Remote radio control of insect flight reveals why beetles lift their legs in flight while other insects tightly fold

Abstract

In the research and development of micro air vehicles, understanding and imitating the flight mechanism of insects presents a viable way of progressing forward. While research is being conducted on the flight mechanism of insects such as flies and dragonflies, research on beetles that can carry larger loads is limited. Here, we clarified the beetle midlegs' role in the attenuation and cessation of the wingbeat. We anatomically confirmed the connection between the midlegs and the elytra. We also further clarified which pair of legs are involved in the wingbeat attenuation mechanism, and lastly demonstrated free-flight control via remote leg muscle stimulation. Observation of multiple landings using a high-speed camera revealed that the wingbeat stopped immediately after their midlegs were lowered. Moreover, the action of lowering the midleg attenuated and often stopped the wingbeat. A miniature remote stimulation device (backpack) mountable on beetles was designed and utilized for the free-flight demonstration. Beetles in free flight were remotely induced into lowering (swing down) each leg pair via electrical stimulation, and they were found to lose significant altitude only when the midlegs were stimulated. Thus, the results of this study revealed that swinging down of the midlegs played a significant role in beetle wingbeat cessation. In the future, our findings on the wingbeat attenuation and cessation mechanism are expected to be helpful in designing bioinspired micro air vehicles.

Biohybrid robots: recent progress, challenges, and perspectives

“…They tested this hypothesis by manipulating the forelegs via a miniature remote stimulator mounted onto flying beetles, in which the flying beetles turned when the forelegs were swung by the stimulation of leg muscles. In a similar study, the beetles' midlegs also attenuate wing beats [156].…”

“…The locomotion of these augmented animals can then be externally controlled, spanning three modes of locomotion: walking/running, flying, and swimming. Notably, these capabilities have been demonstrated in jellyfish (figure 4(A)) [139,140], clams (figure 4(B)) [141], turtles (figure 4(C)) [142,143], and insects, including locusts (figure 4(D)) [27,144], beetles (figure 4(E)) [28,[145][146][147][148][149][150][151][152][153][154][155][156][157][158], cockroaches (figure 4(F)) [159][160][161][162][163][164][165], and moths [166][167][168][169][170].…”

A hierarchical model for external electrical control of an insect, accounting for inter-individual variation of muscle force properties

“…The Motion Hacking ( Owaki et al, 2019 ; Owaki and Dürr, 2022 ) method strives to observe the adaptation process in the insect’s own sensorymotor system as leg movements are intentionally controlled by a human operator, so as to reveal hidden mechanisms underlying natural locomotion. Thus far, research on insect cyborg control has addressed aspects of flight control ( Sato et al, 2009 ; Sato and Maharbiz, 2010 ; Sato et al, 2015 ; Kosaka et al, 2021 ; Sane et al, 2007 ; Bozkurt et al, 2009 ; Hinterwirth et al, 2012 ), gait control ( Cao et al, 2016 ; Doan et al, 2018 ; Nguyen et al, 2020 ; Ando and Kanzaki, 2017 ; Sanchez et al, 2015 ), and controlling jellyfish propulsion ( Xu and Dabiri, 2020 ; Xu et al, 2020 ). In contrast to our present study, the main objective of the mentioned studies was to convert target animals into cyborgs, with little examination of the control mechanisms and/or muscle properties involved.…”

“…With the advancement and diversity in micro-flexible and micro-printable electronics ( Rogers et al, 2010 ; Rich et al, 2021 ), micro-mechanical fabrication, and micro-actuator technologies ( Kim et al, 2020 ), such biohybrid, i.e. cyborg robots have been engineered to manipulate their gait and flight through electrical stimulation of target muscles in various insects, includings beetles ( Sato et al, 2009 ; Sato and Maharbiz, 2010 ; Sato et al, 2015 ; Cao et al, 2016 ; Doan et al, 2018 ; Nguyen et al, 2020 ; Kosaka et al, 2021 ), moths ( Sane et al, 2007 ; Bozkurt et al, 2009 ; Hinterwirth et al, 2012 ; Ando and Kanzaki, 2017 ), and cockroaches ( Sanchez et al, 2015 ). The advantage of biohybrid (cyborg) robots is that they do not require individual “design,” “fabrication,” and “assembly” processes for each component because they use the body tissues of living insects ( Cao et al, 2014 ).…”

Cyborg Insects: Bug or a Feature?

“…For instance, while several insects (such as flies and honeybees) rely on vision for flight control, in beetles it seems that vision is superseded by other modalities [78], but it has remained unclear why during flight beetles stretch out their forelegs, which increases air resistance, in contrast to other insects. The hypothesis that beetles' legs have a different role in flight control has been tested in a series of studies [79]- [81], including tethered experiments, with and without electrical stimulation, and free-flight studies. The authors found that beetles' legs are fundamental in flight directional steering and in controlling wingbeat during landing, which can have profound implications both in further understanding motor control but also in designing novel miniature flying robots.…”