Introduction       Materials and Methods    Results    Discussion   Tables

Introduction

Bluetongue (BT) disease affects wild and domestic ruminants and is widely distributed globally. Biting midges of the genus Culicoides transmit bluetongue viruses, and the distribution and abundance of the vector are thought to account for the seasonal and spatial distributions of BT (1). Several attempts have been made to relate climatic factors to outbreaks and spread of BT in various regions (2, 3, 4). Walker and Davies (5) found in Kenya that numbers of several dominant Culicoides species, including the principal vector C. imicola (=pallidipennis) greatly increased after the rainy season. They postulated a causal relationship between peak rainfall in April-May, peak numbers of Culicoides in May-June and peak bluetongue prevalence in June-July. However, Davies (6) did not find that rainfall affected serological conversion rates of sentinel cattle to BT viruses in Kenya. Wright et al. (4) related weather variables to seroconversion in cattle to bluetongue in Alabama, USA; while the best predictors were mean daily hours of wet vegetation (as the result of dew) and total rain days during the second weekly period prior to sample collection. The most thorough studies have been done in Australia, where Ward (3) studied 18 climatic variables: Daily maximum temperature and average annual rainfall best explained the variability in the prevalence of BT. Subsequent modeling efforts (7) showed that spring rainfall and minimum temperatures had the greatest effects on predicted transmission; periodic disruptions (drought) introduced cyclic instability into the model, mirroring patterns that are sometimes seen naturally.

Movement of Culicoides species in Australia has been associated with northerly winds (8) and that in Israel with a summer north-westerly wind system termed the Persian Trough (9). Most outbreaks of BT in Israel occur from mid-summer (July) to the onset of cold winter temperatures (November-December) paralleling the activity of the Persian Trough and the buildup of large numbers of C. imicola vectors (9) with high vectorial capacity (10, 11). Similar climatic factors prevail over the eastern Mediterranean, and the situation in Israel should be representative of this area. The present study was undertaken to elucidate which climatic factors, or combination thereof, determine BT prevalence in Israel. We also investigated whether BT-free zones might exist in Israel.

Materials and methods

Data on BT outbreaks in sheep flocks were available from the Epidemiological Quarterly of the Israeli Veterinary Services. Climate data were obtained from the Israeli Meteorological Service. The rainfall data were regional averages taken from 22 meteorological stations (Table 1) whose distribution was related to the size of the BT-affected area. i.e., more meteorological stations were included for a larger affected area than for a smaller affected area. Data characterizing winter frost days and spring Sharav days (Sharav day=a day with maximum temperature of 330C or more, and relative humidity at 1400 h of 25% or less) were taken from the Kefar Blum meteorological station, where the probabilities for frost and Sharav days are high. This northern locality is representative of the climate of the inland valleys.

Two types of analyses were conducted: linear correlations between BT outbreak frequencies in sheep flocks versus selected climatic factors; and climatological comparisons of years with many BT outbreaks (> 30) versus years with 0 to 1 BT outbreak. Correlations were examined between BT outbreak frequencies (number of outbreaks) and climatic data over a 20-year period (1970-1989). The following climatic factors were tested: 1. Seasonal (September-May) rainfall (mm); 2. Spring (March-May) rainfall (mm); 3. Number of nights between November and March during which the minimum temperature was <50C; 4. Number of frost nights (November-March); 5. Number of consecutive frost nights (November-March); 6. Number of consecutive nights (November-March) with temperature of 20C and below; 7. Number of spring (April-May) Sharav days; 8. Number of spring days with maximum temperature of 350C and above; 9. The highest daily maximum temperature of the year. A detailed analysis was done, to compare climatic factors prevailing before each of four years with many BT outbreaks (>30) (1975, 1987, 1988 and 1994) versus climatic factors for four years with 0-1 BT outbreaks (1980, 1981, 1983 and 1992). The values of each climatic factor in low-BT and high-BT years were compared by t-test. It was assumed that extreme temperatures (very low or very high) and drought prevailing in a certain year would reduce the number of surviving vectors in the following year. Data for this analysis were taken from two meteorological stations: Kefar Blum in the north and Bet Dagan on the central coastal plain, where the frequency of frosts and Sharav days is lower than in Kefar Blum. For each of the four-year groupings, the following averages of meteorological parameters were tested: 1. Average maximum temperature (0C) of the coldest winter month (December-March); 2. Average maximum winter temperature; 3. Minimum winter temperature; 4. Number of days with maximum temperature of 130C or above in January-February; 5. Number of days with maximum temperature of 180C or above in January-February; 6. Number of winter (December-March) nights in which the minimum temperature was 50C or below; 7. The average amount of rainfall at 22 meteorological stations; 8. Spring (April 1 to June 15) maximum temperature; 9. Number of Sharav days in the spring (March-May); 10. The average amount (mm) of spring rainfall as measured at 22 meteorological stations.

