Developing photoreceptor-based models of visual attraction in riverine tsetse, for use in the engineering of more-attractive polyester fabrics for control devices

Riverine tsetse transmit the parasites that cause the most prevalent form of human African trypanosomiasis, Gambian HAT. In response to the imperative for cheap and efficient tsetse control, insecticide-treated ‘tiny targets’ have been developed through refinement of tsetse attractants based on blue fabric panels. However, modern blue polyesters used for this purpose attract many less tsetse than traditional phthalogen blue cottons. Therefore, colour engineering polyesters for improved attractiveness has great potential for tiny target development. Because flies have markedly different photoreceptor spectral sensitivities from humans, and the responses of these photoreceptors provide the inputs to their visually guided behaviours, it is essential that polyester colour engineering be guided by fly photoreceptor-based explanations of tsetse attraction. To this end, tsetse attraction to differently coloured fabrics was recently modelled using the calculated excitations elicited in a generic set of fly photoreceptors as predictors. However, electrophysiological data from tsetse indicate the potential for modified spectral sensitivities versus the generic pattern, and processing of fly photoreceptor responses within segregated achromatic and chromatic channels has long been hypothesised. Thus, I constructed photoreceptor-based models explaining the attraction of G. f. fuscipes to differently coloured tiny targets recorded in a previously published investigation, under differing assumptions about tsetse spectral sensitivities and organisation of visual processing. Models separating photoreceptor responses into achromatic and chromatic channels explained attraction better than earlier models combining weighted photoreceptor responses in a single mechanism, regardless of the spectral sensitivities assumed. However, common principles for fabric colour engineering were evident across the complete set of models examined, and were consistent with earlier work. Tools for the calculation of fly photoreceptor excitations are available with this paper, and the ways in which these and photoreceptor-based models of attraction can provide colorimetric values for the engineering of more-attractively coloured polyester fabrics are discussed.

[1]  S. Torr,et al.  Improving the Cost-Effectiveness of Artificial Visual Baits for Controlling the Tsetse Fly Glossina fuscipes fuscipes , 2009, PLoS neglected tropical diseases.

[2]  S. Torr,et al.  Know your foe: lessons from the analysis of tsetse fly behaviour. , 2015, Trends in parasitology.

[3]  T. Pohida,et al.  Multiple Redundant Medulla Projection Neurons Mediate Color Vision in Drosophila , 2014, Journal of neurogenetics.

[4]  S. Laughlin,et al.  Photoreceptor performance and the co-ordination of achromatic and chromatic inputs in the fly visual system , 2000, Vision Research.

[5]  G. Gibson,et al.  Visual and olfactory responses of haematophagous Diptera to host stimuli , 1999, Medical and veterinary entomology.

[6]  S. Laughlin,et al.  Changes in the intensity-response function of an insect's photoreceptors due to light adaptation , 1981, Journal of comparative physiology.

[7]  Sarah E. J. Arnold,et al.  University of Huddersfield Repository Optimizing the Colour and Fabric of Targets for the Control of the Tsetse Fly 'Glossina Fuscipes Fuscipes' , 2012 .

[8]  M. Camara,et al.  Tsetse Control and the Elimination of Gambian Sleeping Sickness , 2016, PLoS neglected tropical diseases.

[9]  K. Lunau Visual ecology of flies with particular reference to colour vision and colour preferences , 2014, Journal of Comparative Physiology A.

[10]  M. Vorobyev,et al.  Photoreceptor sectral sensitivities in terrestrial animals: adaptations for luminance and colour vision , 2005, Proceedings of the Royal Society B: Biological Sciences.

[11]  R. Hardie Functional Organization of the Fly Retina , 1985 .

[12]  J. Hargrove,et al.  Explaining the Host-Finding Behavior of Blood-Sucking Insects: Computerized Simulation of the Effects of Habitat Geometry on Tsetse Fly Movement , 2014, PLoS neglected tropical diseases.

[13]  Roger C. Hardie,et al.  The photoreceptor array of the dipteran retina , 1986, Trends in Neurosciences.

[14]  S. Torr,et al.  Towards an Optimal Design of Target for Tsetse Control: Comparisons of Novel Targets for the Control of Palpalis Group Tsetse in West Africa , 2011, PLoS neglected tropical diseases.

[15]  C. Green Bait methods for tsetse fly control. , 1994, Advances in parasitology.

[16]  J. Brady,et al.  Analysis of the components of electric nets' that affect their sampling efficiency for tsetse flies (Diptera: Glossinidae) , 1994 .

[17]  R. Santer A Colour Opponent Model That Explains Tsetse Fly Attraction to Visual Baits and Can Be Used to Investigate More Efficacious Bait Materials , 2014, PLoS neglected tropical diseases.

[18]  N. Franceschini,et al.  Electrophysiological analysis of fly retina , 1979, Journal of comparative physiology.

