Abstract: Scanty information is available about the Culicoides Latreille (Diptera: Ceratopogonidae) fauna of Saudi Arabia. This study was undertaken to investigate the distribution of Culicoides species in the kingdom. In this study, which was conducted during the period March 2004 to February 2006, light traps collected 43505 specimens of Culicoides biting midges. Eight species of Culicoides were identified: Culicoides bahrainensis Boorman, C. imicola Kieffer, C. kingi Austen, C. navaiae Lane, C. newsteadi Austen, C. oxystoma Kieffer, C. punctatus Meigen and C. sahariensis Kieffer. Among these species, C. bahrainensis was reported for the first time in Saudi Arabia. A recent and up to date distribution map of Culicoides in Saudi Arabia is provided and the medicinal importance of some of these species was discussed.
INTRODUCTION
Culicoides Latreille (Diptera: Ceratopogonidae) or the biting midges are very small haematophagous insects measuring from 1-3 mm in size. More than 1400 species have been identified and they occur on all large landmasses, with the exception of Antarctica and New Zealand, ranging from the tropics to tundra and from sea level to 4000 m.a.s.l. (Mellor et al., 2000).
The role of Culicoides in disease transmission has been reviewed by many workers (Toit, 1944; Kettle, 1965; Linley et al., 1983; Lane, 1983; Boorman, 1989; Lane and Crosskey, 1993; Mellor et al., 2000). More than 50 viruses have been isolated from Culicoides species and the most important of these are African Horse Sickness Virus (AHSV), Blue Tongue Virus (BTV), Akabane Virus (AKAV) and Bovine Ephemeral Fever Virus (BEFV). Some species of Culicoides cause considerable nuisance through their bites (Linley et al., 1983).
The climate can influence the distribution of Culicoides. Low temperatures tend to be more significant than high temperatures as determinants of distribution (Gates, 1993). When the temperature is suitable, precipitation can influence the distribution of Culicoides through its effects on availability of breeding sites. Wind speed and direction can also affect Culicoides distribution (Wittman and Baylis, 2000). The climatic factors can also influence the vectorial capacity of a Culicoides population both through changes in the overall size of the adult population and in the proportion of adults within the population capable of transmitting viruses (Wittman and Baylis, 2000). The recent spread of bluetongue and African horse sickness viruses in Europe has been attributed to climate change (Summer, 2009).
Although, several reports on the distribution of Culicoides in Saudi Arabia are available (Lane, 1983; Boorman, 1989; Abu-El-Zein et al., 2002; Hilali et al., 2003; Boorman and Harten, 2003; Alahmed and Kheir, 2005) but, very little is known about Culicoides fauna in Saudi Arabia. Despite reports of severe outbreaks of arboviral diseases in domestic animals in Saudi Arabia (Anderson et al., 1989; Abu-El-Zein et al., 1998a, b), but very little effort has been made to study the potential vectors of these diseases such as Culicoides. More, recent information on distribution and seasonal activity of Culicoides species in Saudi Arabia is required to assess the economic losses due to this serious haematophagous pest. In this study, an attempt was made to investigate the distribution of Culicoides species in Saudi Arabia.
MATERIAL AND METHODS
Study Area
Saudi Arabia is a vast country with an area of about 2.25 million km2.
It lies in the Southwestern part of Asia between lat. 15° 44' N-32°
9' N and long. 34° 24' E-55° 39' E (Fig. 1). The kingdom
is an extremely arid area, except the Southwestern region and some coastal zones.
The mountains in the South and the West, plateaus in the North and the Center,
sand dunes and desert in the East and some scattered valleys characterize the
topography of the kingdom (Brown, 1968; Mohammedein,
2001).
| Fig. 1: | Collection sites of Culicoides sp. in Saudi Arabia |
The Southwestern part of Saudi Arabia, which is a mountainous area, is divided into 3 distinct topographical zones depending on the geographical characteristics: Sarawat Asir (which is mountain series extending North-South along the coastal plains of the Red Sea), Asir Plateau and Tihama lowlands (Fig. 1).
