The effects of loose, firm, fine, and coarse substrates on the movement of the red flour beetle

Abstract

Movement plays a crucial role in animal behavior. However, despite the prevalence of uneven terrains in nature, many movement studies are conducted in arenas with smooth substrates. This discrepancy raises questions about the ecological validity of such experiments. To address this gap, we investigated the effect of rough substrates on movement properties using the red flour beetle (Tribolium castaneum) as a model organism. Our findings revealed significant variations in movement behavior between rough and smooth substrates. Notably, beetles traveled longer distances on smooth surfaces compared to sandpaper and loose sand. Moreover, variations in step size were influenced by substrate treatment, with the highest values observed on sand and sandpaper treatments. The proportion of time spent standing still also showed sensitivity to substrate conditions. The interaction between substrate properties and beetle sex further influenced several movement properties. Even the spatial configuration of rough and smooth areas in the arena had an impact on beetle movement, with areas along the arena perimeter exhibiting a stronger effect. These results highlight the impact of uneven terrain on beetle movement, underscoring the importance of considering environmental conditions when designing experimental setups. Here, this refers to the substrate on which animals move, but it may refer to other conditions, such as the test arena size and shape, temperature, humidity, and illumination. Failure to account for these background environmental conditions may result in inadvertently examining the interaction of the tested animals with these conditions, rather than focusing on the effect of the treatments applied in the experiment.

Keywords

movement ecology / obstacles / pest ecology / sand / thigmotaxis / wall-following behavior

References

[1] Abràmoff, M.D. Magalhães, P.J. and Ram, S.J. (2004) Image processing with ImageJ. Biophotonics International, 11, 36-42.

[2] Anukiruthika, T. Jian, F. and Jayas, D.S. (2021) Movement and behavioral response of stored product insects under stored grain environments—a review. Journal of Stored Products Research, 90, 101752.

[3] Arnold, P.A. Cassey, P. and White, C.R. (2016) Maturity matters for movement and metabolic rate: trait dynamics across the early adult life of red flour beetles. Animal Behaviour, 111, 181-188.

[4] Arnold, P.A. Cassey, P. and White, C.R. (2023) Morphological shifts in response to spatial sorting of dispersal behaviour in red flour beetles across multiple generations. Journal of Zoology, 320, 131-142.

[5] Arnold, P.A. Rafter, M.A. Malekpour, R. Cassey, P. Walter, G.H. and White, C.R. (2017) Investigating movement in the laboratory: dispersal apparatus designs and the red flour beetle, Tribolium castaneum. Entomologia Experimentalis et Applicata, 163, 93-100.

[6] Arthur, F.H. Hale, B.A. Starkus, L.A. Gerken, A.R. Campbell, J.F. and McKay, T. (2019) Development of Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae) on rice milling components and by-products: Effects of diet and temperature. Journal of Stored Products Research, 80, 85-92.

[7] Bergmann, P.J. Pettinelli, K.J. Crockett, M.E. and Schaper, E.G. (2017) It's just sand between the toes: how particle size and shape variation affect running performance and kinematics in a generalist lizard. Journal of Experimental Biology, 220, 3706-3716.

[8] Cain, M.L. (1987) Prey capture behavior and diel movement of Brachynemurus (Neuroptera: Myrmeleontidae) antlion larvae in south central Florida. Florida Entomologist, 70, 397-400.

[9] Campbell, J.F. and Hagstrum, D.W. (2002) Patch exploitation by Tribolium castaneum: Movement patterns, distribution, and oviposition. Journal of Stored Products Research, 38, 55-68.

[10] Campbell, J.F. Athanassiou, C.G. Hagstrum, D.W. and Zhu, K.Y. (2022) Tribolium castaneum: a model insect for fundamental and applied research. Annual Review of Entomology, 67, 347-365.

[11] Carvell, G.E. and Simons, D.J. (1990) Biometric analyses of vibrissal tactile discrimination in the rat. Journal of Neuroscience, 10, 2638-2648.

[12] Cho, S.K. Cha, B.J. Bae, B.S. and Park, S.W. (2014) A laboratory study of the correlation between texture and the speed of locomotion by the sea urchin Hemicentrotus pulcherrimus. Marine and Freshwater Behaviour and Physiology, 47, 329-334.

[13] Clifton, G.T. Holway, D. and Gravish, N. (2020) Uneven substrates constrain walking speed in ants through modulation of stride frequency more than stride length. Royal Society Open Science, 7, 192068.

