Zebra skin odor repels the savannah tsetse fly, Glossina pallidipes (Diptera: Glossinidae)

Abstract

Background African trypanosomosis, primarily transmitted by tsetse flies, remains a serious public health and economic challenge in sub-Saharan Africa. Interventions employing natural repellents from non-preferred hosts of tsetse flies represent a promising management approach. Although zebras have been identified as non-preferred hosts of tsetse flies, the basis for this repellency is poorly understood. We hypothesized that zebra skin odors contribute to their avoidance by tsetse flies. Methodology/Principal findings We evaluated the effect of crude zebra skin odors on catches of wild savannah tsetse flies ( Glossina pallidipes Austen, 1903) using unbaited Ngu traps compared to the traps baited with two known tsetse fly management chemicals; a repellent blend derived from waterbuck odor, WRC (comprising geranylacetone, guaiacol, pentanoic acid and δ-octalactone), and an attractant comprising cow urine and acetone, in a series of Latin square-designed experiments. Coupled gas chromatography-electroantennographic detection (GC/EAD) and GC-mass spectrometry (GC/MS) analyses of zebra skin odors identified seven electrophysiologically-active components; 6-methyl-5-hepten-2-one, acetophenone, geranylacetone, heptanal, octanal, nonanal and decanal, which were tested in blends and singly for repellency to tsetse flies when combined with Ngu traps baited with cow urine and acetone in field trials. The crude zebra skin odors and a seven-component blend of the EAD-active components, formulated in their natural ratio of occurrence in zebra skin odor, significantly reduced catches of G . pallidipes by 66.7% and 48.9% respectively, and compared favorably with the repellency of WRC (58.1%– 59.2%). Repellency of the seven-component blend was attributed to the presence of the three ketones 6-methyl-5-hepten-2-one, acetophenone and geranylacetone, which when in a blend caused a 62.7% reduction in trap catch of G . pallidipes . Conclusions/Significance Our findings reveal fundamental insights into tsetse fly ecology and the allomonal effect of zebra skin odor, and potential integration of the three-component ketone blend into the management toolkit for tsetse and African trypanosomosis control.

Tsetse blood-meal sources, endosymbionts, and trypanosome infections provide insight into African trypanosomiasis transmission in the Maasai Mara National Reserve, a wildlife-human-livestock interface

“…Despite the abundance of wildebeest, zebra, and other antelopes when the study was conducted during the Great Migration season, no blood-meals from these hosts were detected in the tsetse flies. These findings are congruent with previous reports that G. pallidipes and G. swynnertoni exhibit significant specificity in host selection whereby wildebeest are not preferred blood-meal sources [57,58], and that zebra skin odors are repellant to G. pallidipes [59]. The influx of people in the MMNR due to high tourism activities in the Great Migration season, may partially explain why humans were frequent blood-meal sources.…”

“…Better understanding of the molecular mechanisms of tsetse fly olfaction associated with host selection can help to evaluate candidate host semiochemicals as potential attractants or repellants [67–69]. Knowledge of emergent repellant odors (such as those described from zebra and waterbuck) [59,60], coupled with new host attractants, present unique opportunities to further improve tsetse bait technology using “Push-Pull” and/or “Attract-and-Kill” approaches.…”

Zebra stripes, tabanid biting flies and the aperture effect

“…Before concluding, we want to emphasize that stripes are only one way by which zebras reduce successful probing for blood by biting flies. Others include behavioural means including frequent swishing of tails and running away from tabanid annoyance [ 13 ] and zebra skin odour deterring tsetse flies from landing [ 32 ], suggesting that there are severe selection pressures for African Equidae to avoid biting fly attack [ 25 ].…”

Sustainable Elimination (Zero Cases) of Sleeping Sickness: How Far Are We from Achieving This Goal?

“…The repellent mix called waterbuck repellent compounds (WRC) and 4-methylguaiacol which were known Mortisan group tsetse fly repellents were tested for their effects on the Palpalis group and found to effectively repel Glossina fuscipes fuscipes [98]. Similarly, unrefined zebra skin odour, as well as a chemical mix with identical odor, was found to significantly repel Glossina pallidipes [99].…”