae (Diptera) of Saudi Arabia H.M. Al Dhafer a, *, H.A. Dawah b, M.A. Abdullah c a King Saud University, College of Food and Agricultural Sciences, Department of Plant Protection, P.O. Box 2460, Riyadh 11451, Saudi Arabia b National Museum of Wales, Department of Biodiversity and Systematic Biology, Entomology Section, Cardiff CF10 3NP, UK c King Khalid University, College of Science, Department of Biology, P.O. Box 9064, Abha, Saudi Arabia Available online 27 October 2009 KEYWORDS Tabanidae; Horseflies; New records; Saudi Arabia; Key to genera Abstract Samples were collected from southern, central and eastern regions of Saudi Arabia using Malaise traps and sweep nets. Nine species of Tabanidae were identified, two for the first time from Saudi Arabia, Hybomitra peculiaris (Szila dy) and Atylotus pulchellus (Loew). Therefore, the total number of Tabanidae in Saudi Arabia is 31 species. Remarks of the species recorded in this study were given. A key to the genera of Tabanidae occurring in the Arabian Peninsula is also provided. Available literature for Saudi Arabian Tabanidae is summarized and provided. It is concluded that the tabanid fauna of Saudi Arabia is more similar to that of the Palaearctic region than to the Afrotropical region. ª 2009 King Saud University. All rights reserved. 1. Introduction The family Tabanidae (horse flies, deer flies and clegs) belongs to the superfamily Tabanoidea, suborder Brachycera, along with 10 other dipteran families (Colless and McAlpine, 1991). Members of the Tabanidae are the largest blood-sucking flies, and the family contains 3000 4000 species throughout the world (Kettle, 1992; Chainey, 1993). It is important because of its veterinary and medical significance (Foil, 1989; * Corresponding author. E-mail address: hdhafer@hotmail.com (H.M. Al Dhafer). 1319-562X ª 2009 King Saud University. All rights reserved. Peerreview under responsibility of King Saud University. doi:10.1016/j.sjbs.2009.10.004 Production and hosting by Elsevier Kettle, 1992; Chainey, 1993), and includes many species important to human and animal health, either by acting as a disease vector, or by debilitating the host. For more information on the diseases for which tabanids act as vectors, see: Chvála et al. (1972), Krinsky (1976). When present in large numbers, Tabanids can also cause economic losses by disturbing labourers and tourists, because the bite of some species can be very irritating and painful and secondary bacteria etc. can be introduced into the wound. Their attack on livestock can be so severe as to reduce milk yields in dairy cattle. The Tabanidae are poorly known in the Middle East. Al-Talafha et al. (2004) reported that there are 27 (Leclercq, 1982 = ca 44) species of Tabanidae recorded from Iraq and 24 species in Jordan. Al-Houty (1989) recorded one species from Kuwait, while Al-Ahmadi and Salem (1999) listed 17 species from Saudi Arabia. The main objective of the present paper is to report on the species recorded in Saudi Arabia during our survey, along with available details on their biology and distribution and to summarize the available literature for Saudi Arabia. A key to the tabanid genera occurring in the Arabian Peninsula is also included.

