Odor tracking flight of male Manduca sexta moths along plumes of different cross-sectional area

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 199, Issue 11, 2013, Pages 1015-1036

  Willis, Mark A ^a   Ford, E A ^a   Avondet, J L ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Behavior; Moth; Olfaction; Orientation; Pheromone

Indexed keywords

SEX PHEROMONE;

ANALYSIS OF VARIANCE; ANIMAL; ANTENNA (ORGAN); ARTICLE; DRUG EFFECT; FEMALE; FLYING; MALE; MANDUCA; METABOLISM; ODOR; ORIENTATION; PHYSIOLOGY; TIME;

ANALYSIS OF VARIANCE; ANIMALS; ARTHROPOD ANTENNAE; FEMALE; FLIGHT, ANIMAL; MALE; MANDUCA; ODORS; ORIENTATION; SEX ATTRACTANTS; TIME FACTORS;

EID: 84886911610     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-013-0856-0     Document Type: Article

References (96)

1. Arbas EA, Willis MA, Kanzaki R (1993) Organization of goal-oriented locomotion: pheromone-modulated flight behavior of moths. In: Beer RD, Ritzmann RE, McKenna T (eds) Biological neural networks in invertebrate neuroethology and robotics. Academic Press, San Diego, pp 159-198.
2. Baker TC (1985) Chemical control of behavior. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology. Pergamon Press, Oxford, pp 621-672.
3. Baker TC (1990) Upwind flight and casting flight: complementary phasic and tonic systems used for location of sex pheromone sources by male moths. In: Døving KB (ed) Proceedings of the 10th international symposium olfaction and taste. Oslo, pp 18-25.
4. Baker TC, Haynes KF (1987) Manoeuvers used by flying male oriental fruit moths to relocate a sex pheromone plume in an experimentally shifted wind-field. Physiol Entomol 12: 263-279.
5. Baker TC, Haynes KF (1989) Field and laboratory electroantennographic measurements of pheromone plume structure correlated with oriental fruit moth behaviour. Physiol Entomol 14: 1-12.
6. Baker TC, Haynes KF (1996) Pheromone-mediated optomotor anemotaxis and altitude control exhibited by male oriental fruit moths in the field. Physiol Entomol 21: 20-32.
7. Baker CF, Montgomery JC (1999) The sensory basis for rheotaxis in the blind Mexican cave fish, Astyanax fasciatus. J Comp Physiol A 184: 519-527.
8. Baker TC, Willis MA, Phelan PL (1984) Optomotor anemotaxis polarizes self-steered zigzagging in flying moths. Physiol Entomol 9: 365-376.
9. Baker TC, Willis MA, Haynes KF, Phelan PL (1985) A pulsed cloud of sex pheromone elicits upwind flight in male moths. Physiol Entomol 10: 257-265.
10. Baker TC, Hansson BS, Löfstedt C, Löfqvist J (1988) Adaptation of antennal neurons in moths is associated with cessation of pheromone-mediated upwind flight. Proc Natl Acad Sci USA 85: 9826-9830.
11. Baker CF, Montgomery JC, Dennis TE (2002) The sensory basis of olfactory search behavior in banded kokopu (Galaxias fasciatus). J Comp Physiol A 188: 553-560.
12. Basil JA, Hanlon RT, Sheikh SI, Atema J (2000) Three-dimensional odor tracking by Nautilus pompilius. J Exp Biol 203: 1409-1414.
13. Bau J, Justus KA, Cardé RT (2002) Antennal resolution of pulsed pheromone plumes in three moth species. J Insect Physiol 48: 433-442.
14. Beglane PF, Grasso FW, Basil JA, Atema J (1997) Far field chemo-orientation in the American lobster, Homarus americanus: effects of unilateral ablation, and lesioning of the lateral antennule. Biol Bull 193: 214-215.
15. Belanger JH, Arbas EA (1998) Behavioral strategies underlying pheromone-modulated flight in moths: lessons from simulation studies. J Comp Physiol A 183: 345-360.
16. Belanger JH, Willis MA (1996) Adaptive control of odor-guided locomotion: behavioral flexibility as an antidote to environmental unpredictability. Adapt Behav 4: 217-253.
17. Bell WJ, Tobin TR (1981) Orientation to sex pheromone in the American cockroach: Analysis of chemo-orientation mechanisms. J Insect Physiol 27: 501-508.
18. Borst A, Heisenberg M (1982) Osmotropotaxis in Drosophila melanogaster. J Comp Physiol A 147: 479-484.
19. Brown B, Rittschoff D (1984) Effects of flow and concentration of attractant on newly hatched oyster drills Urosalpinx cinerea (Say). Mar Behav Physiol 1: 75-93.