Most of the Eastern region of Saudi Arabia is a desert, which includes the part of the kingdom located along the Arabian Gulf between Sultanate of Oman in the South and Kuwait in the North. The region is separated from the interior by the sand dunes known as Al Dahna and is bordered to the South by Al Rub, Al Khali or the Empty Quarter desert.
Al Qassim region is located at the heart of the kingdom and has a typical desert climate, which is cold rainy in winter and hot dry or with low humidity in summer. Al Qassim region is divided by Wadi Al Rumma (Rumma Valley), which is the longest valley in Arabian Peninsula, from the West to the Northeast. The region lies at an altitude of 600-750 m.a.s.l., and it is gliding from West to East in general. Agriculture is the cornerstone of the region’s economy and it produces corn, dates, citrus and some vegetables.
The Western coastal escarpment can be considered as two mountain ranges separated by a gap at the vicinity of Makka Al Mukarrama. The Northern range seldom exceeds 2100 m.a.s.l. and the elevation gradually decreases towards the South to about 600 m around Makka Al Mukarrama, with some coastal plains. The climate is hot dry in summer and warm, slightly humid in winter. The vegetative cover is very poor in the study area, except for some coastal zones. Al Madinah Al Munawwarah region is an upland plateau scored by numerous valleys (wadis) covered with grasses and scrub vegetations which are used for pasture. It has a typical desert climate, which is cold rainy in winter and hot dry in summer. Al Madinah Al Munawwarah is one of the biggest oases in the region and famous for growing dates. The topography of the of the Northern region is characterized by the presence of high plateaus which are extension of Badiat Al Sham. The climate and vegetation of Saudi Arabia has been studied by several authors (Khattab and El-Hadidy, 1971; Mandaville, 1973; Abuelfatih and El-Khalili, 1978).
Collection and Identification of Culicoides
Culicoides biting midges were collected during the period March
2004 to February 2006, during a country-wide survey for mosquitoes (Diptera:
Culicidae). For collection, 18 collection sites representing different ecological
zones in the kingdom were selected (Fig. 1). Culicoides
were collected using one Center for Disease Control miniature light trap (CDC
light traps) and one standard New Jersey (NJ) light trap (Bioquip Company, Gardena,
CA, 90248-3602, USA) in each collection site. The CDC and the NJ light traps
were attached to a battery that supplies power and installed permanently near
suitable breeding sites of Culicoides such as near animal farms with
aquatic habitats, human habitations and animal housings. The light traps were
operated once every 2 weeks from sunset at 18:00 to sunrise at 06:00 h the following
day throughout the study period. The collected adult Culicoides in the
light traps were taken and recorded, then preserved into 70% ethyl alcohol in
glass vials with screw caps, labeled and sent to the Entomology Laboratory,
College of Food and Agricultural Sciences, King Saud University, Riyadh. The
collected Culicoides sp., were identified by Dr. Art Borkent, from Royal
British Columbia Museum in Victoria, British Columbia, Canada and American Museum
of Natural History, New York, USA according to the method described by Borkent
and Bissett (1990).
RESULTS AND DISCUSSION
In this study, 43505 specimens of Culicoides, which represented eight species, were collected and identified as: Culicoides bahrainensis Boorman.; C. imicola Kieffer; C. kingi Austen; C. navaiae Lane; C. newsteadi Austen; C. oxystoma Kieffer; C. punctatus Meigen and C. sahariensis Kieffer (Table 1). Among these species, C. bahrainensis was reported for the first time in Saudi Arabia from Al Hassa and Al Dammam on Arab Gulf and Jeddaha on the Red Sea (Fig. 1). Two specimens were identified as C. montanus and C. langeroni, but not with high certainty until more specimens are available (especially males of these species). The two-suspected species were reported earlier in the Arabian Peninsula (Boorman, 1989).
