The mechanics and control of pitching manoeuvres in a freely flying hawkmoth (Manduca sexta)

Bo Cheng; Xinyan Deng; Tyson L. Hedrick

doi:10.1242/jeb.062760

journal article Dec 15, 2011

The mechanics and control of pitching manoeuvres in a freely flying hawkmoth (Manduca sexta)

Bo Cheng

Xinyan Deng

Tyson L. Hedrick

Journal of Experimental Biology Vol. 214 No. 24 pp. 4092-4106 · The Company of Biologists

View at Publisher Save 10.1242/jeb.062760

Abstract

SUMMARYInsects produce a variety of exquisitely controlled manoeuvres during natural flight behaviour. Here we show how hawkmoths produce and control one such manoeuvre, an avoidance response consisting of rapid pitching up, rearward flight, pitching down (often past the original pitch angle), and then pitching up slowly to equilibrium. We triggered these manoeuvres via a sudden visual stimulus in front of free-flying hawkmoths (Manduca sexta) while recording the animals' body and wing movements via high-speed stereo videography. We then recreated the wing motions in a dynamically scaled model to: (1) associate wing kinematic changes with pitch torque production and (2) extract the open-loop dynamics of an uncontrolled moth. Next, we characterized the closed-loop manoeuvring dynamics from the observed flight behaviour assuming that hawkmoths use feedback control based on translational velocity, pitch angle and angular velocity, and then compared these with the open-loop dynamics to identify the control strategy used by the moth. Our analysis revealed that hawkmoths produce active pitch torque via changes in mean wing spanwise rotation angle. Additionally, body translations produce passive translational damping and pitch torque, both of which are linearly dependent on the translational velocity. Body rotations produce similar passive forces and torques, but of substantially smaller magnitudes. Our comparison of closed-loop and open-loop dynamics showed that hawkmoths rely largely on passive damping to reduce the body translation but use feedback control based on pitch angle and angular velocity to control their orientation. The resulting feedback control system remains stable with sensory delays of more than two wingbeats.

Topics

No keywords indexed for this article. Browse by subject →

References

40

[1]

Bender "Comparison of visual and haltere-mediated feedback in the control of body saccades in Drosophila melanogaster" J. Exp. Biol. (2006) 10.1242/jeb.02583

[2]

Bergou "Fruit flies modulate passive wing pitching to generate in-flight turns" Phys. Rev. Lett. (2010) 10.1103/physrevlett.104.148101

[3]

Cheng "Translational and rotational damping of flapping flight and its dynamics and stability at hovering" IEEE Trans. Rob. (2011) 10.1109/tro.2011.2156170

[4]

Cheng "Aerodynamic damping during rapid flight maneuvers in the fruit fly Drosophila" J. Exp. Biol. (2009) 10.1242/jeb.038778

[5]

Combes "Flexural stiffness in insect wings. II. Spatial distribution and dynamic wing bending" J. Exp. Biol. (2003) 10.1242/jeb.00524

[6]

Cowan "Task-level control of rapid wall following in the American cockroach" J. Exp. Biol. (2006) 10.1242/jeb.02166

[7]

Deng "Flapping flight for biomimetic robotic insects: part I – system modeling" IEEE Trans. Rob. (2006) 10.1109/tro.2006.875480

[8]

Dickinson "The initiation and control of rapid flight maneuvers in fruit flies" Integr. Comp. Biol. (2005) 10.1093/icb/45.2.274

[9]

Wing Rotation and the Aerodynamic Basis of Insect Flight

Michael H. Dickinson, Fritz-Olaf Lehmann, Sanjay P. Sane

Science 1999 10.1126/science.284.5422.1954

[10]

Dickson "A linear systems analysis of the yaw dynamics of a dynamically scaled insect model" J. Exp. Biol. (2010) 10.1242/jeb.042978

[11]

Dudley (2000) 10.1515/9780691186344

[12]

Ellington "The aerodynamics of hovering insect flight. II. Morphological parameters" Phil. Trans. R. Soc. Lond. B (1984) 10.1098/rstb.1984.0051

[13]

Etkin (1996)

[14]

Faruque "Dipteran insect flight dynamics. Part I. Longitudinal motion about hover" J. Theor. Biol. (2010) 10.1016/j.jtbi.2010.02.018

[15]

Fry "The aerodynamics of free-flight maneuvers in Drosophila" Science (2003) 10.1126/science.1081944

[16]

Gao "A numerical analysis of dynamic flight stability of hawkmoth hovering" J. Biomech. Sci. Eng. (2009) 10.1299/jbse.4.105

[17]

Hedrick "Software techniques for two- and three-dimensional kinematic measurements of biological and biomimetic systems" Bioinspir. Biomim. (2008) 10.1088/1748-3182/3/3/034001