Culicoides trapping: Where data were available, the numbers of Culicoides at the various localities were related to specific regions or seasons. Collections were made in DuToit suction light traps (12) equipped with mercury vapor lamps (HPW125 W-TS, Belgium). Bet Dagan, in the central Coastal Plain served as a permanent trapping station, where Culicoides were collected either throughout the summer or throughout the year. Collections at Bet Dagan were made at the byre of the Veterinary Institute, the byre of the Volcani Center, or at both sites. At Bet Jann, Upper Galilee, 36 suction light trap collections were made between August 25 and October 6, 1981. At En Kerem in the Judean Hills, 30 suction light trap collections were made between September and December 1978. At Yotvata in the Arava Valley, two suction light trap collections were made in August 1982.

Introduction       Materials and Methods    Results    Discussion   Tables

Results

The average maximum temperatures of the coldest month (usually January) in Israel are shown in Fig. 1. Temperatures between 12.5 and 180C, which are thought to enable the survival of BT viruses in vectors during winter (13) prevail over most of the country. The exceptions are hills above 700 m (<12.50C) and the Arava and Jordan Valley (>180C). There was no correlation between the 10 individual climatological parameters and the numbers of BT outbreaks in sheep during 1970-1989 (Table 2). Temperatures in the four winters that preceded seasons with many outbreaks and those that preceded seasons with no (or few) outbreaks are shown in Table 3. Seasons with many outbreaks were preceded by winters in which the average maximum temperature of the coldest month was 2 to 30C warmer (P=0.0009). In addition the average maximum and the average minimum temperatures of the entire winter (December-March) were 1 to 1.50C warmer in winters preceding high-incidence years (P=0.0061). High-incidence years were preceded by winters (January-February) with more days in which the maximum temperature was > 130C (P=0.0346) and >180C (P=0.0002). The number of spring Sharav days was not useful to distinguish high-incidence from low-incidence years. Low incidence years were preceded by wet winters, with 40% more rainfall on the average of the coldest month than those which preceded by high-incidence years (and which had approximately normal rainfall) (P=0.0058). The overall amount of rainfall in years without outbreaks was, on average, 17% higher than that in years with many outbreaks. The data of Table 3 indicate that average maximum temperatures below 16.50C in the coldest month of winter were associated with a low probability of BT outbreaks in the following summer. Likewise, winters with more than 18 days with temperatures above 180C were associated with a high probability of BT outbreaks in the following summer. The mountains (700 m above sea level) had no reported BT outbreaks, and the Arava desert valley (e.g., Yotvata, 75 m above sea level) recorded only a single BT case during 1970-1989. These areas have fewer Culicoides vectors than a typical BT area such as Bet Dagan (Table 4). Table 5 shows the numbers of vectors, namely C. imicola, trapped in June, one month before the usual outbreaks of BT in sheep. There were large differences in the numbers of Culicoides spp. at the two sites at Bet Dagan and between the numbers collected in 1982 and in 1996. In the absence of a source of infection, even a C. imicola population yielding 345 insects per night per trap at the Volcani Center in 1982 did not result in a BT outbreak (Table 5). Table 6 shows the numbers of Culicoides spp. trapped nightly during the BT-free season, i.e., winter of 1997/8. The numbers of the vector C. imicola ranged from 170 in November 1997 to 6 in February and March 1998. The Rehovot District (Fig. 2), which includes Bet Dagan, contains large numbers of reservoir animals, i.e., dairy cattle, it is not surprising therefore that the BT virus is active in this area. In contrast parts of the Be'er Sheva District, which includes the flat Arava, and the Jerusalem and Akko Districts, which are hilly and contains smaller numbers of cattle that may serve as BT reservoirs.  

