The Culicoides biting midge, a tiny fly in the order Diptera, transmits several important animal viruses. One of the most significant is the bluetongue virus, which causes bluetongue disease in cattle, sheep, deer and other ruminants. A new study gets closer to answering how biting midges such as Culicoides sonorensis (shown here) maintain transmission of bluetongue virus to cattle in temperate regions year after year, even though individual midges are unlikely to survive entire winters. (Photo by Xinmi Zhang, Ph.D.)

By Xinmi Zhang, Ph.D., and Alec Gerry, Ph.D.

Alec Gerry, Ph.D.

Xinmi Zhang, Ph.D.

The Culicoides biting midge, a tiny fly in the order Diptera, transmits several important animal viruses. One of the most significant is the bluetongue virus (BTV), which causes bluetongue disease in cattle, sheep, deer and other ruminants. When a new serotype or strain of BTV is introduced to a region with susceptible animals, it can lead to severe clinical symptoms and even death in some animal species.

In southern California, BTV is endemic on dairy farms, where cattle typically exhibit subclinical symptoms. The predominant biting midge species responsible for BTV transmission in this region (and much of the western United States) is Culicoides sonorensis.

BTV transmission in California is highly seasonal, with the virus commonly detected in cattle and field-collected midges during summer and fall each year but then essentially undetected during the colder winter and early spring months. This BTV transmission pattern is typical in many temperate regions of the world. The period during which BTV is not detected is referred to as the interseasonal or overwintering period. An unanswered question is how, or even whether, BTV persists during this overwintering period in California (and other similar temperate regions) so that transmission is again initiated following the overwintering period. In a study published in April in the Journal of Medical Entomology, we offer new some new evidence that points to an ongoing, though difficult-to-detect, virus transmission cycle involving active adult biting midges and hosts.

Background

In a 1971 paper on this subject, Errol Nevill, Ph.D., in South Africa presented five hypotheses for overwintering of BTV in warmer temperate regions where seasonal BTV transmission occurs consistently each year:

1. BTV might be transmitted from female midges to their offspring (vertical transmission) with immature midges surviving the overwintering period in immature habitat;
2. BTV might persist in cattle or other reservoir animals throughout the winter;
3. adult midges infected with BTV might survive the winter and initiate transmission of BTV again as the weather becomes warmer;
4. a low (undetectable) transmission might be maintained between adult biting midges and their animal hosts;
5. BTV might be reintroduced to the region every year from distant locations.

Studies with C. sonorensis in California have previously shown BTV is not vertically transmitted from female midges to their offspring, and the most abundant animal hosts (cattle) harbor infectious virus for less than 60 days. Thus, with hypotheses 1 and 2 ruled out, it appears that some activity of adult biting midges must be responsible for overwintering of the virus.

The Culicoides biting midge, a tiny fly in the order Diptera, transmits several important animal viruses. One of the most significant is the bluetongue virus, which causes bluetongue disease in cattle, sheep, deer and other ruminants. A new study gets closer to answering how biting midges such as Culicoides sonorensis (shown here) maintain transmission of bluetongue virus to cattle in temperate regions year after year, even though individual midges are unlikely to survive entire winters. (Photo by Xinmi Zhang, Ph.D.)

The Culicoides biting midge, a tiny fly in the order Diptera, transmits several important animal viruses. One of the most significant is the bluetongue virus, which causes bluetongue disease in cattle, sheep, deer and other ruminants. A new study gets closer to answering how biting midges such as Culicoides sonorensis (shown here next to a U.S. dime) maintain transmission of bluetongue virus to cattle in temperate regions year after year, even though individual midges are unlikely to survive entire winters. (Photo by Xinmi Zhang, Ph.D.)

Host-seeking biting midges have been collected during the winter months in California in small numbers, with BTV detected in midges typically starting in May. One study in northern California reported a very small number of host-seeking, BTV-infected parous midges (i.e., female midges that have laid at least one batch of eggs) captured in February and suggested that BTV may overwinter in long-lived infected adult midges. While these studies captured only a small number of host-seeking midges, field collections were not scheduled on dates when activity might be most likely to occur during winter.

In South Africa, Nevill had reported that biting midge host-seeking activity during winter months was greater on warmer days. Since previous studies in California did not focus on these warmest winter days, we wondered if host-seeking activity by midges here might largely occur on the warmest days in winter.

A New Investigation

To address this question, we conducted extensive collections of host-seeking Culicoides midges during winter (November to April) over a period of three years in the Chino dairy region of southern California. On the warmest day during each trapping week, we set up carbon dioxide traps throughout the dairy region to capture host-seeking midges active on that date. For a visual demonstration of our trapping process, see the video below, originally featured at the annual Insect Fair organized by the University of California, Riverside, Entomology Department.

In a new study seeking to answer how Culicoides biting maintain transmission of bluetongue virus to cattle in temperate regions year after year, researchers conducted extensive collections of host-seeking midges during winter (November to April) over a period of three years in the Chino dairy region of southern California. On the warmest day during each trapping week, carbon dioxide traps such as the one shown here were set up throughout the dairy region to capture host-seeking midges active on that date. (Photo by Xinmi Zhang, Ph.D.)

In contrast to previous studies in California, our study demonstrated that host-seeking activity of C. sonorensis biting midges was continuous throughout winter in southern California (at least on warmer dates during winter). Studies in northern California showed midges active during winter were more often older parous midges, suggesting that an increased proportion of host-seeking midges were long-lived adults. However, our study showed that both young and old midges were actively host-seeking throughout winter, indicating continuous emergence of new adult midges from immature development sites.

In addition, adult midges were estimated to survive no more than 30 days, suggesting even long-lived adults would not survive the entire length of the overwintering period (hypothesis 3, above). These results suggest that overwintering of BTV, at least in southern California, is more likely due to continuous BTV transmission than to survival of infected adult midges through the winter season.

Despite the continuous collection of adult midges throughout winter in our study, BTV was only detected in captured adult midges during fall (November and December) in each of the three study years. We suggest that BTV transmission occurs during winter in California, but at a very low level—in line with Nevill’s hypothesis 4, listed above. This hypothesis is also supported by the lifespan of adult midges during winter, estimated in our study to be less than 30 days, significantly shorter than the duration of the overwintering period, making it unlikely that an individual infected midge might survive from fall through spring to initiate a new cycle of BTV transmission.

Our study provides increased support that overwintering of BTV in warmer temperate regions such as southern California occurs through a continuous and ongoing virus transmission cycle involving active adult biting midges and susceptible hosts. Increasing trapping efforts during winter might facilitate BTV detection in hosts and vectors during this period, providing additional support for this hypothesis.

Xinmi Zhang, Ph.D., is a former graduate student in the Department of Entomology at the University of California, Riverside, and currently a postdoctoral research fellow at the W.M. Keck Science Department at Claremont McKenna, Pitzer, and Scripps Colleges. Email: xzhan218@ucr.edu. Alec Gerry, Ph.D., is a professor of entomology and extension specialist at the University of California, Riverside. Email: alecg@ucr.edu.