Chemical ecology of Equid-Tsetse interactions for improved control of African Trypanosomosis

Abstract

Tsetse flies (Diptera: Glossinidae) are vectors of the trypanosome parasites causing African trypanosomosis which hinders sustainable agriculture and livestock production, affects human health, and negatively impacts the economy of most African countries. Available vector control strategies including sequential aerosol techniques, use of stationary attractive devices and live baits, and sterile insect techniques have limitations and are mostly used in tandem. Sense of smell largely dictates tsetse flies’ ability to discriminate among preferred hosts such as buffalo and cattle, and non-preferred ones including waterbuck and zebra, and can be exploited for innovative vector control strategies. Previous studies identified a four-component repellent blend, waterbuck repellent compounds (WRC), comprising geranyl acetone, guaiacol, pentanoic acid and δ-octalactone, from waterbuck, a non-preferred host. Among the equids, zebra is less preferred by tsetse flies for blood feeding compared to horse and donkey. However, the chemical basis for this feeding preference has not been elucidated, thus the focus of this study. Chapter one is a general introduction of the study. Chapter two investigated the semiochemical basis of the avoidance of zebras by tsetse flies. Crude skin odours of zebra were evaluated for repellency on savannah tsetse flies Glossina pallidipes in the field. Odour extracts were subjected to chemical analyses (gas chromatography-mass spectrometry, GC/MS and GC-electroantennographic detection, GC/EAD) to identify physiologically-active compounds. Identified compounds were screened for repellency in field-based behavioural assays. It was established that zebra skin volatiles contribute to the avoidance behaviour of the savannah tsetse fly, G. pallidipes. Tsetse flies consistently detected and responded to three ketones (6-methyl-5-hepten-2-one, acetophenone, geranyl acetone) and four aldehydes (heptanal, octanal, nonanal, decanal) from zebra skin odours. Additionally, a synthetic blend of the three ketones (blend K) repelled G. pallidipes in a similar way as the known tsetse repellent blend, WRC. In chapter three, the three repellent compounds identified from zebra skin in chapter two were evaluated for repellency on the riverine tsetse fly G. fuscipes fuscipes, whose chemical ecology has mostly been understudied but are key vectors of trypanosomes causing HAT. The three-component blend (blend K) significantly reduced field trap catches of G. f. fuscipes, similar to WRC. Geranyl acetone, a component of both WRC and blend K, exhibited comparable repellency to the blends (WRC and blend K). Chapter four presents a comparative analysis of GC/MS skin volatile profiles of zebra and two other equids (donkey and horse). Results show skin odours of the three equids contain the seven EAD-active compounds earlier identified in Chapter two. Moreover, there were quantitative variations of these compounds among the equids, with generally higher concentrations in zebra odours in relation to donkey and horse. Taken together, the study established the allomonal effect of zebra skin on both savannah and riverine tsetse flies and revealed the semiochemical basis for the differential attraction of tsetse flies to the equids examined. The three-component repellent blend identified in zebra skin odour has potential for integration into the management toolkit for savannah and riverine species of tsetse flies and African trypanosomosis.