Introduction       Materials and Methods    Results    Discussion   Tables

Discussion

Climatic variables presumably influence BT spatial and seasonal distributions through modifications of vector capacity and abundance. Vector capacity incorporates biting rates, vector survival, extrinsic incubation (time required between ingesting the virus and becoming infective), and vector competence (ability of the vector to become infected by the virus). Our analysis concentrated more on winter climate parameters than on summer ones, since in the eastern Mediterranean summer parameters are stable whereas the winter ones are variable (14, 15). The importance of winter was confirmed in a recent study in Spain, where it was reported that C. imicola predominated in a zone with the highest minimum and maximum temperatures during the winter (16). Both temperature and rainfall appear to be significant.

Temperature: Temperature has a profound influence on several of these vector capacity components. Our temperature analysis shows that, theoretically, BT virus types should be able to survive the winters, at least in part, in infected insects throughout the entire country, except in the mountains above 700 m. Extrinsic incubation of BT virus in the vectors is temperature dependent: in the laboratory, C. sonorensis, BT virus remained in a quiescent state for at least 22 days, but it replicated rapidly when infected insects were exposed to higher temperatures (17). The virus is assumed to survive above a temperature threshold of 12.50C (13), which is below the activity threshold for flight of C. imicola. While C. imicola may be collected on warm winter evenings, its minimum temperature for flight is 17-180C (18). It has been suggested in other subtropical areas that are within its wide range, that winter persistence of infected C. imicola provides at least a partial means of over-wintering for BT viruses (19, 20).

Developmental rates, and, therefore, the generation interval of a multivoltine insect such as C. imicola, are considerably shorter at higher temperatures (see, e.g., 21), which might enable population densities to increase more quickly. In winter larvae of C. imicola do not hibernate, but develop at a slower pace, so that higher winter temperatures might lead to a larger spring generation. The length of the gonotrophic cycle, particularly the time required from blood ingestion to egg development, is also much shorter at higher temperatures, provided they are below the upper threshold limits (22). Thus individual vectors should feed more often, increasing opportunity for transmission over a defined time period. These factors would act to encourage BT activity at higher temperatures. Indeed Rawling et al. (23) suggested that the presence of C. imicola in Iberia is favoured by high summer temperatures, possibly in conjunction with the seasonal low relative humidity. No significant relationships between the presence of C. imicola and winter temperatures and relative humidity were found. On the other hand, it is expected that daily survival would be lower at higher temperatures, such as those prevailing in the Arava. The fact that the preferred climatic conditions for reaching peak populations of C. imicola always occur everywhere in Israel in the autumn (September- November), when night temperatures are lower and relative humidity is higher than in the summer, reflects a different situation from that in Spain (23). The prevailing high winds in the Arava probably regularly suppress the host-seeking activity of C. imicola and increase their mortality, as was suggested previously (24, 25). However, Braverman et al. (11) found that C. imicola collected in light traps in the Coastal Plain, where temperatures are more permissive maintained a high parity level (stage survival) during the mid summer and early fall months. Survival between blood meals was actually highest in August on the Coastal Plain (Bet Dagan).

Our analysis suggests that warm winters, which encourage survival in C. imicola, precede periods of substantial BT transmission. This could be a result of reduced mortality and higher overwintering populations of the vector but, except for the Bet Dagan area, we lack concurrent long-term vector monitoring data to substantiate this. The above suggestion does not mean that BT outbreaks will actually occur after every warm winter; the very dry and warm winters of 1998 and 1999 were followed by summers with few BT outbreaks only in 1998. C. imicola is essentially an African species, more adapted to high temperatures than low ones. Warm spring Sharav days had no detectable influence on BT occurrence, probably because winter-induced C. imicola mortality had already occurred and preceded the Persian Trough air stream that starts in the 2nd half of June and is believed to introduce BT-infected vectors (9).