78 H.M. Al Dhafer et al. 2. Materials and methods 2.1. Collection methods and specimen preparation and specimens of flies examined Malaise traps were set up at two locations in the Asir province of Saudi Arabia and operated at various periods. In addition, other specimens collected by other collectors from other sites were also examined. These sites were: Al Qatif, Alkarj, Al Hufuf, Fifa, Riyadh and Najran. These specimens were deposited in The Arabian National Museum of Arthropods, Ministry of Agriculture, Riyadh (ANMA); in The King Saud University Museum of Arthropods King Saud University, College of Food and Agricultural Sciences, Department of Plant Table 1 List of localities sampled with coordinates and altitude, trapping methods and dates of collection. Abha Farm Centre; vegetable farm 18 13 0 N42 30 0 E 2150 m Malaise trap 3.lll.-3.Vl.2001 Alkarj 24 13 0 N47 15 0 E 300 m Sweeping 28.X.1980 Al Hufuf 25 15 0 N49 32 0 E 250 m Sweeping 30.XI.1982; 20.V.1984 Al Qatif 26 45 0 N49 58 0 E 100 m Sweeping 15.XI.1985; 15.XI.1980; 30.XI.1982 Al-Rakaba, Alhurytha 90 km South of Abha 17 07 0 N42 39 0 E 60 m Sweeping 3.II.2006 Fifa 19 12 0 N43 6 0 E 250 m Sweeping 1.IV.1983; 31.X.1984 Maraba 60 km South of Abha; fruit farm, mainly mango and banana 17 54 0 N42 23 0 E 80 m Malaise trap 1-17.Vl.2003 1-31.V. 2004 15-X-30.IX.2004 Najran 17 32 0 N44 20 0 E 1257 Sweeping 15.IV.1983 Riyadh 24 36 0 N46 45 0 E 650 m Sweeping 14.V.1977; 2.V.1981; 15.II.1981; 8.I.1985; 3.VIII.1980 Table 2 List of Tabanidae species recorded from Saudi Arabia. Species References Origin * Subfamily Tabanini Ancala latipes (Macquart) Amoudi (1989) P, A Atyloyus farinosus (Szilady) Moucha (1976), Amoudi and Leclercq (1992), Gadallah and Bosly (2006) P Atyloyus pallescens (Walker) Moucha (1976) P Atylotus agrestis (Wiedemann) Amoudi (1989), this study P, A, O Atylotus pulchellus Loew This study P, O Atylotus venturii Leclercq, 1966 Amoudi and Leclercq (1996) P Atylotus pallescens ** (Walker, 1871) Moucha (1976) P Atylotus agricola (Wiedemann) Amoudi and Leclercq (1993) P Hybomitra peculiaris (Szilády) This study P, O Haematopota coronata Austen Leclercq (1982, 1986), this study P, A Haematopota abyssinica Surcouf Amoudi (1989 P, A Haematopota minuscula Austen Amoudi and Leclercq (1993) P Tabanus albifacies Loew Leclercq (1966), Amoudi and Leclercq (1996) P, A Tabanus arabicus Macquart Leclercq (1982), Amoudi and Leclercq (1996) P Tabanus biguttatus Wiedemann Oldroyd (1954), Amoudi (1989), this study P, A Tabanus camelarius Austen Leclercq (1986) P, A Tabanus cordiger Meigen Leclercq (1986) P Tabanus fumidus Austen Leclercq (1982) P Tabanus leleani turkestanicus Olsufjev Leclercq (1982), this study P, O Tabanus leucostomus Loew Leclercq (1986) P, A Tabanus mordax Austen Leclercq (1986), Walker and Pittaway (1987) P Tabanus polygonus Walker Walker and Pittaway (1987) P Tabanus rupinae Austen Walker and Pittaway (1987), this study P Tabanus riyadhae Amoudi and Leclercq Amoudi and Leclercq (1988) P Tabanus separatus Efflatoun Amoudi and Leclercq (1996) P Tabanus sabuletorum Loew Leclercq (1982), this study P, O Tabanus taeniola Palisot de Beauvois Amoudi (1989), Amoudi and Leclercq (1992), Gadallah and Bosly (2006) P, A Tabanus sufis Jaennicke Leclercq (1986), Amoudi and Leclercq (1993, 1996), this study P, A, O Tabanus unifasciatus Loew Amoudi and Leclercq (1996) P Subfamily Pangoniinae Philoliche (Philoliche) magrettii (Bezzi) Amoudi and Leclercq (1992) P, A Philoliche (Dorcaloemus) auricoma (Austen) Amoudi and Leclercq (1992) P, A * A: Afrotropical; P: Palaearctic; O: Oriental. ** Moucha (1976) recorded this species from Saudi Arabia, followed by Leclercq (1982). However, Chvála (1988) records this as a doubtful species and states that the type locality (Tor) is in Sinai, Egypt and not in Arabia. Leclercq (2000) supported Chvála s statement.

