Advertisement

Journal of Comparative Physiology A

, Volume 200, Issue 8, pp 723–738 | Cite as

Responses of a pair of flying locusts to lateral looming visual stimuli

  • Indika Benaragama
  • John R. Gray
Original Paper

Abstract

We presented a pair of locusts flying loosely tethered with laterally looming discs. Two experiments tested whether looming-evoked flight behaviour was affected by the presence (1) or relative position (2) of a conspecific. We recorded: the type of behavioural response, motion within 6 degrees of freedom, behavioural onset time and duration, distance between individuals and relative direction of motion. Response distributions of the locust furthest from the stimulus (L1) were not affected by the presence or relative position of a conspecific, whereas distributions of the closer locust (L2) were affected by its position relative to the stimulus. Motion tracks of L1 were affected by the presence of L2, which generated relatively robust responses directed forward and away from the stimulus. Translational and rotational motion of L1 differed across treatments in both experiments, whereas L2 motion was less sensitive to the presence or position of a conspecific. The start and duration of the behaviour were invariant to the presence or position of a conspecific and locust pairs maintained a fixed distance during responses to looming. Results suggest that looming-evoked behaviour is influenced by visual cues from a conspecific in the vicinity.

Keywords

Insect Flight Collision avoidance Vision Locust 

Notes

Acknowledgments

Funding provided by the Natural Sciences and Engineering Research Council of Canada, the Canada Foundation for Innovation, and the University of Saskatchewan.

Supplementary material

359_2014_916_MOESM1_ESM.pdf (69 kb)
Supplementary Figure 1 Two-dimensional motion tracks from Experiment 1 with the azimuthal (top panels) and elevation (bottom panels) planes of L1 (n = 19) and L2 (n = 19) separated into active steering (black lines) and non-steering (glide or startle, grey lines) behaviours. Data were aligned relative to the initial position at the start of the recording (x, y, z coordinates = 0,0,0) and represent motion tracks during the behavioural epoch. Inset in each graph plot shows the average motion vectors from all animals during the first 2 frames of the behavioural epoch. For all data positive (negative) deviations along the x, y and z axis represent movement to the right (left), up (down) or forward (back), respectively. The data show that active steering resulted in greater excursions in the x-plane compared to glides or startle responses and average vectors show more pronounced motion to the left (away from the stimulus). Nevertheless, glides and startle responses also resulted in excursions within the x-plane that were, on average for L2, to the left. For L1, irrespective of response type, and L2 non-steering behaviours, motion within the y-plane was maintained along the longitudinal midline (i.e. motion was primarily forward with little change in altitude). Active steering in L2 resulted in an average decrease in altitude. (PDF 68 kb)
359_2014_916_MOESM2_ESM.pdf (68 kb)
Supplementary Figure 2. Two-dimensional motion tracks from Experiment 2 within the azimuthal (top panels) and elevation (bottom panels) planes of L1 (n = 18) and L2 (n = 18) separated into active steering (black lines) and non-steering (glide or startle, grey lines) behaviours. Data were aligned relative to the initial position at the start of the recording (x, y, z coordinates = 0,0,0) and represent motion tracks during the behavioural epoch. Inset in each graph plot shows the average motion vectors from all animals during the first two frames of the behavioural epoch. For all data positive (negative) deviations along the x, y and z axis represent movement to the right (left), up (down) or forward (back), respectively. The data show similar trends as described in Supplementary Figure 1 except that the average motion vector for L1 in the azimuthal plane aligned with 0 in the x axis. (PDF 67 kb)

