Desiccation Tolerance in the Eggs of the Primary North American Bluetongue Virus Vector, <I>Culicoides sonorensis</I> (Diptera: Ceratopogonidae), and Implications for Vector Persistence

Abstract

Culicoides sonorensis Wirth and Jones transmits bluetongue virus and develops in a variety of polluted mud habitats. Egg desiccation tolerance was tested by obtaining eggs of known age, drying them, and placing them back on wet substrate. Eggs 4-10 h old failed to hatch after 12 h of drying at 75% relative humidity (RH). Older eggs (28-34 h) survived severe desiccation and >50% water weight loss. They regained their water within ≈2 h of rehydration. Relative to control eggs, average egg hatch was reduced by 36% after 12 h of drying, 79% after 24 h, 91% after 36 h, and 97% after 48 h. Some embryos (1%) survived and hatched after 60 h of drying and water losses of nearly 60%. Eggs in specific 25-40 h age categories did not differ in hatch after a 12-h desiccation stress; critical embryo age to survive drying is between 10 and 24 h. Humidity gradients relieved desiccation stress, and eggs appeared to regain water from saturated RH conditions. Individual, gravid C. sonorensis oviposited in 1-liter containers with an artificial mud bank. If they laid eggs, 73% deposited them singly in lines ranging up to 5-6 cm in length (meanderers), while 27% laid eggs in clumps (dumpers). Eggs were positioned an average of 45 ± 12 mm back from waterline. Younger eggs, if laid in early evening, may not experience severe desiccation. Embryo recovery from such severe desiccation could be adaptive in ephemeral habitats where the species may have evolved.

Ecological Dynamics Impacting Bluetongue Virus Transmission in North America

“…In temperate enzootic zones, like Colorado, freezing winter temperatures preclude adult activity, and it is thought that in these areas, C. sonorensis populations persist as overwintering larvae (81). However, laboratory experiments have shown that eggs are the most cold-tolerant life stage (96), and are also highly desiccation tolerant (97), suggesting that they may be the true overwintering stage. Although eggs may be how the vector persists, they are unlikely to be how the virus persists.…”

Culicoides-borne Orbivirus epidemiology in a changing climate

“…Laboratory studies have also demonstrated that AHSV can replicate and persist in C. sonorensis (Boorman et al 1975, Wellby et al 1996), of particular concern as AHSV has not yet been documented in the United States. The ability of C. sonorensis to withstand temperatures of –20°C and significant desiccation in the egg stage may indicate resilience to changing climatic conditions in the future (McDermott and Mullens 2014, McDermott et al 2016). C. insignis is a competent BTV vector present in subtropical and tropical zones of the far southeastern United States, Central America, and South America north of Argentina (Borkent and Grogan 2009).…”

Deeper knowledge of shallow waters: reviewing the invertebrate fauna of southern African temporary wetlands

“…There are no African examples. Larvae of Culicoides sonorensis Wirth & Jones, 1957 from the Sonoran Desert in North America, for instance, are able to survive drying, but only for a day or two (McDermott & Mullens, 2014). Pools lasting several days often contain larvae of the ceratopogonid Dasyhelea thompsoni de Meillon, 1936 that burrow into mud at the bottom of the pond when water evaporates (McLachlan & Cantrell, 1980).…”