Jewel beetles pose significant threats to forestry, and effective traps are needed to monitor and manage them. Green traps often catch more beetles, but purple traps catch a greater proportion of females. Understanding the function and mechanism of this behavior can provide a rationale for trap optimization. Jewel beetles possess UV-, blue-, green-, and red-sensitive photoreceptors, and perceive color differently from humans. Jewel beetle photoreceptor signals were calculated for tree leaf and tree bark stimuli, representing feeding and oviposition sites of adult jewel beetles respectively. Artificial neural networks (ANNs) were trained to discriminate those stimuli using beetle photoreceptor signals, providing in silico models of the neural processing that might have evolved to drive behavior. ANNs using blue-, green-, and red-sensitive photoreceptor inputs could classify these stimuli with very high accuracy (>99%). ANNs processed photoreceptor signals in an opponent fashion: increasing green-sensitive photoreceptor signals promoted leaf classifications, while increasing blue- and red-sensitive photoreceptor signals promoted bark classifications. Trained ANNs were fed photoreceptor signals calculated for traps, wherein they always classified green traps as leaves, but often classified purple traps as bark, indicating that these traps share salient features with different classes of tree stimuli from a beetle's eye view. A metric representing the photoreceptor opponent mechanism implicated by ANNs then explained catches of emerald ash borer, Agrilus planipennis, at differently colored traps from a previous field study. This analysis provides a hypothesized behavioral mechanism that can now guide the rational selection and improvement of jewel beetle traps.
| [1] |
Briscoe, A.D. and Chittka, L. (2001) The evolution of color vision in insects. Annual Review of Entomology, 46, 471–510.
|
| [2] |
Brooks, M.E., Kristensen, K., van Benthem, K.J., Magnusson, A., Berg, C.W., Nielsen, A. et al. (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R Journal, 9, 378–400.
|
| [3] |
Campbell, S.A. and Borden, J.H. (2005) Bark reflectance spectra of conifers and angiosperms: implications for host discrimination by coniferophagous bark and timber beetles. Canadian Entomologist, 137, 719–722.
|
| [4] |
Caves, E.M., Nowicki, S. and Johnsen, S. (2019) Von Uexküll revisited: addressing human biases in the study of animal perception. Integrative and Comparative Biology, 59, 1451–1462.
|
| [5] |
Crook, D.J., Francese, J.A., Zylstra, K.E., Fraser, I., Sawyer, A.J., Bartels, D.W. et al. (2009) Laboratory and field response of the emerald ash borer (Coleoptera: Buprestidae), to selected regions of the electromagnetic spectrum. Journal of Economic Entomology, 102, 2160–2169.
|
| [6] |
Dearden, A.E., Wood, M.J., Frend, H.O., Butt, T.M. and Allen, W.L. (2023) Visual modelling can optimise the appearance and capture efficiency of sticky traps used to manage insect pests. Journal of Pest Science, 97, 469–479.
|
| [7] |
Dodds, K.J., Sweeney, J., Francese, J.A., Besana, L. and Rassati, D. (2024) Factors affecting catches of bark beetles and woodboring beetles in traps. Journal of Pest Science, 97, 1767–1793.
|
| [8] |
Endler, J.A. (1990) On the measurement and classification of colour in studies of animal colour patterns. Biological Journal of the Linnean Society, 41, 315–352.
|
| [9] |
Endler, J.A. (1993) The color of light in forests and its implications. Ecological Monographs, 63, 1–27.
|
| [10] |
Francese, J.A., Crook, D.J., Fraser, I., Lance, D.R., Sawyer, A.J. and Mastro, V.C. (2010) Optimization of trap color for emerald ash borer (Coleoptera: Buprestidae). Journal of Economic Entomology, 103, 1235–1241.
|
| [11] |
Francese, J.A., Oliver, J.B., Fraser, I., Lance, D.R., Youssef, N., Sawyer, A.J. et al. (2008) Influence of trap placement and design on capture of the emerald ash borer (Coleoptera: Buprestidae). Journal of Economic Entomology, 101, 1831–1837.
|
| [12] |
Gokan, N. and Meyer-Rochow, B. (1984) Fine-structure of the compound eye of the buprestid beetle Curis caloptera (Coleoptera, Buprestidae). Zeitschrift für mikroskopisch-anatomische Forschung, Leipzig, 98, 17–35.
|
| [13] |
Goverdovskii, V.I., Fyhrquist, N., Reuter, T., Kuzmin, D.G. and Donner, K. (2000) In search of the visual pigment template. Visual Neuroscience, 17, 509–528.
|
| [14] |
Gurney, K. (2007) Neural networks for perceptual processing: from simulation tools to theories. Philosophical Transactions of the Royal Society B, 362, 339–353.
|
| [15] |
Hartig, F. (2022) DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.4.6. http://florianhartig.github.io/DHARMa/.
|
| [16] |
Imrei, Z., Lohonyai, Z., Csóka, G., Muskovits, J., Szanyi, S., Vétek, G. et al. (2020) Improving trapping methods for buprestid beetles to enhance monitoring of native and invasive species. Forestry, 93, 254–264.
|
| [17] |
Kelber, A. (1999) Ovipositing butterflies use a red receptor to see green. Journal of Experimental Biology, 202, 2619–2630.
|
| [18] |
Kelber, A. (2001) Receptor based models for spontaneous colour choices in flies and butterflies. Entomologia Experimentalis et Applicata, 99, 231–244.
