The Role of Cattle Urine as a Host-Habitat Cue and Nutrient Resource for Malaria Mosquitoes

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Addis Ababa University


Behavioural and physiological resistance of Anopheles mosquitoes to long lasting insecticide treated nets (LLINs) and indoor residual spraying (IRS) is an emerging challenge for the malaria vector control and elimination programmes. This necessitates the development of new tools, deriving, at least in part, from a more in-depth understanding of the behavioural ecology of these disease vectors. Olfaction is at the centre of the interaction between the mosquito and host, an interaction that is essential to the fitness of the insects. As such, the olfactory system must be able to accurately assess these resources, by the quality and quantity of odorants emitted by the hosts in a dynamic background of habitat odours within the landscape. At the broadest scale, olfactory cues emanating from both the host and from odours deposited within the landscape by the host, indicate the recent presence of potential hosts. These host-habitat cues have gained attention recently, as they have the potential to provide novel substrates for control tool development. Mammalian urine has previously been shown to act as a host habitat cue for tsetse flies, and attract the malaria vector, Anopheles arabiensis. Research presented in this thesis, extends these findings and identifies cattle urine as a host-habitat cue and a source for nutrients. Host seeking and gravid An. arabiensis are differentially attracted to the odour of fresh and aged cattle urine. Using combined gas chromatography and electroantennographic detection as well as combined gas chromatography and mass spectrometry analyses, bioactive volatile compounds were identified in aging urine. The quality and quantity of these compounds changed with the age of the urine. In general, the number of bioactive compounds decreased with the age, whereas the total release rate of these compounds increased from 30 to 242 μg h-1. Synthetic blends of the bioactive compounds in their natural ratio generally reproduced the behavioural response of host iv seeking and gravid An. arabiensis to fresh and aging urine. The odour 24 h aged cattle urine and its synthetic blend was found to elicit a significant behavioural response in host seeking An. arabiensis, as well as in the sibling species An. coluzzii and An. quadriannulatus. To further evaluate the role of individual components within this blend, subtractive assays were conducted and showed that all compounds are required to elicit the full behavioural response in An. arabiensis. These results strongly suggests that host seeking Anopheles gambiae sensu lato use the odour fresh cattle urine as faithful indicator of the presence of potential hosts. To further evaluate the efficacy of the synthetic odour blend of 24 h aged urine, field studies were performed at a village near Meki town in Central Great Rift Valley of Ethiopia. Using indoor Centre of Disease and Control light traps, a significantly higher number of host seeking and blood fed An. arabiensis, as well as host seeking Culex spp., were collected in odour-baited traps compared to control traps. This suggests that a synthetic blend of cattle urine odour urine has the potential of attracting a wide range of physiological stages and species of mosquitoes, and thus be used as a component in integrated vector control management. Besides acting as a host habitat cue, cattle urine, and its main nitrogenous constituent, urea, provides an important nutrient resource for host seeking and gravid An. arabiensis. Feeding assays, in which gravid females fed on diluted aging cattle urine revealed that most females readily imbibed the largest meals of cattle urine, when aged less than 48 h. In addition, females imbibed urea over a large range of concentrations, excepting concentrations approximating those isotonic with mosquito haemolymph. Host seeking females, which fed on cattle urine and those fed on urea were shown to exhibit similar levels of short distance flight as those fed on sugar or water in tethered flight assays. Long distance flight, however, was curtailed in those fed on cattle urine and urea compared to sugar and water. While this did not indicate a role for cattle urine in v increasing the flight energy reserves, it suggests that imbibed urine may be acting as a signal of host presence and to remain in the local area. Feeding on urine and urea also significantly affected reproduction. The size of both eggs and larvae were enhanced following the intake of 24 h aged urine and moderate concentrations of urea. The number of eggs increased after feeding on select doses of urea. In summary, cattle urine provides malaria mosquitoes with both a host-habitat cue, which attracts host seeking mosquitoes, through which novel odour baits can be developed, and a nutritional resource that enhances flight energy and reproduction.



Malaria, Mosquito, Host-Habitat, Host Seeking, Gravid, Urine, Nutrient