Bluetongue , spread by gnat, causes mouth ulcers in and lameness due to , inflammation of the hoof wall, and muscle damage. Abor- tion and congenitally deformed lambs may also occur.

Clues- - -- to-- control-- -- of- bluetonaue- -~___ virus--

Bradley A. Mullens 0 Edmond C. Loomis 0 John R. Anderson

Control strategy aimed at early life stages of vector gnats is one possibility

Bluetongue disease of California live- ers at the School of Veterinary Medicine, Although the virus can be transmitted stock and wildlife is most severe in sheep University of California, Davis, demon- from an infected dam to her offspring and in certain species of wild , strated that at least 41 percent of , through the placenta or from an infected notably white-tailed and . 42 percent of sheep, and 21 percent of bull to a heifer or cow venereally (shed in Caused by a virus, the disease is generally had been exposed to bluetongue. the semen), bluetongue is transmitted pri- subclinical in cattle, but subtle losses as- The virus was more prevalent in central marily by blood-sucking Culicoides gnats sociated with reproductive failure may be and southern California; in the (fig. 1). Knowledge of the gnat’s biology more significant than producers realize. north had less exposure to bluetongue. and details of its role in virus transmis- Cattle are considered a primary reservoir Bluetongue virus serotype 11 was most sion are of considerable importance in host for the virus, which then may be commonly isolated from infected ani- controlling this disease. spread to other more susceptible species. mals. The disease apparently originated in Bluetongue affects agriculture Vector life cycle southern Africa, where many serotypes in several ways. Infected animals often The primary transmitting agent of have been isolated and identified in wild feed poorly because of ulcers in the mouth bluetongue virus in the United States is and domestic ruminants. Bluetongue was and lameness due to edema, inflamma- Culicoides variipennis, a blood-sucking first diagnosed in the United States in the tion of the hoof wall, and muscle damage. gnat about 2.5 mm (0.1 inch) long. A few late 1940s and was present in California Abortion and congenitally deformed workers feel that C. variipennis consists by 1952. Twenty-four serotypes are recog- calves and lambs also occur, and infected of multiple subspecies or perhaps two nized worldwide, of which five are known sheep often succumb to secondary pneu- species. Since behavioral and morphologi- to exist in the United States and four are monia. Additionally, there are interna- cal characteristics vary considerably in California (types 10, 11, 13, and 17). tional trade restrictions on animals and with habitat and temperature, most work- Statewide serological surveys in 1978- semen from bluetongue-endemic areas to ers currently consider C. variipennis to be 80 by B.I. Osburn, J.L. Stott, and cowork- countries free of the disease. a single species.

CALIFORNIA AGRICULTURE, MARCH-APRIL 1986 23 The basic biology is similar regardless of geographic region or habitat. Eggs are laid at dusk or at night just above the wa- terline, primarily on shallow, silty mud banks at the edges of ponded or slowly moving water, particularly when it is pol- luted with manure. Eggs hatch in about three days, and the four larval stages de- velop in the surface mud at the pond edge, presumably feeding on bacteria, algae, and organic detritus. Larval development Wild ruminants time varies with temperature and per- haps larval dietary factors, but takes two shT t 1. to four weeks during warm weather. Pu- + Culicoides pation takes place above the waterline, Culicoides and adults emerge about three days later. After a delay of one to two days, fe- males are ready to seek a blood meal (needed for egg development), often from the most abundant mammals in the area. Cattle, sheep, rabbits, and even pigs have been reported as hosts. Humans are sel- dom attacked, though this trait apparent- ly varies in different gnat populations. After a blood meal, egg development re- quires about three days. Fig. 1. Transmission cycle of bluetonguevirus. Biting gnats (Culicoides) take blood meal Gnat distribution from virus-infectedanimal, and virus replicates in the ’s body. The virus can be intro- duced into a susceptible when the gnat refeeds 10 to 14 days later. Venereal and From 1978 to 1980, larval and adult transplacentaltransmission are minor routes, best known in cattle, but transplacental trans- gnat sampling surveys were done in 10 mission also can occur in sheep. counties, from Butte and Mendocino in the north to Imperial in the south, to de- termine the distribution of C. variipennis in California and begin to characterize larval development sites. The gnat was widely distributed and is probably present essentially throughout the state, except at high altitudes or in areas without water sources. Some larvae occurred along natural waterways, but most larval sites were man-made. Urban/industrial sources, such as oxidation ponds, supported light to moderate densities. Dense populations (more than 100 larvae per 25 cc of mud) generally were found in agricultural areas. Of these, dairy wastewater lagoons were prime sources; 55 percent of 113 dairy lagoons were positive for this spe- cies. In southern California, as many as 7,600 larvae have been recovered from only 30 cc (1 ounce) of mud in these habi- tats. Some large dairy lagoons produce literally millions of gnats per week during late summer and fall emergence periods. Studies on biology and dispersal Adult C. variipennis are most active at dusk, with a smaller peak of activity at Culicoides variipennis (adult, above, and dawn. We have observed that winds de- pupa, left) is widely distributed, especially crease flight activity, although some in southern areas of the state. It often oc- flight may persist close to the ground curs in sites such as dairy lagoons, where even during breezy periods. During cool dense populations expose animals to high weather, flight may begin well before biting intensity. sunset. Activity at night also is common, especially during moonlit periods, pro- vided temperatures are above 50°F. We usually collect adults with small suction