Tabanidae (Diptera) of Saudi Arabia 79 Protection, Riyadh (KSMA), and in The National Museum of Wales, Cardiff (NMWC). 2.2. Identification of flies Insects were identified at the National Museum of Wales, Cardiff (NMWC). They were first identified to genus level using Stubbs and Drake (2001) and then to species level using mainly Oldroyd (1952, 1954, 1957), Leclercq (1966) and Chva la et al. (1972). Comparisons were also made with reliably identified specimens in the National Museum of Wales, Cardiff. 2.3. Illustrations A photographic montage of some of the species of Tabanidae occurring in the Arabian Peninsula was prepared in the NMWC using images from a video camera and Synaptics Automontage software. 3. Results and discussion Nine species of Tabanidae were identified, two for the first time recorded from Saudi Arabia, Hybomitra peculiaris (Szila dy, 1914) and Atylotus pulchellus (Loew, 1858) Therefore, the total number of Tabanidae in Saudi Arabia is 31 species. It is concluded that the tabanid fauna of Saudi Arabia is more similar to that of the Palaearctic region than to that of the Afrotropical region (Table 2). Figure 1 (A) Tibiae of hind leg of Adersia sp.; (B) tibiae of hind leg of Tabanus sp. 3.1. Key to genera of Tabanidae occurring in the Arabian Peninsula (1) Middle and hind tibiae with apical spurs......(fig. 1A)............2 Only middle tibiae with apical spurs.................. (Fig. 1B)..............3 (2) Grey dusty-looking flies found on sea beaches; mouth parts in both sexes very much reduced, female with frons very wide and swollen (Fig. 2)...........Adersia Austen Habitat otherwise, mouth parts fully functional in female; wing usually with distinctive cross band or bands and often with fore margin and apex with similar dark markings; basal two antennal segments usually long and subequal in length (Fig. 3)... Chrysops Meigen Figure 2 The general features of the female of Adersia guichardi Austen (Photograph by James Turner ª Amgueddfa Cymru (3) Wing with a distinct grey brown pattern of small spots and rosettes; basal part of third antennal segment slender but differentiated from the three terminal segments (Fig. 4).........................................................Haematopota Meigen Not this combination of characters, wing markings may be present but not of this pattern..........................4 (4) Eyes of living specimens light yellowish to pale green grey, usually with one incomplete narrow band or unbanded; eyes of dry specimens light to reddish-brown. Figure 3 The general features of the female of Chrysops flavipes Meigen (Photograph by James Turner ª Amgueddfa Cymru

80 H.M. Al Dhafer et al. Figure 4 The general features of the female of Haematopota coronata Austen (Photograph by James Turner ª Amgueddfa Cymru Frontal calli in female reduced, very small or absent both small and almost round, occupying only 1/3rd of the width of the frons. Femora mainly yellow or orange (rarely only a quarter pale). Generally a smaller lightgrey or yellowish-brown species (Fig. 5)... tyloyus (Osten-Sacken) Eyes of living specimens bright green to dark reddishbrown, with 1 4 bands or unbanded; eyes of dry s- pecimens blackish. Frontal calli in female well-developed, Femora only narrowly yellow at apex (much less than a quarter of length of femur). A dark or l- ight species of various sizes.................5 Figure 5 The general features of the female of Atylotus agrestis