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

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

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

A Receptor-Based Explanation for Tsetse Fly Catch Distribution between Coloured Cloth Panels and Flanking Nets

Tsetse flies transmit trypanosomes that cause nagana in cattle, and sleeping sickness in humans. Therefore, optimising visual baits to control tsetse is an important priority. Tsetse are intercepted at visual baits due to their initial attraction to the bait, and their subsequent contact with it due to landing or accidental collision. Attraction is proposed to be driven in part by a chromatic mechanism to which a UV-blue photoreceptor contributes positively, and a UV and a green photoreceptor contribute negatively. Landing responses are elicited by stimuli with low luminance, but many studies also find apparently strong landing responses when stimuli have high UV reflectivity, which would imply that UV wavelengths contribute negatively to attraction at a distance, but positively to landing responses at close range. The strength of landing responses is often judged using the number of tsetse sampled at a cloth panel expressed as a proportion of the combined catch of the cloth panel and a flanking net that samples circling flies. I modelled these data from two previously published field studies, using calculated fly photoreceptor excitations as predictors. I found that the proportion of tsetse caught on the cloth panel increased with an index representing the chromatic mechanism driving attraction, as would be expected if the same mechanism underlay both long- and close-range attraction. However, the proportion of tsetse caught on the cloth panel also increased with excitation of the UV-sensitive R7p photoreceptor, in an apparently separate but interacting behavioural mechanism. This R7p-driven effect resembles the fly open-space response which is believed to underlie their dispersal towards areas of open sky. As such, the proportion of tsetse that contact a cloth panel likely reflects a combination of deliberate landings by potentially host-seeking tsetse, and accidental collisions by those seeking to disperse, with a separate visual mechanism underlying each behaviour

Motion dazzle:A locust's eye view

Motion dazzle describes high-contrast patterns (e.g. zigzags on snakes and dazzle paint on World War I ships) that do not conceal an object, but inhibit an observer's perception of its motion. However, there is limited evidence for this phenomenon. Locusts have a pair of descending contralateral movement detector (DCMD) neurons which respond to predator-like looming objects and trigger escape responses. Within the network providing input to a DCMD, separate channels are excited when moving edges cause areas of the visual field to brighten or darken, respectively, and these stimuli interact antagonistically. When a looming square has an upper half and lower half that are both darker than background, it elicits a stronger DCMD response than the upper half does alone. However, when a looming square has a darker-than-background upper half and a brighter-than-background lower half, it elicits a weaker DCMD response than its upper half does alone. This effect allows high-contrast patterns to weaken and delay DCMD response parameters implicated in escape decisions, and is analogous to motion dazzle. However, the motion dazzle effect does not provide the best means of motion camouflage, because uniform bright squares, or low-contrast squares, elicit weaker DCMD responses than high-contrast, half dark, half bright squares

Evidence for air movement signals in the agonistic behaviour of a nocturnal arachnid (Order Amblypygi)

Many arthropods possess filiform hair sensilla (termed trichobothria in arachnids), which are extremely sensitive detectors of medium particle displacement. Electrophysiological evidence in some taxa suggests that these sensilla can detect air particle displacements resulting from intraspecific communication signals. However, it has not yet been shown for any species that the air particle displacements detected by the filiform hairs are themselves perceived as a ‘signal’ (i.e. that individuals make behavioural decisions based upon the responses of these organs to the displays of conspecifics). We investigate the agonistic behaviour of the whip spider Phrynus marginemaculatus and the role of its trichobothria in receiving agonistic signals. Whip spiders have extremely elongated ‘antenniform’ first legs, which they vibrate close to their opponents during agonistic interactions, inducing air movements that excite their opponents' trichobothria. We find that ablation of the trichobothria causes significant increases in: (I) contest duration, and (II) the probability of contest escalation past aggressive displays to physical fighting. Therefore, in the absence of air movement-sensitive sensilla, contest assessment is impaired. This suggests that whip spiders exploit true air movement signals during agonistic interactions, and that these are received by the trichobothria. Furthermore, these results indicate that, in whip spiders, such signals help mitigate the cost of agonistic interaction

Optimising targets for tsetse control:Taking a fly’s-eye-view to improve the colour of synthetic fabrics

The savannah tsetse flies, Glossina morsitans morsitans and G. pallidipes, are important vectors of Rhodesian human African trypanosomiasis and animal African trypanosomiasis in East and southern Africa. We tested in Zimbabwe whether robust, synthetic fabrics, and innovative fly’s-eye-view approaches to optimise fabric colour, can improve insecticide-treated targets employed for tsetse control. Flies were caught by electrocution at a standard target comprising a 1m x 1m black cotton cloth panel with 1m x 0.5m black polyester net panels on each side. Catches were subdivided by species and sex. Tsetse catches were unaffected by substitution of the black cotton with a blue polyester produced for riverine tsetse targets. Exchanging the net panels for phthalogen blue cotton to simulate the target routinely used in Zimbabwe significantly reduced catches of female G. m. morsitans (mean catch 0.7 times that at standard), with no effect on other tsetse catches. However, significantly greater proportions of the catch were intercepted at the central panel of the Zimbabwe (means 0.47–0.79) versus standard designs (0.11–0.29). We also engineered a new violet polyester cloth using models of tsetse attraction based upon fly photoreceptor responses. With and without odour lure, catches of females of both species at the violet target were significantly greater than those at standard (means 1.5–1.6 times those at standard), and typical blue polyester targets (means 0.9–1.3 times those at standard). Similar effects were observed for males under some combinations of species and odour treatment. The proportions of catch intercepted at the central panel of the violet target (means 0.08–0.18) were intermediate between those at standard and typical blue polyester. Further, the reflectance spectrum of violet polyester was more stable under field conditions than that of black cotton. Our results demonstrate the effectiveness of photoreceptor-based models as a novel means of improving targets to control tsetse and trypanosomiases