20. Budick SA, Dickinson MH (2006) Free-flight responses of Drosophila melanogaster to attractive odors. J Exp Biol 209: 3001-3017.
21. Cardé RT, Hagaman TE (1979) Behavioral responses of the gypsy moth in a wind tunnel to air-borne enantiomers of disparlure. Environ Entomol 8: 475-484.
22. Carde RT, Minks AK (1995) Control of moth pest by mating disruption: successes and constraints. Ann Rev Entomol 40: 559-585.
23. Cardé RT, Willis MA (2008) Navigational strategies used by insects to find distant, wind-borne sources of odor. J Chem Ecol 34: 854-866.
24. Cardé RT, Staten RT, Mafra-Neto A (1998) Behavior of pink bollworm males near high-dose point sources of pheromone in field wind tunnels insights into mechanisms of mating disruption. Entomol Exp Appl 89: 35-46.
25. Carton AG, Montgomery JC (2003) Evidence of a rheotactic component in the odour search behaviour of freshwater eels. J Fish Biol 2: 501-516.
26. Charlton RE, Kanno H, Collins RD, Cardé RT (1993) Influence of pheromone concentration and ambient temperature on the flight of the gypsy moth, Lymantria dispar (L.), in a sustained-flight wind-tunnel. Physiol Entomol 18: 349-362.
27. David CT, Kennedy JS (1987) The steering of zigzagging flight by male gypsy moths. Naturwissenschaften 74: 194-195.
28. Duistermars BJ, Frye MA (2008) Crossmodal visual input for odor tracking during fly flight. Curr Biol 18: 270-275.
29. Duistermars BJ, Chow DM, Frye MA (2009) Flies require bilateral sensory input to track odor gradients in flight. Curr Biol 19: 1301-1307.
30. Farkas SR, Shorey HH (1972) Chemical trail following by flying insects: A mechanism for orientation to a distant odor source. Science 178: 67-68.
31. Fransson J, Matsubara M, Alfredsson P (2005) Transition induced by free-stream turbulence. J Fluid Mech 527: 1-25.
32. Gardiner JM, Atema J (2010) The function of bilateral odor arrival time differences in olfactory orientation of sharks. Curr Biol 20: 1187-1191.
33. Gnanadesikan R (1997) Methods for statistical data analysis of multivariate observations, 2 edn. Wiley, Inc, New York.
34. Gurun A (2006) Interactions of Tollmien-Schlichting waves and stationary transient disturbances. PhD, Case Western Reserve University.
35. Hoerner SF (1965) Fluid-dynamic drag: practical information on aerodynamic drag and hydrodynamic resistance. Hoerner Fluid Dynamics, Midland Park.
36. Justus KA, Cardé RT, French AS (2004) Dynamic properties of antennal responses to pheromone in two moth species. J Neurophysiol 93: 2233-2239.
37. Kanzaki R (1996) Behavioral and neural basis of instinctive behavior in insects: odor-source searching strategies without memory and learning. Robot Auton Syst 18: 33-43.
38. Kanzaki R (1998) 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.
39. Kanzaki R, Sugi N, Shibuya T (1992) Self-generated zigzag turning of Bombyx mori males during pheromone-mediated upwind walking. Zool Sci 9: 515-527.
40. Keller T, Powell I, Weissburg M (2003) Role of olfactory appendages in chemically mediated orientation of blue crabs. Mar Ecol Prog Ser 261: 217-231.
41. Kennedy JS (1939) The visual responses of flying mosquitoes. Proc Zool Soc Lond A 109: 221-242.
42. Kennedy JS (1977) Olfactory responses to distant plants and other odor sources. In: Shorey HH, McKelvey JJ Jr (eds) Chemical control of insect behavior. Wiley-Interscience, New York, pp 67-91.
43. Kennedy JS (1983) Zigzagging and casting as a response to wind-borne odor: A review. Physiol Entomol 8: 109-120.
44. Kennedy JS, Marsh D (1974) Pheromone regulated anemotaxis in flying moths. Science 184: 999-1001.
45. Kennedy JS, Ludlow AR, Sanders AR (1980) Guidance system used in moth sex attraction. Nature 288: 474-477.
46. Kennedy JS, Ludlow AR, Sanders AR (1981) Guidance of flying male moths by wind-borne sex pheromone. Physiol Entomol 6: 395-412.
47. Kuenen LPS, Baker TC (1982) The effects of pheromone concentration on the flight behavior of the oriental fruit moth, Grapholitha molesta. Physiol Entomol 7: 423-434.