[19]  G. Vale The trap-orientated behaviour of tsetse flies (Glossinidae) and other Diptera , 1982, Bulletin of Entomological Research.

[20]  S. Torr,et al.  Prospects for Developing Odour Baits To Control Glossina fuscipes spp., the Major Vector of Human African Trypanosomiasis , 2009, PLoS neglected tropical diseases.

[21]  F. Checchi,et al.  Prevalence and under-detection of gambiense human African trypanosomiasis during mass screening sessions in Uganda and Sudan , 2012, Parasites & Vectors.

[22]  M. Vorobyev,et al.  Animal colour vision — behavioural tests and physiological concepts , 2003, Biological reviews of the Cambridge Philosophical Society.

[23]  Roger D. Santer,et al.  A Receptor-Based Explanation for Tsetse Fly Catch Distribution between Coloured Cloth Panels and Flanking Nets , 2015, PLoS neglected tropical diseases.

[24]  N. Strausfeld,et al.  Neuronal basis for parallel visual processing in the fly , 1991, Visual Neuroscience.

[25]  T. Wachtler,et al.  Color Discrimination with Broadband Photoreceptors , 2013, Current Biology.

[26]  S. Torr,et al.  Is vector control needed to eliminate gambiense human African trypanosomiasis? , 2013, Front. Cell. Infect. Microbiol..

[27]  K. Kirschfeld,et al.  Ultraviolet sensitivity of fly photoreceptors R7 and R8: Evidence for a sensitising function , 1983, Biophysics of structure and mechanism.

[28]  Joseph Hilbe Generalized Estimating Equations, Second Edition , 2012 .

[29]  S. Mihok The development of a multipurpose trap (the Nzi) for tsetse and other biting flies , 2002, Bulletin of Entomological Research.

[30]  Sally Galbraith,et al.  A Study of Clustered Data and Approaches to Its Analysis , 2010, The Journal of Neuroscience.

[31]  C. Green,et al.  An analysis of colour effects in the performance of the F2 trap against Glossina pallidipes Austen and G. morsitans morsitans Westwood (Diptera: Glossinidae) , 1986 .

[32]  S. Torr,et al.  Vegetation and the Importance of Insecticide-Treated Target Siting for Control of Glossina fuscipes fuscipes , 2011, PLoS neglected tropical diseases.

[33]  S. Torr,et al.  Costs Of Using “Tiny Targets” to Control Glossina fuscipes fuscipes, a Vector of Gambiense Sleeping Sickness in Arua District of Uganda , 2015, PLoS neglected tropical diseases.

[34]  R. Menzel,et al.  Detection of coloured stimuli by honeybees: minimum visual angles and receptor specific contrasts , 1996, Journal of Comparative Physiology A.

[35]  D. C. Rich,et al.  Billmeyer and Saltzman's principles of color technology, 3rd edition , 2001 .

[36]  S. Welburn,et al.  Controlling sleeping sickness – a review , 2009, Parasitology.

[37]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[38]  Giuliano Cecchi,et al.  Human African trypanosomiasis , 2017, The Lancet.

[39]  Roger C. Hardie,et al.  The compound eye of the tsetse fly (Glossina morsitans morsitans and Glossina palpalis palpalis) , 1989 .

[40]  N. Troje,et al.  Spectral Categories in the Learning Behaviour of Blowflies , 1993 .

[41]  W. Pan Akaike's Information Criterion in Generalized Estimating Equations , 2001, Biometrics.

[42]  Lars Chittka,et al.  The colour hexagon: a chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency , 1992, Journal of Comparative Physiology A.

[43]  S. Torr,et al.  Improving the Cost-Effectiveness of Visual Devices for the Control of Riverine Tsetse Flies, the Major Vectors of Human African Trypanosomiasis , 2011, PLoS neglected tropical diseases.

[44]  A. Kelber Receptor based models for spontaneous colour choices in flies and butterflies , 2001 .

[45]  R. Berns Billmeyer and Saltzman's Principles of Color Technology , 2000 .

[46]  S. Torr,et al.  Tsetse Control and Gambian Sleeping Sickness; Implications for Control Strategy , 2015, PLoS neglected tropical diseases.

[47]  R. Menzel,et al.  Opponent colour coding is a universal strategy to evaluate the photoreceptor inputs in Hymenoptera , 1992, Journal of Comparative Physiology A.

[48]  J. Hanley,et al.  Statistical analysis of correlated data using generalized estimating equations: an orientation. , 2003, American journal of epidemiology.

[49]  C. Green The effect of colour on trap- and screen-orientated responses in Glossina palpalis palpalis (Robineau-Desvoidy) (Diptera: Glossinidae) , 1988 .

[50]  M. Vorobyev,et al.  Receptor noise as a determinant of colour thresholds , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.