Predator versus Prey:Locust Looming-Detector Neuron and Behavioural Responses to Stimuli Representing Attacking Bird Predators

Many arthropods possess escape-triggering neural mechanisms that help them evade predators. These mechanisms are important neuroethological models, but they are rarely investigated using predator-like stimuli because there is often insufficient information on real predator attacks. Locusts possess uniquely identifiable visual neurons (the descending contralateral movement detectors, DCMDs) that are well-studied looming motion detectors. The DCMDs trigger ‘glides’ in flying locusts, which are hypothesised to be appropriate last-ditch responses to the looms of avian predators. To date it has not been possible to study glides in response to stimuli simulating bird attacks because such attacks have not been characterised. We analyse video of wild black kites attacking flying locusts, and estimate kite attack speeds of 10.8±1.4 m/s. We estimate that the loom of a kite’s thorax towards a locust at these speeds should be characterised by a relatively low ratio of half size to speed (l/|v|) in the range 4–17 ms. Peak DCMD spike rate and gliding response occurrence are known to increase as l/|v| decreases for simple looming shapes. Using simulated looming discs, we investigate these trends and show that both DCMD and behavioural responses are strong to stimuli with kite-like l/|v| ratios. Adding wings to looming discs to produce a more realistic stimulus shape did not disrupt the overall relationships of DCMD and gliding occurrence to stimulus l/|v|. However, adding wings to looming discs did slightly reduce high frequency DCMD spike rates in the final stages of object approach, and slightly delay glide initiation. Looming discs with or without wings triggered glides closer to the time of collision as l/|v| declined, and relatively infrequently before collision at very low l/|v|. However, the performance of this system is in line with expectations for a last-ditch escape response

Uncovering \u27Hidden\u27 Signals: Previously Presumed Visual Signals Likely Generate Air Particle Movement

Wolf spiders within the genus Schizocosa have become a model system for exploring the form and function of multimodal communication. In terms of male signaling, much past research has focused on the role and importance of dynamic and static visual and substrate-borne vibratory communication. Studies on S. retrorsa, however, have found that female-male pairs were able to successfully mate in the absence of both visual and vibratory stimuli, suggesting a reduced or non-existent role of these signaling modalities in this species. Given these prior findings, it has been suggested that S. retrorsa males may utilize an additional signaling modality during courtship-air particle movement, often referred to as near-field sound-which they likely produce with rapid leg waving and receive using thin filiform sensory hairs called trichobothria. In this study, we tested the role of air-particle movement in mating success by conducting two independent sets of mating trials with randomly paired S. retrorsa females and males in the dark and on granite (i.e., without visual or vibratory signals) in two different signaling environments-(i) without ( No Noise ) and (ii) with ( Noise ) introduced air-particle movement intended to disrupt signaling in that modality. We also ran foraging trials in No Noise/Noise environments to explore the impact of our treatments on overall behavior. Across both mating experiments, our treatments significantly impacted mating success, with more mating in the No Noise signaling environments compared to the Noise environments. The rate of leg waving-a previously assumed visual dynamic movement that has also been shown to be able to produce air particle displacement-was higher in the No Noise than Noise environments. Across both treatments, males with higher rates of leg waving had higher mating success. In contrast to mating trials results, foraging success was not influenced by Noise. Our results indicate that artificially induced air particle movement disrupts successful mating and alters male courtship signaling but does not interfere with a female\u27s ability to receive and assess the rate of male leg waving

Increased Male-Male Mounting Behaviour in Desert Locusts during Infection with an Entomopathogenic Fungus

Same-sex sexual behaviour occurs across diverse animal taxa, but adaptive explanations can be difficult to determine. Here we investigate male-male mounting (MMM) behaviour in female-deprived desert locust males infected with the entomopathogenic fungus Metarhizium acridum. Over a four-week period, infected locusts performed more MMM behaviours than healthy controls. Among infected locusts, the probability of MMM, and the duration of time spent MMM, significantly increased with the mounting locust?s proximity to death. In experimental trials, infected locusts were also significantly more likely than controls to attempt to mount healthy males. Therefore, we demonstrate that MMM is more frequent among infected than healthy male locusts, and propose that this may be explained by terminal reproductive effort and a lowered mate acceptance threshold in infected males. However, during experimental trials mounting attempts were more likely to be successful if the mounted locusts were experimentally manipulated to have a reduced capacity to escape. Thus, reduced escape capability resulting from infection may also contribute to the higher frequency of MMM among infected male locusts. Our data demonstrate that pathogen infection can affect same-sex sexual behaviour, and suggest that the impact of such behaviours on host and pathogen fitness will be a novel focus for future research.publishersversionPeer reviewe