References

  1. Baker PS, Gewecke M, Cooter RJ (1981) The natural flight of the migratory locust, Locusta migratoria L. III. Wing-beat frequency, flight speed and attitude. J Comp Physiol A 141:233–237CrossRefGoogle Scholar
  2. Baker PS, Gewecke M, Cooter RJ (1984) Flight orientation of swarming Locusta migratoria. Physiol Entomol 9:247–252CrossRefGoogle Scholar
  3. Ball D, Tronick E (1971) Infant responses to impending collision—optical and real. Science 171:818–820PubMedCrossRefGoogle Scholar
  4. Berger S, Kutsch W (2003) Turning manoeuvres in free-flying locusts: high-speed video-monitoring. J Exp Zool Part A Comp Exp Biol 299:127–138CrossRefGoogle Scholar
  5. Burrows M, Rowell CHF (1973) Connections between descending visual interneurons and metathoracic motoneurons in the locust. J Comp Physiol A 85:221–234CrossRefGoogle Scholar
  6. Cao P, Gu Y, Wang SR (2004) Visual neurons in the pigeon brain encode the acceleration of stimulus motion. J Neurosci 24:7690–7698PubMedCrossRefGoogle Scholar
  7. Chan RW, Gabbiani F (2013) Collision-avoidance behaviors of minimally restrained flying locusts to looming stimuli. J Exp Biol 216:641–655PubMedCentralPubMedCrossRefGoogle Scholar
  8. Dawson JW, Dawson-Scully K, Robert D, Robertson RM (1997) Forewing asymmetries during auditory avoidance in flying locusts. J Exp Biol 200:2323–2335PubMedGoogle Scholar
  9. Dawson JW, Kutsch W, Robertson RM (2004) Auditory-evoked evasive manoeuvres in free-flying locusts and moths. J Comp Physiol A 190:69–84CrossRefGoogle Scholar
  10. Dewell RB, Gabbiani F (2012) Escape behavior: linking neural computation to action. Curr Biol 22:R152–R153. doi: 10.1016/j.cub.2012.01.034 PubMedCrossRefGoogle Scholar
  11. Domenici P, Batty RS (1997) Escape behaviour of solitary herring (Clupea harengus) and comparisons with schooling individuals. Mar Biol 128:29–38CrossRefGoogle Scholar
  12. Edmunds M, Brunner D (1999) Ethology of defenses against predators. In: Prete FR, Wells H, Wells PH, Hurd LE (eds) The praying mantids. Johns Hopkins University Press, Baltimore, pp 276–302Google Scholar
  13. Ellard CG (2004) Visually guided locomotion in the gerbil: a comparison of open- and closed-loop control. Behav Brain Res 149:41–48PubMedCrossRefGoogle Scholar
  14. Farrow RA (1990) Flight and migration in Acridoids. In: Chapman RF, Joern A (eds) Biology of grasshoppers. Wiley, New York, pp 227–314Google Scholar
  15. Fotowat H, Gabbiani F (2007) Relationship between the phases of sensory and motor activity during a looming-evoked multistage escape behavior. J Neurosci 27:10047–10059PubMedCentralPubMedCrossRefGoogle Scholar
  16. Fotowat H, Fayyazuddin A, Bellen HJ, Gabbiani F (2009) A novel neuronal pathway for visually guided escape in Drosophila melanogaster. J Neurophysiol 102:875–885PubMedCentralPubMedCrossRefGoogle Scholar
  17. Gabbiani F, Krapp HG, Laurent G (1999) Computation of object approach by a wide-field motion-sensitive neuron. J Neurosci 19:1122–1141PubMedGoogle Scholar
  18. Gabbiani F, Mo CH, Laurent G (2001) Invariance of angular threshold computation in a wide-field looming-sensitive neuron. J Neurosci 21:314–329PubMedGoogle Scholar
  19. Gabbiani F, Krapp HG, Hatsopoulos NG et al (2004) Multiplication and stimulus invariance in a looming-sensitive neuron. J Physiol Paris 98:19–34PubMedCrossRefGoogle Scholar
  20. Gray JR (2005) Habituated visual neurons in locusts remain sensitive to novel looming objects. J Exp Biol 208:2515–2532PubMedCrossRefGoogle Scholar
  21. Gray JR, Lee JK, Robertson RM (2001) Activity of descending contralateral movement detector neurons and collision avoidance behaviour in response to head-on visual stimuli in locusts. J Comp Physiol A 187:115–129PubMedCrossRefGoogle Scholar
  22. Gray JR, Blincow E, Robertson R (2010) A pair of motion-sensitive neurons in the locust encode approaches of a looming object. J Comp Physiol A 196:927–938CrossRefGoogle Scholar