Rainfall: Because the immature stages of C. imicola are found in areas of damp or wet manure/organic soil, one might assume that rainfall would have a major positive influence on vector population densities. A recent study used the Normalized Difference Vegetation Index (NDVI), a satellite-derived measure of photosynthetic activity, to evaluate relative abundances of C. imicola (24). Abundances were positively correlated with the average and minimum NDVI (NDVImin), an index which is strongly correlated with total annual rainfall. In the eastern Mediterranean the rainy season is limited to the winter, and our analysis suggests that very wet winters result in reduced BT transmission the following summer. An important reason for this is that heavy rains inundate and erode the breeding sites of C. imicola. Ample rainfall-independent development sites for C. imicola are found near water troughs, etc., in and around livestock yards (26, 27). Unlike the situation in Morocco and Iberia (24) grass-covered wet sites were found to be poor biotopes for C. imicola. Irrigated fields and horticultural crops in Israel are also not dependent on rainfall, and provide breeding sites for C. schultzei gp. and other species (not C. imicola). The negative influence of rainfall is more likely due to the fact that wetter winters are also much cooler, which may reduce vector survival. A contradictory phenomenon was found in South Africa regarding C. imicola and African horse sickness (AHS) outbreaks. It was found that a spell of drought succeeded by heavy rainfall was followed by AHS epizootics (28).

Wind patterns: It is as yet unclear to what extent the BT virus overwinters in vectors in Israel, as opposed to overwintering in vertebrate reservoirs, exploiting seasonal animal movement (limited to the Bedouin's flocks, who raise non-susceptible animals), or potential seasonal introduction via airborne vectors. The local air stream in the Arava valley flows from the Dead Sea southward through the Red Sea region. Constant winds between 20:00 and 23:00 h have a velocity of 15 km/h, and this might actually suppress flight activity, prevent biting during the main feeding hours and result in increased mortality of C. imicola (25, 29). The detrimental effects of high wind speeds on C. imicola are due to desiccation, prevention of feeding and physical removal. High wind speeds have the potential to move insects considerable distances quickly, but this is difficult to demonstrate. Despite this, one may consider the potential influence of the air stream on vector introduction into the two candidate regions we propose as BTV-free zones.

Candidate bluetongue-free zones: Based on historical BT records, the disease is basically unknown in two regions of Israel-mountainous areas and the Arava Desert (30). Mountainous regions above 700 m, although in the path of the Persian Trough airstream (15), have several characteristics that suggest they will remain BTV-free for at least the near future. First, numbers of C. imicola are relatively low, and substantial overwintering is unlikely. Animal densities are relatively low (Fig. 2), and species composition is dominated by goats, mainly of the Mamber breed, and local sheep breeds, mainly Awassi, which are fairly resistant to BT (31, 32) and are not preferred hosts for the vector, C. imicola (33). This area is likely to remain BT-free until more susceptible ruminants are introduced. Higher standards of living might result in the introduction of more cattle and European sheep breeds, which could, in turn, result in more BT transmission. This would be especially true for dairies, which provide disproportionately suitable developmental sites for the vector. The Arava Desert also has a relatively small number of C. imicola. The growing numbers of dairies in this area are likely to increase vector numbers, but very high summer temperatures also should result in poor survival of the vectors and thus maintain low vector capacity (11, 36). The Arava Desert should be investigated thoroughly to check whether it is a valid BTV-free area. The indication of probably being BTV-free is supported by the fact that in the Southern Arava serological survey in sentinel cattle showed that they have been free of BTV at least 13 years (30). However, this region may also serve as a source of C. imicola innoculum for more northerly regions in spring and early summer, particularly after winter mortality in those cooler climates, and given the prevailing wind patterns. The density of C. imicola in the Arava will rise with the growing numbers of new dairies there but, as the Arava is beyond the Persian Trough system (15) and because of the supraoptimal temperatures prevailing in the summer, the survival of the C. imicola population may be too low for transmitting BT (11, 36). Probably an additional limiting factor, for the survival of C. imicola at present is the scarcity of carbohydrate sources. This might change as the areas of irrigated crops and trees increase in the future. Therefore, the Arava should be considered as a probable BT-free safe zone, at present.