Among the total Culicoides collected in the kingdom, C. imicola and C. punctatus were the most abundant species and they represented 19.51 and 19.31% of the total collection, respectively, followed by C. kingi (17.49%), C. oxystoma (15.31%), C. navaiae (11.18%), C. newsteadi (9.02%), C. bahrainensis (5.31%) and C. sahariensis (3.05%). The highest number of Culicoides was collected from Al Hassa (10.95%) and Al Dammam (10.62%), followed by Jeddaha (9.93%), Riyadh (8.53%), Abha (7.56%), Al Qassim (7.31%), Makka Al Mukarrama (7.04%), Jazan (6.87%), Hail (5.77%), Al Madinah Al Munawwara (4.51%), Hafr Al Batin (3.85%), Najran (3.72%), Al Jouf (3.14%), Al Taif (3.05%), Addawadmi (2.22%), Wadi Addawasir (2.16%), Al Baha (2.09%) and Tabouk (0.68%) (Table 1).
Out of 4765 Culicoides specimens collected at Al Hassa, 9.61% were Culicoides bahrainensis, 20.61% were C. imicola, 7.53% were C. kingi, 15.01% were C. navaiae, 13.81% were C. oxystoma and 33.43% were C. punctuates (Table 2). Similarly, 2308 specimens of C. bahrainensis were collected during this study, 458 (9.61%) of them were collected from Al Hassa, 872 (18.87%) from Al Dammam and 978 (22.63%) from Jeddaha. The relative percent abundance of each Culicoides species in each collection site is shown in Table 2.
In this study, 8 species of Culicoides were encountered and some of them were important vectors of some arboviruses (Lane, 1983; Anderson et al., 1989; Mellor and Boorman, 1995; Mellor et al., 2000). Culicoides kingi, which is the main vector of bovine ephemeral fever in Kenya (Davies and Walker, 1974) and onchocercaisis in Sudan (El-Sinnary and Hussein, 1980), was reported earlier in Saudi Arabia from Central and Eastern Regions (Boorman, 1989). In this study, it was encountered for the first time in the Northern region (Al Jouf, Tabouk and Hail), Western region (Makka Al Mukarrama and Jeddaha) the Southwestern region (Al Baha, Abha, Najran and Jazan), Wadi Addawasir, Addawadmi and Al Qassim. Nothing is known about its biology and medical importance in the kingdom.
| Table 1: | Distribution of Culicoides sp. in Saudi Arabia |
| Table 2: | Percent distribution of Culicoides sp. in each collection site in Saudi Arabia |
Culicoides oxystoma is broadly distributed species throughout the Palaearctic region, the Oriental region and possibly even Northen Australia. In Saudi Arabia, it was reported from Central and Eastern regions (Lane, 1983; Boorman, 1989). In this study, it was reported for the first time from the Northern region (Al Jouf and Hail), Western region (Makka Al Mukarrama, Al Madinah Al Munawwara, Al Taif and Jeddaha), the Southwestern region (Abha, Najran and Jazan), Wadi Addawasir and Al Qassim. Culicoides oxystoma is a serious pest of large ungulates, including cattle. It is a potential vector of bovine ephemeral fever in Arabian Peninsula (Boorman, 1989) and also associated with the transmission of some filariae to livestock in the Sudan (El-Sinnary and Hussein, 1980). Kurogi et al. (1987) isolated Akabane virus from C. oxystoma in Japan. The widespread of Culicoides kingi and Culicoides oxystoma in Saudi Arabia may lead to appearance of bovine ephemeral fever in many parts of the kingdom in the near future and every effort should be made to prevent the spread of this disease.
In this study, C. bahrainensis was reported for the first time in Saudi Arabia from Al Hassa and Al Dammam on the Arab Gulf and from Jeddaha on the Red Sea suggesting that this species requires high humidity for its survival and development. Significant variations were observed within this species (Borkent, pers. comm.) and it may be that this species is conspecific with C. badooshensis and C. kurensis which are more broadly distributed throughout much of Western Palaearctic region (Boorman, 1989). Another possibility is that there may be more species in this species group that are not described in this study. More research is needed to better understand the taxonomy of these species. Nothing is known about the habits and biology of this Culicoides species.
In Saudi Arabia Culicoides sahariensis was reported in the Eastern region from Al Hassa and Al Hofuf (Boorman, 1989). In this study, it was reported for the first time in Saudi Arabia from Hafr Al Batin, Wadi Addawasir, Addawadmi and Al Qassim. Nothing is known about its biology and relation to disease in the kingdom.