[14] Clifton, G. Stark, A.Y. Li, C. and Gravish, N. (2023) The bumpy road ahead: the role of substrate roughness on animal walking and a proposed comparative metric. Journal of Experimental Biology, 226, jeb245261.

[15] Collinge, S.K. and Palmer, T.M. (2002) The influences of patch shape and boundary contrast on insect response to fragmentation in California grasslands. Landscape Ecology, 17, 647-656.

[16] Conceição, P.M.D. Faroni, L.R. Sousa, A.H. Pimentel, M.A. and Freitas, R.S. (2012) Diatomaceous earth effects on weevils with different susceptibility standard to phosphine. Revista Brasileira de Engenharia Agrícola e Ambiental, 16, 309-313.

[17] Dürr, V. and Krause, A.F. (2022) Tactile sensing in insects. In Encyclopedia of Computational Neuroscience (eds. D. Jaeger & R. Jung), pp. 3389-3393. New York, NY, Springer.

[18] England, S.J. and Robert, D. (2022) The ecology of electricity and electroreception. Biological Reviews, 97, 383-413.

[19] Fabres, A. de Campos Macedo da Silva, J. Fernandes, K.V. Xavier-Filho, J. Rezende, G.L. and Oliveira, A.E.A. (2014) Comparative performance of the red flour beetle Tribolium castaneum (Coleoptera: Tenebrionidae) on different plant diets. Journal of Pest Science, 87, 495-506.

[20] Fedina, T.Y. and Lewis, S.M. (2007) Female mate choice across mating stages and between sequential mates in flour beetles. Journal of Evolutionary Biology, 20, 2138-2143.

[21] Fewell, J.H. (1988) Energetic and time costs of foraging in harvester ants, Pogonomyrmex occidentalis. Behavioral Ecology and Sociobiology, 22, 401-408.

[22] Fišer, Ž. Prevorčnik, S. Lozej, N. and Trontelj, P. (2019) No need to hide in caves: shelter-seeking behavior of surface and cave ecomorphs of Asellus aquaticus (Isopoda: Crustacea). Zoology, 134, 58-65.

[23] Gerken, A.R. and Campbell, J.F. (2020) Oviposition and development of Tribolium castaneum Herbst (Coleoptera: Tenebrionidae) on different types of flour. Agronomy, 10, 1593.

[24] Goossens, S. Wybouw, N. Van Leeuwen, T. and Bonte, D. (2020) The physiology of movement. Movement Ecology, 8, 5.

[25] Gotelli, N.J. and Ellison, A.M. (2013) A Primer of Ecological Statistics (2nd edition). Sinauer Associates Inc., Sunderland, MA, USA.

[26] Hagstrum, D.W. Flinn, P.W. and Gaffney, J.J. (1998) Temperature gradient on Tribolium castaneum (Coleoptera: Tenebrionidae) adult dispersal in stored wheat. Environmental Entomology, 27, 123-129.

[27] Halsey, L.G. (2016) Terrestrial movement energetics: current knowledge and its application to the optimising animal. Journal of Experimental Biology, 219, 1424-1431.

[28] Hansson, L.A. and Åkesson, S. (2014) Animal Movement Across Scales. Oxford University Press, Oxford, UK.

[29] Hartmann, M.J. (2009) Active touch, exploratory movements, and sensory prediction. Integrative and Comparative Biology, 49, 681-690.

[30] Iwatsuki, K. Hirano, T. Kawase, M. Chiba, H. Michibayashi, N. Yamada, C. et al. (1996) Thigmotaxis in Paramecium caudatum is induced by hydrophobic or polyaniline-coated glass surface to which liver cells from rat adhere with forming multicellular spheroids. European Journal of Protistology, 32, 58-61.

[31] Katz, N. and Scharf, I. (2018) Habitat geometry and limited perceptual range affect habitat choice of a trap-building predator. Behavioral Ecology, 29, 958-964.

[32] Kent, J.A. Sommerfeld, J.H. Mukherjee, M. Takahashi, K.Z. and Stergiou, N. (2019) Locomotor patterns change over time during walking on an uneven surface. Journal of Experimental Biology, 222, jeb202093.

[33] Kim, R.C. Le, D. Ma, K. Heath-Heckman, E.A. Whitehorn, N. Kristan, W.B. et al. (2019) Behavioral analysis of substrate texture preference in a leech, Helobdella austinensis. Journal of Comparative Physiology A, 205, 191-202.