Routine monitoring of the vector C. imicola is advisable, particularly near animals, in these proposed BTV-free zones. Trap collections are highly variable and, therefore, must be interpreted cautiously. On the assumption that light trap collections in some way approximate biting rates, it is possible approximately to relate collections to risk, pending more definitive research. Holbrook (35), for example, reported no observed BT transmission to sentinel sheep at light trap collections below ca. 35-40 C. sonorensis females/trap. From our extensive observations at Bet Dagan, where BT often occurs (but seasonally), DuToit light trap collections in cow sheds of ca. 345 C. imicola or above tend to be associated with BT outbreaks. If vector populations of such magnitude exist in an area when BT viruses are introduced by some means, substantial transmission might be expected. In simulation studies of African horse sickness in Spain, it was found that during an outbreak the proportion of infected C. imicola never exceeded 3% and that below a threshold of ca. 11,000 C. imicola per host no outbreaks occurred (23). Further studies would be useful to refine this rough figure and relate it to specific fluctuations in vector capacity components.

Acknowledgements

We are obliged to Dr. E. Rapaport of the Veterinary and Animal Health Services, Afula for providing the data on outbreaks of BT in sheep, to Dr. A. Gnizi and Mrs M. Zarchi of the Volcani Centre for performing the statistical analysis and to Dr. M. Van Ham of the Israeli Veterinary and Animal Health Services, Bet Dagan for providing the figures on farm animal abundance in the various districts.

Introduction       Materials and Methods    Results    Discussion   Tables

References

1.  Gibbs, E. P. J. and Greiner, E. C.:  The epidemiology of bluetongue. Comp. Immunol. Microbiol. Infect. Dis. 17: 207-220, 1994.

2.  Braverman, Y. and Galun R.:  The occurrence of Culicoides in Israel with reference to the incidence of bluetongue. Refuah Vet. 30: 121-127, 1973.

3.  Ward, M.P.: Climatic factors associated with the prevalence of bluetongue virus infection of cattle herds in Queensland, Australia. Vet. Rec. 134: 407-410, 1994.

4.  Wright, J.C., Getz, R.R., Powe, T.A., Nusbaum, K.E., Stringfellow, D.A., Mullen, G.R. and Lauerman, L.H.:  Model based on weather variables to predict seroconversion to bluetongue virus in Alabama cattle. Prev. Vet. Med. 16: 271-278, 1993.

5.  Walker, A.R. and Davies, F.G.: A preliminary survey of the epidemiology of bluetongue in Kenya. J. Hyg. Camb. 69: 47-60, 1971.

6.  Davies, F.G.:  Bluetongue studies with sentinel cattle in Kenya. J. Hyg. Camb. 80: 187-204, 1978.

7.  Ward, M. P. and Carpenter, T. E.:  Simulation modeling of the effect of climatic factors on bluetongue virus infection in Australian cattle herds. Prev. Vet. Med. 27: 13-22, 1996.

8.  Murray, M. D.: The spread of ephemeral fever of cattle during the 1967-68 epizootic in Australia. Aust. Vet. J. 46: 77-82, 1970.

9.  Braverman, Y. and Chechik, F.: Air streams and introduction of animal disease borne on Culicoides (Diptera, Ceratopogonidae) into Israel. Rev. Sci. Tech. Off. Int. Epiz. 15: 1037-1199, 1996.

10. Birley, M.H., Braverman, Y. and Frish, K.: Survival and blood feeding rate of some Culicoides species in Israel. Environ. Entomol. 13: 424-429, 1984.

