Identification of Cattle-Derived Volatiles that Modulate the Behavioral Response of the Biting Midge Culicoides nubeculosus

Abstract

Identification of host-derived volatiles is an important step towards the development of novel surveillance and control tools for Culicoides biting midges. In this study, we identified compounds from headspace collections of cattle hair and urine that modulate the behavioral response of Culicoides nubeculosus, a research model species with a similar hostrange as the vectors of Bluetongue disease and Schmallenberg disease in Europe. Combined gas chromatography and electroantennographic detection (GC-EAD) analysis revealed 23 bioactive compounds, of which 17, together with octanal, were evaluated in a two-choice behavioral assay in the presence of CO2. Decanal, 2-phenylethanal, 1-octen-3-ol, 2-ethylhexanol, 3-methylindole, phenol, and 3-ethylphenol elicited attraction of host seeking C. nubeculosus, whereas heptanal, octanal, nonanal, 3-propylphenol, and 4-action to CO2, when compared to CO2 alone. 6-Methyl-5-hepten-2-one, 3-methylphenol, 4-methylphenol, and 4-ethylphenol elicited both attraction and inhibition. The behavioral responses were dependent on the concentration tested. Our results show that cattle-derived odors have the potential to be used for the manipulation of the behavior of Culicoides biting midges.

Evaluation of Host-Derived Volatiles for Trapping Culicoides Biting Midges (Diptera: Ceratopogonidae)

“…1-Octen-3-ol is a well-characterized mammalian kairomone (Pickett et al 2010 ), which is known to attract various hematophagous insects, including tsetse flies (Torr 1990 ; Vale and Hall 1985 ) and mosquitoes (Kline et al 1994 ; Takken and Kline 1989 ). As was observed for decanal, C. impunctatus were more attracted to traps with a low release rate of racemic 1-octen-3-ol, as previously shown in both laboratory and field studies (Bhasin et al 2000 ; Blackwell et al 1996 ; Isberg et al 2016 ) of C. impunctatus and C. nubeculosus . While this study analyzed the effect of racemic 1-octen-3-ol on attraction of C. impunctatus , other studies on both biting midges and mosquitoes imply that it is the ( R ) - enantiomer that is important for attraction (Harrup et al 2012 ) and for some species even repellence (Pingxi et al 2015 ).…”

“…Addition of phenol, 4-methylphenol, 3-propylphenol and 2-ethylhexanol, identified in air entrainments of cattle urine (Isberg et al 2016 ), to traps baited with CO 2 increased trap captures of C. impunctatus . The results obtained for phenol, as well as 4-methylphenol, agree with those observed for C. nubeculosus in the laboratory (Isberg et al 2016 ).…”

“…The compounds tested in this study have previously been identified in aerations of cattle hair and urine, and shown to elicit electrophysiological and behavioral responses in C. nubeculosus in the laboratory (Isberg et al 2016 ). Chemicals used were sourced from Sigma-Aldrich Chemie GmbH, Steinheim, Germany, except for 3-propylphenol which was obtained from Alfa Aesar GmbH Karlsruhe, Germany (Table 1 ).…”

“…The addition of cow urine and hexane extracts of hair samples from large animals have also been shown to increase the attraction of C. impunctatus to traps baited with CO 2 alone, and CO 2 and 1-octen-3-ol, respectively (Bhasin et al 2001 ; Mands et al 2004 ). While the chemical components responsible for this increase in attraction of C. impunctatus to animal odor have not been elucidated fully, in analyses by coupled gas chromatography and electroantennographic detection (GC-EAD) in our laboratory volatile components have been identified from cow urine and hair that elicit antennal responses in a related species, C. nubeculosus (Isberg et al 2016 ). In a laboratory behavioral assay, 1-octen-3-ol, decanal, 2-ethylhexanol, phenol and 4-methylphenol elicited attraction of C. nubeculosus when combined with CO 2 , whereas octanal, nonanal, ( E )-2-nonenal and 3-propylphenol acted as behavioral inhibitors.…”

Influence of light and kairomone baiting systems on trap collections of biting midges in southern Sweden

“…Carbon dioxide (CO 2 ), a general behavioral activator and attractant for many blood‐feeding insects, has been utilized for biting midge surveillance in the US (Smith and Mullens 2003). Addition of the kairomone 1‐octen3‐ol, expired from the breath of ruminants (Hall et al 1984), to CO 2 , has been found to improve numbers of biting midges caught in the UK, mainland Europe, the US, and Australia (Takken and Kline 1989, Kline et al 1994, Ritchie et al 1994, Bhasin et al 2001, Harrup et al 2012, Isberg et al 2016). UV light traps are widely used for capturing Culicoides and have been suggested as the gold standard for biting midge surveillance even though they may not accurately reflect biting rates on host animals (Carpenter et al 2008, Gerry et al 2009, Viennet et al 2011).…”