[34] Knief, U. and Forstmeier, W. (2021) Violating the normality assumption may be the lesser of two evils. Behavior Research Methods, 53, 2576-2590.

[35] Knight, K. (2024) Dung beetles knocked off course by uneven terrain. Journal of Experimental Biology, 227, jeb247121.

[36] Laurent Salazar, M.O. Planas-Sitjà, I. Sempo, G. and Deneubourg, J.L. (2018) Individual thigmotactic preference affects the fleeing behavior of the American cockroach (Blattodea: Blattidae). Journal of Insect Science, 18, 9.

[37] Lejeune, T.M. Willems, P.A. and Heglund, N.C. (1998) Mechanics and energetics of human locomotion on sand. Journal of Experimental Biology, 201, 2071-2080.

[38] Li, C. Umbanhowar, P.B. Komsuoglu, H. Koditschek, D.E. and Goldman, D.I. (2009) Sensitive dependence of the motion of a legged robot on granular media. Proceedings of the National Academy of Sciences USA, 106, 3029-3034.

[39] Martin, O.Y. Michalczyk, Ł. Millard, A.L. Emerson, B.C. and Gage, M.J. (2017) Lack of support for Rensch's rule in an intraspecific test using red flour beetle (Tribolium castaneum) populations. Insect Science, 24, 133-140.

[40] Matsumura, K. and Miyatake, T. (2015) Differences in attack avoidance and mating success between strains artificially selected for dispersal distance in Tribolium castaneum. PLoS ONE, 10, e0127042.

[41] Matsumura, K. and Miyatake, T. (2018) Costs of walking: differences in egg size and starvation resistance of females between strains of the red flour beetle (Tribolium castaneum) artificially selected for walking ability. Journal of Evolutionary Biology, 31, 1632-1637.

[42] Mazouchova, N. Gravish, N. Savu, A. and Goldman, D.I. (2010) Utilization of granular solidification during terrestrial locomotion of hatchling sea turtles. Biology Letters, 6, 398-401.

[43] McDonald, R.W. and Cassady St Clair, C. (2004) The effects of artificial and natural barriers on the movement of small mammals in Banff National Park, Canada. Oikos, 105, 397-407.

[44] McIntyre, N.E. and Wiens, J.A. (1999) How does habitat patch size affect animal movement? An experiment with darkling beetles. Ecology, 80, 2261-2270.

[45] O'Connor, S.M. Xu, H.Z. and Kuo, A.D. (2012) Energetic cost of walking with increased step variability. Gait and Posture, 36, 102-107.

[46] Okada, J. and Toh, Y. (2000) The role of antennal hair plates in object-guided tactile orientation of the cockroach (Periplaneta americana). Journal of Comparative Physiology A, 186, 849-857.

[47] Parlin, A.F. Kendzel, M.J. Taylor, O.R. Culley, T.M. Matter, S.F. and Guerra, P.A. (2023) The cost of movement: assessing energy expenditure in a long-distant ectothermic migrant under climate change. Journal of Experimental Biology, 226, jeb245296.

[48] Patullo, B.W. and Macmillan, D.L. (2006) Corners and bubble wrap: the structure and texture of surfaces influence crayfish exploratory behaviour. Journal of Experimental Biology, 209, 567-575.

[49] Pembury Smith, M.Q.R. and Ruxton, G.D. (2021) How fast is a snail's pace? The influences of size and substrate on gastropod speed of locomotion. Journal of Zoology, 314, 12-19.

[50] Pyke, G. (1983) Animal movements: an optimal foraging approach. In The Ecology of Animal Movement (eds. I.R. Swingland & P.J. Greenwood), pp. 7-31. Clarendon Press, Oxford, UK.

[51] Pyke, G. (2019) Animal movements: an optimal foraging approach. In Encyclopedia of Animal Behavior (ed. J.C. Choe), pp. 149-156. Elsevier Academic Press.

[52] Radnan, G.N. Gibb, H. and Eldridge, D.J. (2018) Soil surface complexity has a larger effect on food exploitation by ants than a change from grassland to shrubland. Ecological Entomology, 43, 379-388.

[53] Ridley, A.W. Hereward, J.P. Daglish, G.J. Raghu, S. Collins, P.J. and Walter, G.H. (2011) The spatiotemporal dynamics of Tribolium castaneum (Herbst): adult flight and gene flow. Molecular Ecology, 20, 1635-1646.

