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      A Colour Opponent Model That Explains Tsetse Fly Attraction to Visual Baits and Can Be Used to Investigate More Efficacious Bait Materials

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      PLoS Neglected Tropical Diseases
      Public Library of Science

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          Abstract

          Palpalis group tsetse flies are the major vectors of human African trypanosomiasis, and visually-attractive targets and traps are important tools for their control. Considerable efforts are underway to optimise these visual baits, and one factor that has been investigated is coloration. Analyses of the link between visual bait coloration and tsetse fly catches have used methods which poorly replicate sensory processing in the fly visual system, but doing so would allow the visual information driving tsetse attraction to these baits to be more fully understood, and the reflectance spectra of candidate visual baits to be more completely analysed. Following methods well established for other species, I reanalyse the numbers of tsetse flies caught at visual baits based upon the calculated photoreceptor excitations elicited by those baits. I do this for large sets of previously published data for Glossina fuscipes fuscipes (Lindh et al. (2012). PLoS Negl Trop Dis 6: e1661), G. palpalis palpalis (Green (1988). Bull Ent Res 78: 591), and G. pallidipes (Green and Flint (1986). Bull Ent Res 76: 409). Tsetse attraction to visual baits in these studies can be explained by a colour opponent mechanism to which the UV-blue photoreceptor R7y contributes positively, and both the green-yellow photoreceptor R8y, and the low-wavelength UV photoreceptor R7p, contribute negatively. A tool for calculating fly photoreceptor excitations is made available with this paper, and this will facilitate a complete and biologically authentic description of visual bait reflectance spectra that can be employed in the search for more efficacious visual baits, or the analysis of future studies of tsetse fly attraction.

          Author Summary

          Tsetse flies transmit sleeping sickness (human African trypanosomiasis), and visually attractive targets and traps are important tools for the control of the flies and prevention of disease. Previous studies have tried to determine the best colour for visual baits by relating their light reflectance properties to their attractiveness to tsetse. However, these methods represent only part of the visual information captured by the fly's eye, which is encoded by five different types of photoreceptor with varying sensitivities to different wavelengths of light. I use established methods to calculate the excitation of each fly photoreceptor type by the visual baits used to catch tsetse flies in three previous field studies. This method more completely describes the visual information captured by the fly's eye. Tsetse fly attraction can then be largely explained by a comparison of the excitations of three different photoreceptor types within the fly's nervous system. This knowledge and approach will allow for the more complete quantification of visual bait reflectance spectra, so that more efficient bait materials can be identified and employed to control tsetse flies.

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          Most cited references19

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          Human African trypanosomiasis.

          Human African trypanosomiasis (sleeping sickness) occurs in sub-Saharan Africa. It is caused by the protozoan parasite Trypanosoma brucei, transmitted by tsetse flies. Almost all cases are due to Trypanosoma brucei gambiense, which is indigenous to west and central Africa. Prevalence is strongly dependent on control measures, which are often neglected during periods of political instability, thus leading to resurgence. With fewer than 12 000 cases of this disabling and fatal disease reported per year, trypanosomiasis belongs to the most neglected tropical diseases. The clinical presentation is complex, and diagnosis and treatment difficult. The available drugs are old, complicated to administer, and can cause severe adverse reactions. New diagnostic methods and safe and effective drugs are urgently needed. Vector control, to reduce the number of flies in existing foci, needs to be organised on a pan-African basis. WHO has stated that if national control programmes, international organisations, research institutes, and philanthropic partners engage in concerted action, elimination of this disease might even be possible. Copyright 2010 Elsevier Ltd. All rights reserved.
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            Visual and olfactory responses of haematophagous Diptera to host stimuli.

            Key biotic and environmental constraints on the host-orientated behaviour of haematophagous Diptera are summarized. For each major group of biting Diptera, responses to host stimuli are reviewed, including activation and ranging behaviour, long-range and short-range olfactory responses and visual responses. Limitations to the comparison of results between groups of species, and the practical problems of experimental method and equipment are discussed.
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              The color-vision circuit in the medulla of Drosophila.

              Color vision requires comparison between photoreceptors that are sensitive to different wavelengths of light. In Drosophila, this is achieved by the inner photoreceptors (R7 and R8) that contain different rhodopsins. Two types of comparisons can occur in fly color vision: between the R7 (UV sensitive) and R8 (blue- or green sensitive) photoreceptor cells within one ommatidium (unit eye) or between different ommatidia that contain spectrally distinct inner photoreceptors. Photoreceptors project to the optic lobes: R1-R6, which are involved in motion detection, project to the lamina, whereas R7 and R8 reach deeper in the medulla. This paper analyzes the neural network underlying color vision into the medulla. We reconstruct the neural network in the medulla, focusing on neurons likely to be involved in processing color vision. We identify the full complement of neurons in the medulla, including second-order neurons that contact both R7 and R8 from a single ommatidium, or contact R7 and/or R8 from different ommatidia. We also examine third-order neurons and local neurons that likely modulate information from second-order neurons. Finally, we present highly specific tools that will allow us to functionally manipulate the network and test both activity and behavior. This precise characterization of the medulla circuitry will allow us to understand how color vision is processed in the optic lobe of Drosophila, providing a paradigm for more complex systems in vertebrates.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                December 2014
                4 December 2014
                15 December 2014
                : 8
                : 12
                : e3360
                Affiliations
                [1]Institute of Biological, Environmental, and Rural Sciences, Aberystwyth University, Aberystwyth, Ceredigion, United Kingdom
                International Centre of Insect Physiology and Ecology, Kenya
                Author notes

                The author has declared that no competing interests exist.

                Analyzed the data: RDS. Contributed reagents/materials/analysis tools: RDS. Wrote the paper: RDS.

                Article
                PNTD-D-14-01330
                10.1371/journal.pntd.0003360
                4256293
                25473844
                403f6210-acc6-4e79-baa0-3922a7d48d15
                Copyright @ 2014

                Santer. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 3 August 2014
                : 20 October 2014
                Page count
                Pages: 16
                Funding
                The author received no specific funding for this work.
                Categories
                Research Article
                Biology and Life Sciences
                Ecology
                Behavioral Ecology
                Neuroscience
                Sensory Perception
                Vision
                Color Vision
                Neuroethology
                Psychology
                Zoology
                Animal Behavior
                Entomology
                Medicine and Health Sciences
                Epidemiology
                Disease Vectors
                Arthropod Vectors
                Insect Vectors
                Vector Biology
                Infectious Diseases
                Vector-Borne Diseases
                People and Places
                Geographical Locations
                Africa
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. The complete, collated data set on which statistical analyses were conducted, and a tool with which to calculate photoreceptor excitations, are all contained within the paper and its supporting information files. Also contained within these files are the author's measurements of reflectance spectra from two of the source publications (Green, 1988 and Green & Flint, 1986), using which photoreceptor excitation calculations can be repeated and verified. The reflectance spectra with which to do this for the remaining source publication (Lindh et al. 2012) were made freely available by those authors in their online supporting information files ( http://dx.doi.org/10.1371/journal.pntd.0001665).

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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