  23. Guest BB, Gray JR (2006) Responses of a looming-sensitive neuron to compound and paired object approaches. J Neurophysiol 95:1428–1441PubMedCrossRefGoogle Scholar
  24. Imada H, Hoki M, Suehiro Y, et al (2010) Coordinated and cohesive movement of two small conspecific fish induced by eliciting a simultaneous optomotor response. PLoS ONE. doi: 10.1371/journal.pone.0011248
  25. Judge SJ, Rind FC (1997) The locust DCMD, a movement-detecting neurone tightly tuned to collision trajectories. J Exp Biol 200:2209–2216PubMedGoogle Scholar
  26. Kang H-J, Li X-H (2010) Response properties and receptive field organization of collision-sensitive neurons in the optic tectum of bullfrog, Rana catesbeiana. Neurosci Bull 26:304–316PubMedCrossRefGoogle Scholar
  27. Kennedy JS (1951) The migration of the desert locust (Schistocerca gregaria Forsk.). I. The behaviour of swarms II. A theory of long-range migrations. Phil Trans R Soc (Lond) B 235:163–290Google Scholar
  28. Krapp HG, Gabbiani F (2005) Spatial distribution of inputs and local receptive field properties of a wide-field, looming sensitive neuron. J Neurophysiol 93:2240–2253PubMedCrossRefGoogle Scholar
  29. Krapp HG, Hengstenberg B, Hengstenberg R (1998) Dendritic structure and receptive-field organization of optic flow processing interneurons in the fly. J Neurophysiol 79:1902–1917PubMedGoogle Scholar
  30. Kullberg C, Jakobsson S, Fransson T (1998) Predator-induced take-off strategy in great tits (Parus major). Proc R Soc B Biol Sci 265:1659–1664CrossRefGoogle Scholar
  31. Libersat F, Hoy RR (1991) Ultrasonic startle behavior in bushcrickets (Orthoptera; Tettigoniidae). J Comp Physiol A 169:507–514PubMedCrossRefGoogle Scholar
  32. Lind J, Kaby U, Jakobsson S (2002) Split-second escape decisions in blue tits (Parus caeruleus). Naturwissenschaften 89:420–423PubMedCrossRefGoogle Scholar
  33. Maier JX, Neuhoff JG, Logothetis NK, Ghazanfar AA (2004) Multisensory integration of looming signals by Rhesus monkeys. Neuron 43:177–181PubMedCrossRefGoogle Scholar
  34. McMillan GA, Gray JR (2012) A looming-sensitive pathway responds to changes in the trajectory of object motion. J Neurophysiol 108:1052–1068PubMedCrossRefGoogle Scholar
  35. McMillan GA, Loessin V, Gray JR (2013) Bilateral flight muscle activity predicts wing kinematics and 3-dimensional body orientation of locusts responding to looming objects. J Exp Biol 216:3369–3380PubMedCrossRefGoogle Scholar
  36. Nakagawa H, Hongjian K (2010) Collision-sensitive neurons in the optic tectum of the bullfrog, Rana catesbeiana. J Neurophysiol 104:2487–2499PubMedCrossRefGoogle Scholar
  37. Oliva D, Medan V, Tomsic D (2007) Escape behavior and neuronal responses to looming stimuli in the crab Chasmagnathus granulatus (Decapoda: Grapsidae). J Exp Biol 210:865–880PubMedCrossRefGoogle Scholar
  38. O’Shea M, Williams JLD (1974) The anatomy and output connections of a locust visual interneurone: the lobula giant movement detector (LGMD) neurone. J Comp Physiol 91:257–266CrossRefGoogle Scholar
  39. Parrish JK, Viscido SV, Grünbaum D (2002) Self-organized fish schools: an examination of emergent properties. Biol Bull 202:296–305PubMedCrossRefGoogle Scholar
  40. Paskins KE, Bowyer A, Megill WM, Scheibe JS (2007) Take-off and landing forces and the evolution of controlled gliding in northern flying squirrels Glaucomys sabrinus. J Exp Biol 210:1413–1423PubMedCrossRefGoogle Scholar
  41. Preiss R (1992) Set point of retinal velocity of ground images in the control of swarming flight of desert locusts. J Comp Physiol A 171:251–256CrossRefGoogle Scholar
  42. Preiss R, Spork P (1993) Flight-phase and visual-field related optomotor yaw responses in gregarious desert locusts during tethered flight. J Comp Physiol A 172:733–740CrossRefGoogle Scholar
  43. Preuss T, Osei-Bonsu PE, Weiss SA et al (2006) Neural representation of object approach in a decision-making motor circuit. J Neurosci 26:3454–3464PubMedCrossRefGoogle Scholar