[54] Romero, S.A. Campbell, J.F. Nechols, J.R. and With, K.A. (2010) Movement behavior of red flour beetle: response to habitat cues and patch boundaries. Environmental Entomology, 39, 919-929.

[55] Scharf, I. Gilad, T. Bar-Ziv, M.A. Katz, N. Gregorian, E. Pruitt, J.N. et al. (2018) The contribution of shelter from rain to the success of pit-building predators in urban habitats. Animal Behaviour, 142, 139-145.

[56] Scharf, I. Hanna, K. and Gottlieb, D. (2024a) Experimental arena settings might lead to misinterpretation of movement properties. Insect Science, 31, 271-284.

[57] Scharf, I. Radai, A. Goldshtein, D. and Hanna, K. (2024b) Flour beetles prefer corners over walls and are slowed down with increasing habitat complexity. Royal Society Open Science, 11, 231667.

[58] Schmitz, B. (1992) Directionality of antennal sweeps elicited by water jet stimulation of the tailfan in the crayfish Procambarus clarkii. Journal of Comparative Physiology A, 171, 617-627.

[59] Schütz, C. and Dürr, V. (2011) Active tactile exploration for adaptive locomotion in the stick insect. Philosophical Transactions of the Royal Society B, 366, 2996-3005.

[60] Semeao, A.A. Campbell, J.F. Whitworth, R.J. and Sloderbeck, P.E. (2013) Movement of Tribolium castaneum within a flour mill. Journal of Stored Products Research, 54, 17-22.

[61] Shepard, E.L. Wilson, R.P. Rees, W.G. Grundy, E. Lambertucci, S.A. and Vosper, S.B. (2013) Energy landscapes shape animal movement ecology. American Naturalist, 182, 298-312.

[62] Simon, P. Dupuis, R. and Costentin, J. (1994) Thigmotaxis as an index of anxiety in mice. Influence of dopaminergic transmissions. Behavioural Brain Research, 61, 59-64.

[63] Soibam, B. Mann, M. Liu, L. Tran, J. Lobaina, M. Kang, Y.Y. et al. (2012) Open-field arena boundary is a primary object of exploration for Drosophila. Brain and Behavior, 2, 97-108.

[64] Sponberg, S. and Full, R.J. (2008) Neuromechanical response of musculo-skeletal structures in cockroaches during rapid running on rough terrain. Journal of Experimental Biology, 211, 433-446.

[65] Staudacher, E.M. Gebhardt, M. and Dürr, V. (2005) Antennal movements and mechanoreception: neurobiology of active tactile sensors. Advances in Insect Physiology, 32, 49-205.

[66] Torres-Contreras, H. and Vásquez, R.A. (2007) Spatial heterogeneity and nestmate encounters affect locomotion and foraging success in the ant Dorymyrmex goetschi. Ethology, 113, 76-86.

[67] Violle, N. Balandras, F. Le Roux, Y. Desor, D. and Schroeder, H. (2009) Variations in illumination, closed wall transparency and/or extramaze space influence both baseline anxiety and response to diazepam in the rat elevated plus-maze. Behavioural Brain Research, 203, 35-42.

[68] Voloshina, A.S. and Ferris, D.P. (2015) Biomechanics and energetics of running on uneven terrain. Journal of Experimental Biology, 218, 711-719.

[69] Voloshina, A.S. Kuo, A.D. Daley, M.A. and Ferris, D.P. (2013) Biomechanics and energetics of walking on uneven terrain. Journal of Experimental Biology, 216, 3963-3970.

[70] Wang, L. Johannesson, C.M. and Zhou, Q. (2015) Effect of surface roughness on attachment ability of locust Locusta migratoria manilensis. Wear, 332, 694-701.

[71] Wexler, Y. Subach, A. Pruitt, J.N. and Scharf, I. (2016) Behavioral repeatability of flour beetles before and after metamorphosis and throughout aging. Behavioral Ecology and Sociobiology, 70, 745-753.

[72] Wexler, Y. Wertheimer, K.O. Subach, A. Pruitt, J.N. and Scharf, I. (2017) Mating alters the link between movement activity and pattern in the red flour beetle. Physiological Entomology, 42, 299-306.

[73] Yoder, J.M. Marschall, E.A. and Swanson, D.A. (2004) The cost of dispersal: predation as a function of movement and site familiarity in ruffed grouse. Behavioral Ecology, 15, 469-476.

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