24 CALIFORNIA AGRICULTURE, MARCH-APRIL 1986 traps baited with carbon dioxide, which The basis of susceptibility is still poorly below the waterline. The eggs and early particularly attracts host-seeking fe- understood, but it appears to be influ- larval stages of these gnats are extremely males. Males often form mating swarms enced by both genetic and environmental small (less than 1 mm), but late fourth- 1 to 2 meters above the ground near ob- factors. stage larvae are 8 to 9 mm in length. Our jects that contrast with the background in This species is a good colonizer of new experiments also have shown that larvae color or height. developmental habitats. We have found strongly avoid deeply shaded areas, pre- We have shown that adult males and early larval instars within a week of the ferring shallow mud exposed to the sun. females often feed on sugar sources, such flooding of a new dairy lagoon. In Califor- This behavior is not related to tempera- as flower nectar and plant sap. This be- nia, gnats have been recaptured up to 2 ture or time of day as much as to light, havior probably contributes substantially miles from their emergence site. Younger and may be related to larval feeding to survival and dispersal capabilities of females show a greater tendency to dis- habits. the gnats in nature. In southern Califor- perse; dispersal to traps baited with car- nia, UC research has shown that the gnats bon dioxide generally is upwind from the Implications for control are active to some extent year-round, al- developmental sites. Control of these disease vectors re- though numbers are very small in late We sample immature C. variipennis by quires a thorough knowledge of their life winter and early spring (February to removing portions of the mud and rearing cycle and ecology and their relationship April). The presence of blood-feeding and the larvae, sieving them, or extracting to disease transmission. California popu- reproducing adult gnats in the winter them by salt flotation. Larval populations lations of C. variipennis are widespread raises the possiblity of the insect serving peak in the fall and can average over 500 and, particularly in southern areas, have as a reservoir of bluetongue, but this has larvae per 30 cc of mud in southern Cali- several characteristics that encourage not been proved. In more northerly re- fornia dairy lagoons (fig 2.) Densities of- virus transmission. First, the populations gions of the state, gnat activity ceases in ten are much lower during the winter, are dense, exposing animals to high biting late fall, and the Culicoides overwinter in averaging less than 10 larvae per 30 cc. intensities. Second, the gnats are, in gen- mud in the late larval stages, emerging as Fluctuations in larval numbers and eral, very susceptible to bluetongue virus adults the following spring (April to May). age structure can be extremely valuable replication. Third, survival of adult fe- We have collected females that have in determining when the successive gen- males appears to be more than sufficient completed at least five egg batches (at erations emerge. In southern California, to allow transmission, particularly in least five blood meals) in southern Cali- the generation interval appears to be light of the generally high biting intensi- fornia. The ability of females to survive close to seven weeks during cooler ties and susceptibility. and complete several ovarian cycles is a months, but shortens to 25 to 35 days dur- While much remains to be learned critical component of bluetongue trans- ing the hot summer months. Some overlap about the basic biology, we now have mission, since they must live at least 10 to occurs in these generations, but it is sig- enough information to examine the poten- 14 days after feeding on a viremic host for nificant that they remain fairly distinct, tial of specific vector control strategies. the virus to replicate in the insect and be even late in the season. Since the generations are distinct and are transmitted to another ruminant. Many Our studies have shown that eggs and to some extent predictable, efforts can be California populations of C. variipennis most of the first two larval stages occur directed against certain life stages that are susceptible to virus replication, al- at or above the waterline, while the larger may be more susceptible. The very early though resistant populations are known. third and fourth larval stages usually are stages, for example, because they are above the waterline and are so small, Culicoides variipennis density might be susceptible to scheduled water 3rd & 4th larval stages level fluctuations, insecticide applica- tions, or both. Our observations suggest that deeper, steep-sided ponds are not particularly suitable habitats. Likewise, it appears that ponded water sources with either no manure or a great deal of ma- nure are poor producers of the gnats. These relationships are yet to be quanti- fied. F A J A 0 D F A J Sources such as dairy lagoons are un- stable, and it is difficult to define the ef- fects that management practices can be Generations expected to have on their gnat popula- 100 4th-stage larvae tions. Extrapolating these to predict their effect on virus transmission is still more complex, and so we are not yet able to recommend vector control strategies. We are now conducting studies in experimen- tal dairy lagoons, which we hope will lead 20 to the reduction of bluetongue disease in California livestock. F A J A 0 D F A J

1983 Months 1984 Bradley A. Mullens is Assistant Professor, Depart- ment of Entomology, University of California,River- side; Edmond C. Loomis is Parasitologist, Veterinary Fig. 2. Highest Culicoides variipennis larval densities in southern California dairy lagoon oc- Medicine Extension, University of California, Davis; and John R. Anderson is Professor, Department of cur in the fall (L3 and L4 are the last two larval stages). Peaks in generations (lower graph) Entomology and Parasitology, University of Califor- correspond roughly to adult gnat emergence. nia. Berkeley.

CALIFORNIA AGRICULTURE, MARCH-APRIL 1986 25