  44. Rind FC, Simmons PJ (1997) Signaling of object approach by the DCMD neuron of the locust. J Neurophysiol 77:1029–1033PubMedGoogle Scholar
  45. Robertson RM, Johnson AG (1993a) Collision avoidance of flying locusts: steering torques and behaviour. J Exp Biol 183:35–60Google Scholar
  46. Robertson RM, Johnson AG (1993b) Retinal image size triggers obstacle avoidance in flying locusts. Naturwissenschaften 80:176–178CrossRefGoogle Scholar
  47. Robertson RM, Reye DN (1992) Wing movements associated with collision-avoidance manoeuvers during flight in the locust Locusta migratoria. J Exp Biol 163:231–258Google Scholar
  48. Robertson RM, Kunhert CT, Dawson JW (1996) Thermal avoidance during flight in the locust Locusta migratoria. J Exp Biol 199:1383–1393PubMedGoogle Scholar
  49. Rogers SM, Harston GWJ, Kilburn-Toppin F et al (2010) Spatiotemporal receptive field properties of a looming-sensitive neuron in solitarious and gregarious phases of the desert locust. J Neurophysiol 103:779–792PubMedCentralPubMedCrossRefGoogle Scholar
  50. Santer RD, Simmons PJ, Rind FC (2005a) Gliding behaviour elicited by lateral looming stimuli in flying locusts. J Comp Physiol A 191:61–73CrossRefGoogle Scholar
  51. Santer RD, Yamawaki Y, Rind FC, Simmons PJ (2005b) Motor activity and trajectory control during escape jumping in the locust Locusta migratoria. J Comp Physiol A 191:965–975CrossRefGoogle Scholar
  52. Santer RD, Rind FC, Stafford R, Simmons PJ (2006) Role of an identified looming-sensitive neuron in triggering a flying locust’s escape. J Neurophysiol 95:3391–3400PubMedCrossRefGoogle Scholar
  53. Schiff W, Caviness JA, Gibson JJ (1962) Persistent fear responses in rhesus monkeys to the optical stimulus of “looming”. Science 136:982–983PubMedCrossRefGoogle Scholar
  54. Simmons PJ (1980) Connexions between a movement-detecting visual interneurone and flight motoneurones of a locust. J Exp Biol 86:87–97Google Scholar
  55. Simmons PJ, Rind FC (1992) Orthopteran DCMD neuron: a reevaluation of responses to moving objects. II. Critical cues for detecting approaching objects. J Neurophysiol 68:1667–1682PubMedGoogle Scholar
  56. Spork P, Preiss R (1993) Control of flight by means of lateral visual-stimuli in gregarious desert locusts, Schistocerca gregaria. Physiol Entomol 18:195–203CrossRefGoogle Scholar
  57. Straw AD (2008) Vision Egg: an open-source library for realtime visual stimulus generation. Front Neuroinform 4:12Google Scholar
  58. Sugiura H, Dickinson MH (2009) The generation of forces and moments during visual-evoked steering maneuvers in flying Drosophila. PLoS ONE. doi: 10.1371/journal.pone.0004883
  59. Sun H, Frost BJ (1998) Computation of different optical variables of looming objects in pigeon nucleus rotundus neurons. Nat Neurosci 1:296–303PubMedCrossRefGoogle Scholar
  60. Uvarov BP (1977) Grasshoppers and locusts. In: A handbook of general acridology, vol 2. Behaviour, ecology, biogeography, population dynamics. Cambridge University Press, Cambridge and Centre for Overseas Pest Research, LondonGoogle Scholar
  61. Verspui R, Gray JR (2009) Visual stimuli induced by self-motion and object-motion modify odour-guided flight of male moths (Manduca sexta L.). J Exp Biol 212:3272–3282PubMedCrossRefGoogle Scholar
  62. Wylie D, Frost BJ (1999) Responses of neurons in the nucleus of the basal optic root to translational and rotational flowfields. J Neurophysiol 81:267–276PubMedGoogle Scholar
  63. Yamamoto K, Nakata M, Nakagawa H (2003) Input and output characteristics of collision avoidance behavior in the frog Rana catesbeiana. Brain Behav Evol 62:201–211PubMedCrossRefGoogle Scholar
  64. Yamawaki Y, Toh Y (2009) Responses of descending neurons to looming stimuli in the praying mantis Tenodera aridifolia. J Comp Physiol A 195:253–264CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of BiologyUniversity of SaskatchewanSaskatoonCanada

Personalised recommendations