Olfactory sampling volume for pheromone capture by wing fanning of silkworm moth: a simulation-based study.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
02 Aug 2024
02 Aug 2024
Historique:
received:
16
02
2024
accepted:
18
07
2024
medline:
3
8
2024
pubmed:
3
8
2024
entrez:
2
8
2024
Statut:
epublish
Résumé
Odours used by insects for foraging and mating are carried by the air. Insects induce airflows around them by flapping their wings, and the distribution of these airflows may strongly influence odour source localisation. The flightless silkworm moth, Bombyx mori, has been a prominent insect model for olfactory research. However, although there have been numerous studies on antenna morphology and its fluid dynamics, neurophysiology, and localisation algorithms, the airflow manipulation of the B. mori by fanning has not been thoroughly investigated. In this study, we performed computational fluid dynamics (CFD) analyses of flapping B. mori to analyse this mechanism in depth. A three-dimensional simulation using reconstructed wing kinematics was used to investigate the effects of B. mori fanning on locomotion and pheromone capture. The fanning of the B. mori was found to generate an aerodynamic force on the scale of its weight through an aerodynamic mechanism similar to that of flying insects. Our simulations further indicate that the B. mori guides particles from its anterior direction within the ~ 60° horizontally by wing fanning. Hence, if it detects pheromones during fanning, the pheromone can be concluded to originate from the direction the head is pointing. The anisotropy in the sampling volume enables the B. mori to orient to the pheromone plume direction. These results provide new insights into insect behaviour and offer design guidelines for robots for odour source localisation.
Identifiants
pubmed: 39095549
doi: 10.1038/s41598-024-67966-y
pii: 10.1038/s41598-024-67966-y
doi:
Substances chimiques
Pheromones
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
17879Subventions
Organisme : F-REI
ID : JPFR23010401
Organisme : F-REI
ID : JPFR23010401
Organisme : Japan Society for the Promotion of Science
ID : 17K17638;18H05468; 19H02060; 24K00829; 24K03014
Organisme : Japan Society for the Promotion of Science
ID : 17K17638;18H05468; 19H02060; 24K00829; 24K03014
Organisme : Japan Society for the Promotion of Science
ID : 17K17638;18H05468; 19H02060; 24K00829; 24K03014
Organisme : JKA Foundation
ID : 2024M-419
Organisme : JKA Foundation
ID : 2024M-419
Informations de copyright
© 2024. The Author(s).
Références
Weissburg, M. J. The fluid dynamical context of chemosensory behavior. Biol. Bull. 198, 188–202 (2000).
pubmed: 10786940
doi: 10.2307/1542523
Celani, A., Villermaux, E. & Vergassola, M. Odor landscapes in turbulent environments. Phys. Rev. X 4, 041015 (2014).
Vickers, N. J. Mechanisms of animal navigation in odor plumes. Biol. Bull. 198, 203–212 (2000).
pubmed: 10786941
doi: 10.2307/1542524
Cardé, R. T. & Willis, M. A. Navigational strategies used by insects to find distant, wind-borne sources of odor. J. Chem. Ecol. 34, 854–866 (2008).
pubmed: 18581182
doi: 10.1007/s10886-008-9484-5
Cardé, R. T. Navigation along windborne plumes of pheromone and resource-linked odors. Annu. Rev. Entomol. 66, 317–336 (2021).
pubmed: 32926790
doi: 10.1146/annurev-ento-011019-024932
Renou, M. & Anton, S. Insect olfactory communication in a complex and changing world. Curr Opin Insect Sci 42, 1–7 (2020).
pubmed: 32485594
doi: 10.1016/j.cois.2020.04.004
Murlis, J., Elkinton, J. S. & Cardé, R. T. Odor plumes and how insects use them. Annu. Rev. Entomol. 37, 505–532 (1992).
doi: 10.1146/annurev.en.37.010192.002445
Lu, K. et al. Flight muscle and wing mechanical properties are involved in flightlessness of the domestic silkmoth, Bombyx mori. Insects 11 (2020).
Bisch-Knaden, S., Daimon, T., Shimada, T., Hansson, B. S. & Sachse, S. Anatomical and functional analysis of domestication effects on the olfactory system of the silkmoth Bombyx mori. Proc. Biol. Sci. 281, 20132582 (2014).
pubmed: 24258720
pmcid: 3843842
Kanzaki, R., Sugi, N. & Shibuya, T. Self-generated zigzag turning of bombyx mori males during pheromone-mediated upwind walking (physology). Zoolog. Sci. 9, 515–527 (1992).