[18]

Hedrick "Low speed maneuvering flight of the rose-breasted cockatoo (Eolophus roseicapillus). I. Kinematic and neuromuscular control of turning" J. Exp. Biol. (2007) 10.1242/jeb.002055

[19]

Hedrick "Within-wingbeat damping: dynamics of continuous free-flight yaw turns in Manduca sexta. Biol" (2010)

[20]

Hedrick "Wingbeat time and the scaling of passive rotational damping in flapping flight" Science (2009) 10.1126/science.1168431

[21]

Ishihara "A two-dimensional computational study on the fluid–structure interaction cause of wing pitch changes in dipteran flapping flight" J. Exp. Biol. (2009) 10.1242/jeb.020404

[22]

Kammer "The motor output during turning flight in a hawkmoth, Manduca sexta" J. Insect Physiol. (1971) 10.1016/0022-1910(71)90011-4

[23]

Kelber "Light intensity limits foraging activity in nocturnal and crepuscular bees" Behav. Ecol. (2006) 10.1093/beheco/arj001

[24]

Murray (1994)

[25]

Ramamurti "A computational investigation of the three-dimensional unsteady aerodynamics of Drosophila hovering and maneuvering" J. Exp. Biol. (2007) 10.1242/jeb.02704

[26]

Ristroph "Discovering the flight autostabilizer of fruit flies by inducing aerial stumbles" Proc. Natl. Acad. Sci. USA (2010) 10.1073/pnas.1000615107

[27]

Rohrseitz "Behavioural system identification of visual flight speed control in Drosophila melanogaster" J. R. Soc. Interface (2011) 10.1098/rsif.2010.0225

[28]

Sane "Antennal mechanosensors mediate flight control in moths" Science (2007) 10.1126/science.1133598

[29]

Sprayberry "Responses of descending visually-sensitive neurons in the hawkmoth, Manduca sexta, to three-dimensional flower-like stimuli" J. Insect Sci. (2009) 10.1673/031.009.0701

[30]

Sun "Dynamic flight stability of a hovering bumblebee" J. Exp. Biol. (2005) 10.1242/jeb.01407

[31]

Sun "Flight stabilization control of a hovering model insect" J. Exp. Biol. (2007) 10.1242/jeb.004507

[32]

Taylor "Mechanics and aerodynamics of insect flight control" (2001)

[33]

Taylor "Sensory systems and flight stability: what do insects measure and why?" (2007) 10.1016/s0065-2806(07)34005-8

[34]

Taylor "Dynamic flight stability in the desert locust Schistocerca gregaria" J. Exp. Biol. (2003) 10.1242/jeb.00501

[35]

Theobald J. C. (2004). Perceiving motion in the dark.PhD thesis, University of Washington, Seattle, WA, USA, 121 pp.

[36]

Willmott "The mechanics of flight in the hawkmoth Manduca sexta. II. Aerodynamic consequences of kinematic and morphological variation" J. Exp. Biol. (1997) 10.1242/jeb.200.21.2723

[37]

Wu "Unsteady aerodynamic forces of a flapping wing" J. Exp. Biol. (2004) 10.1242/jeb.00868

[38]

Zhang "Dynamic flight stability of a hovering model insect: lateral motion" Acta Mech. Sin. (2009) 10.1007/s10409-009-0303-1

[39]

Zhao "Power distribution in the hovering flight of the hawk moth Manduca sexta" Bioinspir. Biomim. (2009) 10.1088/1748-3182/4/4/046003

[40]

Aerodynamic effects of flexibility in flapping wings

Liang Zhao, Qingfeng Huang, Xinyan Deng et al.

Journal of The Royal Society Interface 2009 10.1098/rsif.2009.0200

Metrics

154

Citations

40

References

Details

Published: Dec 15, 2011
Vol/Issue: 214(24)
Pages: 4092-4106

Authors

B

Bo Cheng

Purdue University, School of Mechanical Engineering, Zucrow Laboratories, 500 Allison Road, Chaffee Hall, West Lafayette, IN 47907, USA

X

Xinyan Deng

Purdue University, School of Mechanical Engineering, Zucrow Laboratories, 500 Allison Road, Chaffee Hall, West Lafayette, IN 47907, USA

T

Tyson L. Hedrick

University of North Carolina at Chapel Hill, Department of Biology CB #3280, Chapel Hill, NC 27599, USA

Cite This Article

Bo Cheng, Xinyan Deng, Tyson L. Hedrick (2011). The mechanics and control of pitching manoeuvres in a freely flying hawkmoth (Manduca sexta). Journal of Experimental Biology, 214(24), 4092-4106. https://doi.org/10.1242/jeb.062760

The mechanics and control of pitching manoeuvres in a freely flying hawkmoth (Manduca sexta)

You May Also Like