|
| [19] |
Kelber, A., Vorobyev, M. and Osorio, D. (2003) Animal colour vision—behavioural tests and physiological concepts. Biological Reviews, 78, 81–118.
|
| [20] |
Meglič, A., Ilić, M., Quero, C., Arikawa, K. and Belušič, G. (2020) Two chiral types of randomly rotated ommatidia are distributed across the retina of the flathead oak borer Coraebus undatus (Coleoptera: Buprestidae). Journal of Experimental Biology, 223, jeb225920.
|
| [21] |
Oliver, J.B., Youssef, N., Fare, D., Halcomb, M., Scholl, S. Klingeman, W. et al. (2002) Monitoring buprestid borers in production nursery areas. In Proceedings of the 29th Annual Meeting of the Tennessee Entomological Society (ed. G. Haun), pp. 17–23. Nashville, TN.
|
| [22] |
Osorio, D. and Bossomaier, T.R.J. (1992) Human cone-pigment spectral sensitivities and the reflectances of natural surfaces. Biological Cybernetics, 67, 217–222.
|
| [23] |
Perkovich, C.L., Addesso, K.M., Basham, J.P., Fare, D.C., Youssef, N.N. and Oliver, J.B. (2022) Effects of color attributes on trap capture rates of Chrysobothris femorata (Coleoptera: Buprestidae) and related species. Environmental Entomology, 51, 737–746.
|
| [24] |
Perkovich, C.L., Oliver, J.B., Addesso, K.M., Basham, J.P. and Youssef, N.N. (2023) Effects of trap shape, size, and color variations on capture rates of Chrysobothris (Coleoptera: Buprestidae) and related buprestids. Florida Entomologist, 106, 63–66.
|
| [25] |
Santer, R.D. (2014) A colour opponent model that explains tsetse fly attraction to visual baits and can be used to investigate more efficacious bait materials. PLoS Neglected Tropical Diseases, 8, e3360.
|
| [26] |
Santer, R.D. (2017) Developing photoreceptor-based models of visual attraction in riverine tsetse, for use in the engineering of more-attractive polyester fabrics for control devices. PLoS Neglected Tropical Diseases, 11, e0005448.
|
| [27] |
Santer, R.D., Akanyeti, O., Endler, J.A., Galván, I. and Okal, M.N. (2023) Why are biting flies attracted to blue objects? Proceedings of the Royal Society B, 290, 20230463.
|
| [28] |
Santer, R.D. and Allen, W.L. (2024) Optimising the colour of traps requires an insect's eye view. Pest Management Science, 80, 931–934.
|
| [29] |
Santer, R.D., Okal, M.N., Esterhuizen, J. and Torr, S.J. (2021) Evaluation of improved coloured targets to control riverine tsetse in East Africa: a Bayesian approach. PLoS Neglected Tropical Diseases, 15, e0009463.
|
| [30] |
Santer, R.D., Vale, G.A., Tsikire, D. and Torr, S.J. (2019) Optimising targets for tsetse control: taking a fly's-eye-view to improve the colour of synthetic fabrics. PLoS Neglected Tropical Diseases, 13, e0007905.
|
| [31] |
Sharkey, C.R., Blanco, J., Lord, N.P. and Wardill, T.J. (2023) Jewel beetle opsin duplication and divergence is the mechanism for diverse spectral sensitivities. Molecular Biology and Evolution, 40, msad023.
|
| [32] |
Sharkey, C.R., Fujimoto, M.S., Lord, N.P., Shin, S., McKenna, D.D., Suvorov, A. et al. (2017) Overcoming the loss of blue sensitivity through opsin duplication in the largest animal group, beetles. Scientific Reports, 7, 8.
|
| [33] |
Stavenga, D.G., Oberwinkler, J. and Postma, M. (2000) Modeling primary visual processes in insect photoreceptors. In Handbook of Biological Physics, Volume 3. Molecular Mechanisms in Visual Transduction (eds. D.G. Stavenga, W.J. DeGrip & E.N. Pugh), pp. 527–574. Elsevier, Amsterdam.
|
| [34] |
Timms, L.L., Smith, S.M. and De Groot, P. (2006) Patterns in the within-tree distribution of the emerald ash borer Agrilus planipennis (Fairmaire) in young, green-ash plantations of south-western Ontario, Canada. Agricultural and Forest Entomology, 8, 313–321.
|
| [35] |
Tummers, B. (2006) Data Thief III. https://datathief.org/.
|
| [36] |
van der Kooi, C.J., Stavenga, D.G., Arikawa, K., Belušič, G. and Kelber, A. (2021) Evolution of insect color vision: From spectral sensitivity to visual ecology. Annual Review of Entomology, 66, 435–461.
|
| [37] |
Venables, W.N. and Ripley, B.D. (2002) Modern Applied Statistics with S, Fourth edition, Springer, New York.
|
| [38] |
von Uexküll, J. (2010) A Foray into the Worlds of Animals and Humans with a Theory of Meaning (J.D. O'Neil, Trans.). University of Minnesota Press, Minneapolis & London (original work published 1934 and 1940).
|
| [39] |
Wang, L.Y., Stuart-Fox, D., Walker, G., Roberts, N.W. and Franklin, A.M. (2022) Insect visual sensitivity to long wavelengths enhances colour contrast of insects against vegetation. Scientific Reports, 12, 982.
|
| [40] |
Wang, W., Jones, P. and Partridge, D. (2000) Assessing the impact of input features in a feedforward neural network. Neural Computing and Applications, 9, 101–112.
|
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2025 The Author(s). Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.