Takasaki, T., Namiki, S. & Kanzaki, R. Use of bilateral information to determine the walking direction during orientation to a pheromone source in the silkmoth Bombyx mori. J. Comp Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 198, 295–307 (2012).
pubmed: 22227850
doi: 10.1007/s00359-011-0708-8
Peters, J. M., Gravish, N. & Combes, S. A. Wings as impellers: Honey bees co-opt flight system to induce nest ventilation and disperse pheromones. J. Exp. Biol. 220, 2203–2209 (2017).
pubmed: 28404729
Peters, J. M., Peleg, O. & Mahadevan, L. Collective ventilation in honeybee nests. J. R. Soc. Interface 16, 20180561 (2019).
pubmed: 30958168
pmcid: 6364655
doi: 10.1098/rsif.2018.0561
Sane, S. P. Induced airflow in flying insects I. A theoretical model of the induced flow. J. Exp. Biol. 209, 32–42 (2006).
pubmed: 16354776
doi: 10.1242/jeb.01957
Sane, S. P. & Jacobson, N. P. Induced airflow in flying insects II. Measurement of induced flow. J. Exp. Biol. 209, 43–56 (2006).
pubmed: 16354777
doi: 10.1242/jeb.01958
Loudon, C. & Koehl, M. A. Sniffing by a silkworm moth: Wing fanning enhances air penetration through and pheromone interception by antennae. J. Exp. Biol. 203, 2977–2990 (2000).
pubmed: 10976034
doi: 10.1242/jeb.203.19.2977
Lei, M. & Li, C. Wings and whiffs: Understanding the role of aerodynamics in odor-guided flapping flight. Phys. Fluids 35 (2023).
Li, C., Dong, H. & Zhao, K. A balance between aerodynamic and olfactory performance during flight in Drosophila. Nat. Commun. 9, 1–8 (2018).
Bau, J., Justus, K. A., Loudon, C. & Cardé, R. T. Electroantennographic resolution of pulsed pheromone plumes in two species of moths with bipectinate antennae. Chem. Senses 30, 771–780 (2005).
pubmed: 16267163
doi: 10.1093/chemse/bji069
Yamada, M., Ohashi, H., Hosoda, K., Kurabayashi, D. & Shigaki, S. Multisensory-motor integration in olfactory navigation of silkmoth, Bombyx mori, using virtual reality system. Elife 10 (2021).
Namiki, S. & Kanzaki, R. The neurobiological basis of orientation in insects: Insights from the silkmoth mating dance. Curr. Opin. Insect Sci. 15, 16–26 (2016).
pubmed: 27436728
doi: 10.1016/j.cois.2016.02.009
Hernandez-Reyes, C. A. et al. Identification of exploration and exploitation balance in the silkmoth olfactory search behavior by information-theoretic modeling. Front. Comput. Neurosci. 15 (2021).
Grosse-Wilde, E., Svatos, A. & Krieger, J. A pheromone-binding protein mediates the bombykol-induced activation of a pheromone receptor in vitro. Chem. Senses 31, 547–555 (2006).
pubmed: 16679489
doi: 10.1093/chemse/bjj059
Gräter, F., Xu, W., Leal, W. & Grubmüller, H. Pheromone discrimination by the pheromone-binding protein of Bombyx mori. Structure 14, 1577–1586 (2006).
pubmed: 17027506
doi: 10.1016/j.str.2006.08.013
Adam, G. & Delbrück, M. Reduction of dimensionality in biological diffusion processes. Structural chemistry and molecular biology (1968).
Walker, S. M., Thomas, A. L. R. & Taylor, G. K. Photogrammetric reconstruction of high-resolution surface topographies and deformable wing kinematics of tethered locusts and free-flying hoverflies. J. R. Soc. Interface 6, 351–366 (2009).
pubmed: 18682361
doi: 10.1098/rsif.2008.0245
Fontaine, E. I., Zabala, F., Dickinson, M. H. & Burdick, J. W. Wing and body motion during flight initiation in Drosophila revealed by automated visual tracking. J. Exp. Biol. 212, 1307–1323 (2009).
pubmed: 19376952
doi: 10.1242/jeb.025379
Ben-Dov, O. & Beatus, T. Model-based tracking of fruit flies in free flight. Insects 13, (2022).
Liu, H. Integrated modeling of insect flight: From morphology, kinematics to aerodynamics. J. Comput. Phys. 228, 439–459 (2009).
doi: 10.1016/j.jcp.2008.09.020
Nakata, T. & Liu, H. A fluid–structure interaction model of insect flight with flexible wings. J. Comput. Phys. 231, 1822–1847 (2012).
doi: 10.1016/j.jcp.2011.11.005
Bomphrey, R. J., Nakata, T., Phillips, N. & Walker, S. M. Smart wing rotation and trailing-edge vortices enable high frequency mosquito flight. Nature 544, 92–95 (2017).
pubmed: 28355184
pmcid: 5412966
doi: 10.1038/nature21727
Weis-Fogh, T. Quick estimates of flight fitness in hovering animals, including novel mechanisms for lift production. J. Exp. Biol. 59, 169–230 (1973).
doi: 10.1242/jeb.59.1.169
Willmott, A. P. & Ellington, C. P. The mechanics of flight in the hawkmoth manduca sexta I. Kinematics of hovering and forward flight. J. Exp. Biol. 200, 2705–2722 (1997).
pubmed: 9418029
doi: 10.1242/jeb.200.21.2705
Zheng, L., Hedrick, T. L. & Mittal, R. Time-varying wing-twist improves aerodynamic efficiency of forward flight in butterflies. PLoS One 8, e53060 (2013).
pubmed: 23341923
pmcid: 3547021
doi: 10.1371/journal.pone.0053060
Aiello, B. R. et al. The evolution of two distinct strategies of moth flight. J. R. Soc. Interface 18, 20210632 (2021).
pubmed: 34847789
pmcid: 8647679
doi: 10.1098/rsif.2021.0632
Bode-Oke, A. T., Zeyghami, S. & Dong, H. Flying in reverse: Kinematics and aerodynamics of a dragonfly in backward free flight. J. R. Soc. Interface 15 (2018).