Culicoides navaiae is known only from Bahrain and from the Eastern region in Saudi Arabia (Lane, 1983; Boorman, 1989). In this study, it was reported for the first time from Hafr Al Batin, Hail, Al Madinah Al Munawwara, Abha, Jazan and Najran regions. Further studies on biology and habits of Culicoides navaiae in Saudi Arabia are required.
Culicoides newsteadi is distributed around the Mediterranean and Middle East and often is associated with livestock. It was reported earlier in Saudi Arabia only from Al Hassa (Abu-El-Zein et al., 2002) but in this study was reported from Al Madinah Al Munawwara, Makka Al Mukarrama, Jeddaha, Al Baha, Abha, Jazan, Najran and Al Qassim. More studies on biology and habits of this Culicoides species in Saudi Arabia are needed.
Although, C. punctatus was reported in Saudi Arabia only from Al Kharj (Hilali et al., 2003) but in this study, it was widely distributed in the kingdom and reported for the first time from Al Hassa, Al Dammam, Hail, Al Jouf, Tabouk, Al Madinah Al Munawwara, Makka Al Mukarrama, Jeddaha, Al Taif, Wadi Addawasir, Riyadh and Al Qassim. Boorman (1989) reported that C. punctatus may cause an allergic reaction in horses. The habits, biology and medical importance of C. punctatus in Saudi Arabia requires further investigations.
This study has confirmed the presence of C. imicola, the main field vector of AHSV and BTV (Lane, 1983; Anderson et al., 1989; Mellor and Boorman, 1995; Mellor et al., 2000) in Saudi Arabia. The biting midge was reported earlier in Saudi Arabia from Riyadh (Alahmed and Kheir, 2005; Boorman, 1989) and from Abha, Jazan and Al Kharj (Hilali et al., 2003). In this study C. imicola was reported for the first time in Al Hassa, Al Dammam, Hail, Al Madinah Al Munawwara, Makka Al Mukarrama, Jeddaha, Al Taif, Abha, Jazan, Najran and Al Qassim. This widespread of C. imicola suggests that horses, particularly racehorses, dairy and beef cattle are potentially at risk and every effort should be made to protect beef and dairy industry in Saudi Arabia from devastating effects of this serious biting Culicoides. Further studies on the distribution and vectorial capacity of these Culicoides are required to evaluate the medical importance of these biting midges in Saudi Arabia before embarking on large scale control projects.
During a recent confirmed outbreak of bluetongue in sheep in Italy, Savini et al. (2005) collected 15 species of Culicoides and species belonging to the Obsoletus complex dominated the light trap collection. He did not collected a single specimen of the classical Afro-Asiatic blue tongue vector, C. imicola. These results indicate that a species other than C. imicola is involved in the current emergence of bluetongue in the Mediterranean basin.
Although, the number of biting midges caught in this study was relatively high, but there was no great diversity in species composition. This might be due to some limitations in the light traps used in this study, since they were permanently stationed in one place at a fixed height throughout the study period. The height of the of light trap may has an effect on the catch of Culicoides, since, Braverman and Linely (1993) showed that C. circumscriptus, C. cataneli and C. imicola were caught in greater numbers in the higher than in lower light traps, while more females of C. schultzi group were caught in lower than higher traps. In fact, species collected more frequently in higher traps may be more prone to carriage for long distances by air currents and therefore, are more likely to be important as dispersal vectors.
Changes in the distribution and abundance of Culicoides are likely to be amongst the most important and immediate effects of climate change (Mellor, 1996). This is particularly worrying in case of insects that transmit pathogens or parasites to humans and livestock, since, it is likely to affect the prevalence of insect-borne diseases. The effect of climate change on distribution and abundance of Culicoides has been discussed by Bethan et al. (2005). Further studies on the effects of temperature and rainfall on distribution and seasonal abundance of Culicoides in Saudi Arabia are required.
ACKNOWLEDGMENT
We would like to thank Dr. Art Borkent, Royal Museum and American Museum for Natural History, British Columbia, Canada, for his identification of Culicoides specimens and valuable comments on Culicoides of Saudi Arabia. Thanks are also extended to King Abdul Aziz City for Science and Technology, Riyadh, for financial support.