11. Braverman, Y., Linely, J.R., Marcus, R. and Frish, K.: Seasonal survival and expectation of infective life of Culicoides spp. (Diptera, Ceratopogonidae) in Israel with implications for bluetongue virus transmission, and a comparison of the parous rate in C. imicola from Israel and Zimbabwe. J. Med. Entomol. 22: 476-484, 1985.

12. DuToit, R. M.: The transmission of bluetongue and horse sickness by Culicoides. Onderstepoort, J. Vet. Sci. Anim. Ind. 19: 7-16, 1944.

13. Sellers, R.F. and Mellor, P.S.: Temperature and the persistence of viruses in Culicoides spp. during adverse conditions. Rev. Sci. Tech. Off. Int. Epiz. 12: 733-755, 1993.

14. Goldreich, Y.: The climate of Israel, observations, research and applications, 292 pp. Published by Bar Ilan University, Ramat Gan and Magnes Publishers, Hebrew University Jerusalem (in Hebrew). 1998.

15. Jaffe, S.: Climate of Israel. In: Yom-Tov, Y. and Tchernov, E. (eds): The Zoogeography of Israel: the distribution and abundance at a zoogeographical crossroad. Dr. W. Junk Publishers, Dordrecht, Netherlands, pp. 79-94, 1988.

16. Ortega, M.D., Holbrook, F.R. and Lloyd, J.E.: Seasonal distribution and relationship to temperature and precipitation of the most abundant species of Culicoides in five provinces of Andalusia, Spain. J. Am. Mosq. Control Assoc. 15: 391-399, 1999.

17. Mullens, B.A., Tabachnick, W.J., Holbrook F.R. and Thompson L.H.: Effects of temperature on virogenesis of bluetongue virus serotype 11 in Culicoides variipennis sonorensis. Med. Vet. Entomol. 9: 71-76, 1995.

18. Braverman, Y.:  Host detection, hourly activity, and the preferred biting sites of Culicoides imicola (Diptera, Ceratopogonidae) in: Bluetongue, African Horse Sickness and Related Orbiviruses, Proc. 2nd. Intern. Symp. CRC Press, Boca Raton, Ann Arbor. pp. 327-332, 1992.

19. Baylis, M., El Hasnaoui, H., Bouayoune, H., Touti, J. and Mellor, P.S.: The spatial and seasonal distribution of African horse sickness and its  potential Culicoides vectors in Morocco. Med. Vet. Entomol. 11: 203-212, 1997.

20. Nevill, E.M.: Cattle and Culicoides biting midges as possible over-wintering host of bluetongue virus. Onderstepoort J. Vet. Res. 38: 65-72, 1971.

21. Akey, D.H., Potter, H.W. and Jones, R.H.: Effects of rearing temperature and larval density on longevity, size, and fecundity in the biting gnat Culicoides variipennis. Annl. Entomol. Soc. Amer. 71: 411-418, 1978.

22. Mullens, B.A. and Holbrook, F.R.: Temperature effects on the gonotrophic cycle of Culicoides variipennis (Diptera: Ceratopogonidae) J. Amer. Mosq. Contr. Assoc. 7: 588-591, 1991.

23. Rawlings, P., Capela, R., Pro, M.J., Ortega, M.D., Penna, I., Rubio, C., Gasca, A. and Mellor, P.S.: The relationship between climate and the distribution of Culicoides imicola in Iberia. Arch. Virol. (Suppl) 14: 93-102, 1998.

24. Baylis, M. and Rawlings, P.: Modelling the distribution and abundance of C. imicola in Morocco and Iberia using climatic data and satellite imagery. Arch. Virol. (Suppl) 14: 137-153, 1998.

25. Meiswinkel, R.: Discovery of a Culicoides imicola-free zone in South Africa: preliminary notes and potential significance. Onderstepoort. J. Vet. Res. 64: 81-86, 1997.

26. Braverman, Y., Galun, R. and Ziv, M.: Breeding sites of some Culicoides species (Diptera, Ceratopogonidae) in Israel. Mosq. News 34: 303-308, 1974.