Wiedemann (Photograph by James Turner ª Amgueddfa Cymru (5) Vertex usually with a well-developed, shining ocellar tubercle (Fig. 6)...... Hybomitra Enderlein Vertex without a shining and well-developed ocellar tubercle (Fig. 7)...Tabanus L. There are no published records of species in the genus Adersia from the Arabian Peninsula but there is a series, A. guichardi Oldroyd collected from Oman, Dhofar, Mughsail beach, 11.X. 1990, M.J. Abejer & Ra s Ghubrah, 19.VI. 1997, M.D. Gallagher in National Museum of Wales, Cardiff. 4. Systematic accounts Subfamily Tabanini Atylotus agrestis (Wiedemann) 1828 Tabanus agrestis Wiedemann, 1828: Aussereuropa ische Zweiflu gelige Insekten, 1: 557. Chainey and Oldroyd (1980) listed eight synonym of A. agrestis. Chva la (1988) listed only one synonym which was different from those listed by Chainey and Oldroyd (1980). Figure 6 The general features of the female of Hybomitra montana (Photograph by James Turner ª Amgueddfa Cymru Specimens examined: Saudi Arabia: 1$, Asir, Maraba,15.X.-30.XI.2004, Malaise trap, H.A. Dawah & M.A. Abdullah (NMWC) (see Table 1). Remarks: This species is very difficult to identify. It can be differentiated from the closely related species fuscipes Ricardo by the short post-occipital fringe and the flatter subcallus. These two characters can also separate agrestis from all the other Atylotus of the Ethiopian region, a part from A. diurnus Walkers. In life, the eyes of A. agrestis are a brighter green than those of A. fuscipes. This character can only be useful if one has both species to compare. This is the first record of this species from Saudi Arabia. This species was described from Egypt. It is widespread in

Tabanidae (Diptera) of Saudi Arabia 81 Figure 7 The general features of the female of Tabanus leleani Austen (Photograph by James Turner ª Amgueddfa Cymru the Afrotropical region outside the Congo Basin and west African forest areas and is known from; Palaearctic Region: Egypt; Afrotropical Region: Madagascar, Mauritius and Reunion, South Yemen (Chainey and Oldroyd, 1980; Chvála, 1988). Atylotus pulchellus (Loew, 1858) Tabanus pulchellus Loew, 1858, Verhandlungen des Zoologisch-Botanischen Gesellschaft in Wien, 8: 597. Chvála (1988) listed two synonym of A. pulchellus. Specimens examined: Saudi Arabia: 1$, 1# Riyadh, 14.V.1977, sweeping, A. Talhouk (ANMA); 3$ Hufuf, 30.XI.1982, sweeping, A. Talhouk (ANMA); 1$ Hufuf, 20.V.1984, sweeping, A. Talhouk (ANMA); 1# Alqatif, 15.XI.1980, sweeping, A. Talhouk (ANMA); 1$ Riyadh, 2.V.1981, sweeping, A. Talhouk (ANMA); 1# Fifa 1.IV.1983, sweeping, Abu-Zuhairah (ANMA). Remarks: This species is rather variable in colouration. Some individuals have tergite 1 only yellowish along the side of the abdomen, whilst others have the whole of the abdomen yellowish at the sides, including the apical tergites. The antennae vary from yellowish to nearly brown. (Chva la et al., 1972). This is the first record of this species from Saudi Arabia. It was described from Turkey, and has since been recorded from the following areas: Palaearctic Region: Algeria, Cyprus, Egypt, Europe, Jordan, Iran, Iraq, Palestine, Sardinia and U.S.S.R (Trancaucasia). Oriental Region: China. (Chva la et al., 1972; Chvála, 1988; Al-Talafha et al., 2004). Haematopota coronata Austen, 1908 Haematopota coronata Austen, 1908, Annals and Magazine of Natural History, (8) 2: 100. Specimens examined: Saudi Arabia: 1$, Asir, Maraba,1-30.V. 