Chin, D. D. & Lentink, D. Flapping wing aerodynamics: From insects to vertebrates. J. Exp. Biol. 219, 920–932 (2016).
pubmed: 27030773
doi: 10.1242/jeb.042317
Combes, S. A. & Daniel, T. L. Flexural stiffness in insect wings II. Spatial distribution and dynamic wing bending. J. Exp. Biol. 206, 2989–2997 (2003).
pubmed: 12878667
doi: 10.1242/jeb.00524
Steppan, S. J. Flexural stiffness patterns of butterfly wings (Papilionoidea). J. Res. Lepidoptera 35, 61–77 (1996).
doi: 10.5962/p.266572
Ellington, C. P., van den Berg, C., Willmott, A. P. & Thomas, A. L. R. Leading-edge vortices in insect flight. Nature 384, 626–630 (1996).
doi: 10.1038/384626a0
Kanzaki, R. Coordination of wing motion and walking suggests common control of zigzag motor program in a male silkworm moth. J. Comp. Physiol. A 182, 267–276 (1998).
doi: 10.1007/s003590050177
Vogel, S. How much air passes through a silkmoth’s antenna?. J. Insect Physiol. 29, 597–602 (1983).
doi: 10.1016/0022-1910(83)90027-6
Jaffar-Bandjee, M., Steinmann, T., Krijnen, G. & Casas, J. Insect pectinate antennae maximize odor capture efficiency at intermediate flight speeds. Proc. Natl. Acad. Sci. USA 117, 28126–28133 (2020).
pubmed: 33122443
pmcid: 7668092
doi: 10.1073/pnas.2007871117
Jaffar-Bandjee, M., Steinmann, T., Krijnen, G. & Casas, J. Leakiness and flow capture ratio of insect pectinate antennae. J. R. Soc. Interface 17, 20190779 (2020).
pubmed: 32486954
pmcid: 7328394
doi: 10.1098/rsif.2019.0779
Terutsuki, D. et al. Real-time odor concentration and direction recognition for efficient odor source localization using a small bio-hybrid drone. Sens. Actuators B Chem. https://doi.org/10.1016/j.snb.2021.129770 (2021).
doi: 10.1016/j.snb.2021.129770
Sakuma, M. Virtual reality experiments on a digital servosphere: Guiding male silkworm moths to a virtual odour source. Comput. Electron. Agric. 35, 243–254 (2002).
doi: 10.1016/S0168-1699(02)00021-2
Lei, M., Willis, M. A., Schmidt, B. E. & Li, C. Numerical investigation of odor-guided navigation in flying insects: Impact of turbulence, wingbeat-induced flow, and schmidt number on odor plume structures. Biomimetics 8, 593 (2023).
pubmed: 38132532
pmcid: 10741642
doi: 10.3390/biomimetics8080593
Terutsuki, D. et al. Electroantennography-based bio-hybrid odor-detecting drone using silkmoth antennae for odor source localization. J. Vis. Exp. https://doi.org/10.3791/62895 (2021).
doi: 10.3791/62895
pubmed: 34515671
Lochmatter, T., Raemy, X., Matthey, L., Indra, S. & Martinoli, A. A comparison of casting and spiraling algorithms for odor source localization in laminar flow. In 2008 IEEE International Conference on Robotics and Automation (IEEE, 2008). https://doi.org/10.1109/robot.2008.4543357 .
Shigaki, S. et al. Animal-in-the-loop system with multimodal virtual reality to elicit natural olfactory localization behavior. Sens. Mater. 33, 4211–4228 (2021).
Ma, K. Y., Chirarattananon, P., Fuller, S. B. & Wood, R. J. Controlled flight of a biologically inspired, insect-scale robot. Science 340, 603–607 (2013).
pubmed: 23641114
doi: 10.1126/science.1231806
Baker, K. L. et al. Algorithms for olfactory search across species. J. Neurosci. 38, 9383–9389 (2018).
pubmed: 30381430
pmcid: 6209839
doi: 10.1523/JNEUROSCI.1668-18.2018
Shigaki, S. et al. Analysis of the role of wind information for efficient chemical plume tracing based on optogenetic silkworm moth behavior. Bioinspir. Biomim. 14, 046006 (2019).
pubmed: 31026859
doi: 10.1088/1748-3190/ab1d34