27. Braverman, Y.: Characteristics of Culicoides (Diptera, Ceratopogonidae) breeding places in the Salisbury area, Rhodesia. Ecol. Entomol. 3: 163-170, 1978.

28. Baylis, M., Mellor, P.S. and Meiswinkel, R.: Horse sickness and ENSO in South Africa. Nature 397: 574, 1999.

29. Baylis, M., Touti, J., Bouayoune, H., Moudni, L., Taoufiq, B. and El Hasnaoui, H.: Studies of the mortality rate of Culicoides imicola in Morocco. Arch. Virol. 14:127-136, 1998.

30. Anonymus: World Animal Health in 1997. Part I, Reports on the animal health status and disease control methods and tables on incidence of list A diseases, p. 195, 1997.

31. Barzilai, E. and Tadmor, A.: Multiplication of bluetongue virus in goats following experimental infection. Refuah Vet. 28: 11-20, 1971.

32. Dafni, I.: Bluetongue in Israel in the years 1964 and 1965. Bull. Off. Int. Epiz. 66: 319-327, 1966.

33. Braverman, Y., Boreham, P.F.L. and Galun, R.: The origin of blood meals of the female Culicoides pallidipennis trapped in a sheepfold in Israel. J. Med. Entomol. 8: 379-381, 1971.

34. Lord, C.C., Woolhouse, M.E.J. and Mellor, P.S.: Simulation studies of African horse sickness in Spain. Arch. Virol. (Suppl) 14: 103-111, 1998.

35. Holbrook, F.R.: Research on the control of bluetongue in livestock by vector suppression. In: Barber, T.L.,  Jochim, M.M. and  Osburn, B.I. (eds.): Bluetongue and Related Orbiviruses. Alan R. Liss, Inc. New York. pp. 617-620, 1985.

36. Wellby, M.P., Baylis, M. Rawlings, P. and Mellor, P.S.: Effects of temperature survival and rate of virogenesis of African horse sickness virus in Culicoides variipennis sonorensis (Diptera, Ceratopogonidae) and its significance in relation to the epidemiology of the disease. Bull. Entomol. Res. 86: 715-720, 1996.

  Tables

 Table 1      Table 2       Table 3     Table 4     Table 5     Table 6  

Introduction       Materials and Methods    Results    Discussion   Tables

 Table 1: Stations from which precipitation data were taken for the BT study

 Table 1      Table 2       Table 3     Table 4     Table 5     Table 6  

Introduction       Materials and Methods    Results    Discussion   Tables

Table 2: Coefficient of correlation between number of BT outbreaks in sheep flocks in Israel in the years 1970-1989 to selected climatic factors at Kefar Blum

*Average from 22 meteorological stations

 Table 1      Table 2       Table 3     Table 4     Table 5     Table 6  

Introduction       Materials and Methods    Results    Discussion   Tables

Table 3: Comparison of the meteorological features at two localities of years with many bluetongue outbreaks in sheep flocks to poor bluetongue years

Years with bluetongue epizootics (>30 flocks)  

 Table 1      Table 2       Table 3     Table 4     Table 5     Table 6  

Introduction       Materials and Methods    Results    Discussion   Tables

Table 4: Numbers of Culicoides spp. suction light trapped in the mountain and Arava areas, i.e., bluetongue free zones versus Bet Dagan zone where bluetongue prevails

 Table 1      Table 2       Table 3     Table 4     Table 5     Table 6  

Introduction       Materials and Methods    Results    Discussion   Tables

Table 5: Average numbers per night, per trap of Culicoides spp. suction light trapped in two sites at Beit Dagan, Rehovot district in June, a month before the bluetongue season  

 Table 1      Table 2       Table 3     Table 4     Table 5     Table 6  

Introduction       Materials and Methods    Results    Discussion   Tables

Table 6: Numbers of Culicoides species per night per trap in the winter of 1997/98
           (November 1997-March 1998)

 Table 1      Table 2       Table 3     Table 4     Table 5     Table 6  

Introduction       Materials and Methods    Results    Discussion   Tables