48. Louis M, Huber T, Benton R, Sakmar TP, Vosshall LB (2008) Bilateral olfactory sensory input enhances chemotaxis behavior. Nature Neurosci 11: 187-199.
49. Mafra-Neto A, Cardé RT (1994) Fine-scale structure of pheromone plumes modulates upwind orientation of flying male moths. Nature 369: 142.
50. Mafra-Neto A, Cardé RT (1995a) Effect of the fine-scale structure of pheromone plumes: pulse frequency modulates activation and upwind flight of almond moth males. Physiol Entomol 20: 229-242.
51. Mafra-Neto A, Cardé RT (1995b) Influence of plume structure and pheromone concentration on upwind flight of Cadra cautella males. Physiol Entomol 20: 117-133.
52. Mafra-Neto A, Cardé RT (1996) Dissection of the pheromone modulated flight of moths using single-pulse response as a template. Experientia 52: 373-379.
53. Marsh D, Kennedy JS, Ludlow AR (1978) An analysis of anemotactic zigzagging flight in male moths stimulated by pheromone. Physiol Entomol 3: 221-240.
54. Mayer M, Mankin R, Lemire G (1984) Quantitation of the insect electroantennogram: measurement of sensillar contributions, elimination of background potentials, and relationship to olfactory sensation. J Insect Physiol 30: 757-763.
55. Merlin C, Lucas P, Rochat D, Francois M, Maibeche-Coisne M, Jacquin-Joly E (2007) An antennal circadian clock and circadian rhythms in peripheral pheromone reception in the moth Spodoptera littoralis. J Biol Rhythm 22: 502.
56. Miller JR, Roelofs WL (1978) Sustained-flight tunnel for measuring insect responses to wind-borne sex pheromones. J Chem Ecol 4: 187-198.
57. Mishima T, Kanzaki R (1998) Coordination of flipflopping neural signals and head turning during pheromone-mediated walking in a male silkworm moth Bombyx mori. J Comp Physiol A 183: 273-282.
58. Montgomery JC, Diebel C, Halstead MDB, Downer J (1999) Olfactory search tracks in the Antarctic fish Trematomus bernacchii. Polar Biol 21: 151-154.
59. Murlis J (1986) The structure of odour plumes. In: Payne TL, Birch MC, Kennedy CEJ (eds) Mechanisms in insect olfaction. Clarendon Press, Oxford, pp 27-38.
60. Murlis J, Jones CD (1981) Fine scale structure of odour plumes in relation to insect orientation to distant pheromone and other attractant sources. Physiol Entomol 6: 71-86.
61. Murlis J, Willis MA, Cardé RT (1990) Odor signals: patterns in time and space. In: Døving K (ed) Proceedings of the 10th international symposium on olfaction and taste, Oslo.
62. Murlis J, Willis MA, Cardé RT (2000) Spatial and temporal structure of pheromone plumes in fields and forests. Physiol Entomol 25(211): 222.
63. Page JL, Dickman BD, Webster DR, Weissburg MJ (2011a) Getting ahead: context-dependent responses to odorant filaments drive along stream progress during odor tracking in blue crabs. J Exp Biol 214: 1498-1512.
64. Page JL, Dickman BD, Webster DR, Weissburg MJ (2011b) Staying the course: chemical signal spatial properties and concentration mediate cross-stream motion in turbulent plumes. J Exp Biol 214: 1513-1522.
65. Pilla RS, Kitska DJ, Loader C (2005) Statistical analysis of modified complete randomized designs: Applications to chemo-orientation studies. J Exp Biol 208: 1267-1276.
66. Porter J, Craven B, Khan RH, Chang S-J, Kang I, Judkewicz B, Volpe J, Settles G, Sobel N (2007) Mechanisms of scent-tracking in humans. Nature Neurosci 10: 27-29.
67. Preiss R, Kramer E (1986) Mechanism of pheromone orientation in flying moths. Naturwissenschaften 73: 555-557.
68. Rajan R, Clement JP, Bhalla US (2006) Rats smell in stereo. Science 311: 666-670.
69. Roelofs WL (1984) Electroantennogram assays: rapid and convenient screening procedures for pheromones. In: Hummel HE, Miller TA (eds) Techniques in pheromone research. Springer, New York, pp 131-159.
70. Rutkowski A, Quinn R, Willis MA (2009) Three-dimensional characterization of the wind-borne pheromone tracking behavior of male hawk moths, Manduca sexta. J Comp Physiol A 195: 39-54.
71. Sasaki M, Riddiford LM (1984) Regulation of reproductive behavior and egg maturation in the tobacco hawk moth, Manduca sexta. Physiol Entomol 9: 315-327.
