Effect of constant temperatures on Culicoides sonorensis midge physiology and vesicular stomatitis virus infection

Authors: ROZO-LOPEZ, PAULA - Kansas State University; PARK, YOONSEONG - Kansas State University; Drolet, Barbara

Submitted to: Insects
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/7/2022
Publication Date: 4/9/2022
Citation: Rozo-Lopez, P., Park, Y., Drolet, B.S. 2022. Effect of constant temperatures on Culicoides sonorensis midge physiology and vesicular stomatitis virus infection. Insects. 13(4):372-386. https://doi.org/10.3390/insects13040372.
DOI: https://doi.org/10.3390/insects13040372

Interpretive Summary: Culicoides biting midges are nuisance pests of livestock and transmit vesicular stomatitis virus (VSV) which affects horses, cattle and swine. Female midges ingest viruses while feeding on the blood they need for laying eggs. After ingesting VSV-infected blood, the environmental temperature of the midge's resting location mediates the rates at which blood is digested, eggs are laid, and virus particles are replicated inside the midge. VSV transmission will occur if the timing of virus amplification aligns with the next feeding-egg laying cycle. We evaluated the impact of environmental temperature on midge physiology (lifespan and reproduction), thermal resting behavior, and vector competence for VSV (infection and dissemination). Our results indicate that after ingesting a blood meal, most midges prefer to rest in areas that fall within their preferred physiological range regardless of the environmental temperatures at which they were being maintained. These preferred temperatures maximize their survival, number of egg-laying cycles, and the likelihood of VSV transmission. Our environmental temperature approach shows that in the Culicoides-VSV system, the preferred resting temperature selected by blood-fed midges is beneficial for both the insect and virus transmission.

Technical Abstract: Culicoides midges play an important role in vesicular stomatitis virus (VSV) transmission to U.S. livestock. After VSV-blood feeding, blood digestion followed by oviposition occurs while ingested virus particles replicate and disseminate for potential transmission during subsequent blood-feeding events. Changes to environmental temperature may alter the feeding-oviposition-refeeding cycles, midge survival, VSV infection and vector competence. However, the heterothermic midge may respond rapidly to environmental changes by adjusting their thermal behavior to resting in areas closer to their physiological range. Here we investigated the effects of four constant environmental temperatures (20, 25, 30, and 35 °C) on C. sonorensis survival, oviposition, and VSV infection, as well as resting thermal preferences after blood-feeding. We found that most midges preferred to rest in areas at 25-30 °C. These two constant temperatures (25 and 30 °C) allowed an intermediate fitness performance, with a 66% survival probability by day 10 and oviposition cycles occurring every 2-3 days. Additionally, VSV infection rates and virus titers in bodies and heads were higher than in midges held at 20 °C and 30 °C. Our results provide insights into the temperature implications on VSV-Culicoides interactions and confirm that the range of temperature preferred by the midges can be beneficial for the vector and the arbovirus.