2004, Malaise trap. Remarks: H. coronata is readily recognized by the doubled or multiple rosettes on the wing, and the swollen, shining, deeply-constricted, first-antennal segment (Oldroyd, 1952). by Leclercq (1982, 1986). It was described from Somalia and further recorded from: Palaearctic area: Iran, Palestine, Jordan and Yemen. Afrotropical Region: Chad, Ethiopia, Sudan (Chainey and Oldroyd, 1980; Chva la, 1988; Al-Talafha et al., 2004). Hybomitra peculiaris (Szilády, 1914) Tabanus (Therioplectes) peculiaris (Szilády, 1914): Annales Historico-Naturales Musei Nationalis Hungarici, 12: 666. Chvála (1988) listed three synonym of H. peculiaris. Specimens examined: Saudi Arabia: 1$ Alqatif, 15.XI.1985, sweeping, A. Talhouk (ANMA). Remarks: This species is often found near salt lakes and along rivers but the most common habitat is the desert zone. Females are known to attack man and domestic and wild animals (horses, horned cattle, camels, saigas and also pelicans). They are also vectors of tularaemia and su-auru diseases of horses and camels (Shevtshenko, 1961). This is the first record of this species from Saudi Arabia. The male was described from Djarkent, Turkestan, and the female from Sarepta (=Krasnoarmejsk), Ukraine. It has since been recorded from the following areas: Palaearctic Region: Afghanistan, Europe (known only from the most south eastern parts, from the region of the Volga river, e.g., in the Kuma river basin), Iraq, Iran, Mongolia and Palestine. Oriental Region: China and India (Chva la, 1988). Tabanus biguttatus Wiedemann, 1830: 623 Tabanus biguttatus Wiedemann, 1830: Aussereuropa ische Zweiflu gelige Insekten, 2, 623. Chainey and Oldroyd (1980) listed seven synonym of T. biguttatus. Specimens examined: Saudi Arabia: 1$ Jizan, 11.II.1983, sweeping, A, Talhouk (ANMA). Remarks: This species breeds in temporary ponds. When the pond dries out and the mud cracks, the larva forms a pupal cell (a mud cylinder) into which it retreats to avoid desiccation in dry condition and attack by predators and parasitoids. At emergence, the pupa rasps its way through the cap of the cell and the adult emerges (Kettle, 1992). Oldroyd (1954) stated that the male of this species is fond of settling on tree-trunks and large stones or rocks, and is frequently seen to drink water. In addition, the eggs are deposited in a rounded mass on grass and reeds overhanging a pool, and each mass may contain up to 450 eggs. by Oldroyd (1954). It was described from South Africa and is known from throughout the Afrotropical region apart from the Congo basin and south Yemen (Chainey and Oldroyd, 1980). Tabanus leleani Austen, 1920 Tabanus leleani Austen, 1920: Bulletin of Entomological Research, 10: 312. Chvála (1988) listed two synonym of T. leleani. Specimens examined: Saudi Arabia: 1#, Asir, Abha Farm Centre, III-VI.2001, Malaise trap, H.A. Dawah & M.A. Abdullah (NMWC); 1$, Maraba,1-17.VI.2003, Malaise trap, H.A. Dawah & M.A. Abdullah (NMWC); 4$, 2# Riyadh, 14.V.1977, sweeping, A. Talhouk (ANMA); 1$ Riyadh, 2.V.1981, sweeping, S. Tilkian (ANMA). Remarks: The male has large eyes with one band and very enlarged facets on upper three-quarter and separated from the lower quarter with small facets, palpi whitish and very stout. The female has small naked eyes with one conspicuously broad band and only an indistinct median callus. Apparently, this species can be very variable in colour (Chvála et al., 1972).