72. Talley JL (2010) Males chasing females: A comparison of flying Manduca sexta and walking Periplaneta americana male tracking behavior to female sex pheromones in different flow environments. PhD, Case Western Reserve University, ProQuest LLC.
73. Tobin TR (1981) Pheromone orientation: role of internal control mechanisms. Science 214: 1147-1149.
74. Tumlinson JH, Brennan MM, Doolittle RE, Mitchell ER, Brabham A, Mazomenos E, Baumhover AH, Jackson DM (1989) Identification of a pheromone blend attractive to Manduca sexta (L.) males in a wind tunnel. Arch Insect Biochem Physiol 10: 255-271.
75. Valeur PG, Hansson BS, Markebo K, Lofstedt C (2000) Relationship between sex pheromone elicited behaviour and response of single olfactory receptor neurones in a wind tunnel. Physiol Entomol 25: 223-232.
76. Vickers NJ (2000) Mechanisms of animal navigation in odor plumes. Biol Bull 198: 203-212.
77. Vickers NJ, Baker TC (1991) The effects of unilateral antennectomy on the flight behavior of male Heliothis virescens in a pheromone plume. Physiol Entomol 16: 497-506.
78. Vickers NJ, Baker TC (1992) Male Heliothis virescens maintain upwind flight in response to experimentally pulsed filaments of their sex pheromone (Lepidoptera: noctuidae). J Insect Behav 5: 669-687.
79. Vickers NJ, Baker TC (1994) Reiterative responses to single strands of odor promote sustained upwind flight and odor source location by moths. Proc Natl Acad Sci USA 91: 5756-5760.
80. Vickers NJ, Baker TC (1996) Latencies of behavioral response to interception of filaments of sex pheromone and clean air influence flight track shape in Heliothis virescens (F.) males. J Comp Physiol A 178: 831-847.
81. Vickers NJ, Baker TC (1997) Flight of Heliothis virescens males in the field in response to sex pheromone. Physiol Entomol 22: 277-285.
82. Vickers NJ, Christensen TA, Baker TC, Hildebrand JG (2001) Odour-plume dynamics influence the brain's olfactory code. Nature 410: 466-470.
83. Vogel S (1994) Life in moving fluids. Princeton University Press, Princeton.
84. Webb B, Harrison RR, Willis MA (2004) Sensorimotor control of navigation in arthropod and artificial systems. Arthropod Struct Dev 33: 301-329.
85. Webster DR, Weissburg MJ (2001) Chemosensory guidance cues in a turbulent chemical odor plume. Limnol Oceanogr 46: 1034-1047.
86. Weissburg MJ (2000) The fluid dynamical context of chemosensory behavior. Biol Bull 198: 188-200.
87. Weissburg MJ, Zimmer-Faust RK (1994) Odor plumes and how blue crabs use them in finding prey. J Exp Biol 197: 349-375.
88. Willis MA (2008) Odor plumes and animal orientation. In: Basbaum AI, Kaneko A, Shepherd GM, Westheimer G (eds) The senses: A comprehensive reference, vol 4. Academic Press, San Diego, pp 771-782.
89. Willis MA, Arbas EA (1991) Odor-modulated upwind flight of the sphinx moth, Manduca sexta L. J Comp Physiol A 169: 427-440.
90. Willis MA, Arbas EA (1998) Variability in odor-modulated flight by moths. J Comp Physiol A 182: 191-202.
91. Willis MA, Avondet JL (2005) Odor-modulated orientation in walking male cockroaches, Periplaneta americana (L.), and the effects of odor plumes of different structure. J Exp Biol 208: 721-735.
92. Willis MA, Baker TC (1988) Effects of varying sex pheromone component ratios on the zigzagging flight movements of the oriental fruit moth, Grapholita molesta. J Insect Behav 1: 357-371.
93. Willis MA, Baker TC (1994) Behaviour of flying oriental fruit moth males during approach to sex pheromone sources. Physiol Entomol 19: 61-69.
94. Willis MA, Murlis J, Carde RT (1991) Pheromone-mediated upwind flight of male gypsy moths, Lymantria dispar, in a forest. Physiol Entomol 16: 507-521.
95. Willis MA, David CT, Murlis J, Cardé RT (1994) Effects of pheromone plume structure and visual stimuli on the pheromone-modulated upwind flight of male gypsy moths (Lymantria dispar), in a forest. J Insect Behav 7: 385-409.
96. Zimmer-Faust RK, Finelli CM, Pentcheff ND, Wethey DS (1995) Odor Plumes and animal navigation in turbulent water flow: A field study. Biol Bull 188: 111-116.