82 H.M. Al Dhafer et al. This species previously recorded from Saudi Arabia by Leclercq (1982). It was described from Palestine and has a wide distribution. It is known from the following areas: (Chva la et al., 1972; Chainey and Oldroyd, 1980; Chva la, 1988; Al-Talafha et al., 2004): Palaearctic Region: Afghanistan, Algeria, Cyprus Greece, Iran, Iraq, Palestine, Jordan, Mongolia, Morocco, Saudi Arabia, Tunisia, Turkey and USSR Oriental Region: China, India and Pakistan. Tabanus rupinae Austen, 1920 Tabanus rupinae Austen, 1920: Bulletin of Entomological Research, 10: 302. Specimens examined: Saudi Arabia: 1$ Fifa, 1.IV.1983, sweeping, A. Talhouk (ANMA). Remarks: This species has been previously recorded from Saudi Arabia by Walker and Pittaway (1987). It was described from Palestine and has since been recorded from Iran and Jordan (Chvála, 1988; Al-Talafha et al., 2004). Tabanus sabuletorum Loew, 1874 Tabanus sabuletorum Loew, 1874: Zeitschrift fu r die Gesammten Naturwissenscha. 43: 414. Chvála (1988) listed five synonym of T. sabuletorum. Specimens examined: Saudi Arabia, 1# Hufuf, 30.XI.1982, sweeping, A. Talhouk (ANMA). Remarks: This species is whitish-grey. The head of the male is large and its eyes have three bands and sharply differentiated large and small facets. The eyes of the female usually have four bands but sometimes only three. This is the only European species of the cordiger-group with more than one eye-band. A slightly variable species, but some pale specimens have antennal segment 3 mostly brownish except black terminal flagellar segments, and tergites 2 and 3 are slightly translucent brownish at sides (Oldroyd, 1954). by Leclercq (1982) It was described from Iran and has since been recorded: Palaearctic Region: Europe, Iran, Mongolia and Saudi Arabia. Oriental Region: China and India (Chva la et al., 1972; Chva la, 1988). Tabanus sufis Jaennicke, 1867 Tabanus sufis Jaennicke, 1867: Abhandlugen hrsg. Von der Senckenbergischen Naturforschenden Gesellschaft, 6: 332. Chvála (1988) listed two synonym of T. sufis, of which one was listed by Chainey and Oldroyd (1980). Specimens examined: Saudi Arabia, 4$, Asir, Maraba, 1-17.VI. 2003, Malaise trap, H.A. Dawah & M.A. Abdullah (NMWC); 1$, Asir, Maraba,1-30.V. 2004, Malaise trap, H.A. Dawah & M.A. Abdullah (NMWC); 1$, Al-Rakaba, Alhurytha, 3.II.2006., sweeping, H.A. Dawah (NMWC); 1$, Dawaseer, Aljoba Village, 1.111-30.iv.2005, Malaise trap, H.A. Dawah & M.A. Abdullah (NMWC), 1$, Riyadh, 14.V.1977, A. Talhouk (ANMA), sweeping; 2#, Alqatif, 15.XI.1985, A. Talhouk (ANMA), sweeping; 1$ Riyadh, 15.II.1981, sweeping, Elmadi (ANMA); 5$, 1#, Alqatif, 15.XI.1985, sweeping, A. Talhouk (ANMA); 1$, 1#, Hufuf, 30.XI.1982, sweeping, A. Talhouk (ANMA); 1$ Riyadh, 8.I.1985, sweeping, A. Talhouk (ANMA); 1#, Jizan, 10.II.1982, sweeping, Elmadi (ANMA); 2$, 2#, Fifa, 1.IV.1983, sweeping, S. Tilkian (ANMA); 1$, Fifa, 31.X.1984, sweeping, A. Talhouk (ANMA); 2$, 1#, Alkarj, 75 km. S.Riyadh, 3.VIII.1980, sweeping, A. Talhouk (ANMA); 1$, Riyadh, VIII, no further data KSMA; 1$, Al- Karj 28.X.1980, sweeping, Abu-Zuhairah (ANMA); 1$, Najran 15.IV.1983, sweeping, no further data (KSMA). Remarks: Both sexes of this species are distinguished from the other member of Tabanus sufis-group by the transverse rectangular brown facial band which runs from eye to eye through the bases of the antennae. This species is gray in colour and has a characteristic abdominal pattern, with the sublateral spots oblique and present on every segment, while the elongate median spots are less conspicuous or absent. by Leclercq (1986). It was described from Sudan, and has since been recorded from the following areas (Chainey and Oldroyd, 1980; Chva la, 1988; Al-Talafha et al., 2004): Palaearctic Region: Egypt, Ethiopia, Iraq, Iran, Palestine and Jordan. Afrotropical Region: Tanzania, Chad, Ethiopia, Kenya, Mauritania, Nigeria and Tanzania; Oriental Region: India. Acknowledgements Dr J.C. Deeming (National Museum of Wales, Cardiff, UK) for identifying the species of Tabanidae, commenting on the manuscript and taxonomic advice; Dr C.J. 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