Pheromone-controlled anemotaxis in moths

Males of several moth species possess very sensitive chemoreceptors for detecting conspecific female sex pheromone. Behavioural experiments conducted in wind tunnels, as well as electrophysiological experiments with pulsed odor stimuli, revealed that moths are remarkably well adapted to the rapid changes in stimulus concentration they encounter in a natural odor plume. As a walking or a flying moth orients to an odor source, it displays turning responses to individual odor pulses of only a few tens of ms duration. Both receptor cells and central neurons can resolve up to ten odor pules per second. When odor pulses stop coming, a walking moth circles on the spot, and a flying moth selects a path transverse to the odor plume, both types of behaviour being thought to serve for regaining olfactory information. Concentration gradients within the odor plume, however, do not provide reliable information on the location of the odor source. The odor pulses rather act to trigger locomotion upwind (positive anemotaxis), a strategy that will eventually guide the male to the odor source. Moths progress upwind most effectively when the odor pulses are repeated at a rate of about 3/s, regardless of the stimulus intensity. The orientational cues by which the animal adjusts its upwind course of locomotion are provided by mechanical and visual stimuli. Possible mechanisms for odorelicited anemotaxis are discussed, in particular the cybernetic model system of Kramer ( 1996) with two feedback loops, that explains anemotactic orientation in flight based solely on the flow of ground patterns over the animal’s eyes. A model system for walking requires only one feedback loop. Computer simulations of anemotactic behaviour produce flight and walking tracks similar to those observed in real animals. The odor stimulus modulates several parameters of this model.

[1]  R. Cardé,et al.  Responses of Lepidoptera to Synthetic Sex Pheromone Chemicals and Their Analogues , 1977 .

[2]  D. Varjú,et al.  Localization and Orientation in Biology and Engineering , 1984, Proceedings in Life Sciences.

[3]  R. Cardé,et al.  Insect Pheromone Research: New Directions , 1997 .

[4]  T. Baker,et al.  Reiterative responses to single strands of odor promote sustained upwind flight and odor source location by moths. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[5]  M. Wortmann,et al.  WING MOVEMENTS AND LIFT REGULATION IN THE FLIGHT OF DESERT LOCUSTS , 1993 .

[6]  R. D. Collins,et al.  Influence of pheromone concentration and ambient temperature on flight of the gypsy moth, Lymantria dispar (L), in a sustained‐flight wind tunnel , 1993 .

[7]  Esch,et al.  Distance estimation by foraging honeybees , 1996, The Journal of experimental biology.

[8]  R. Preiss,et al.  Stabilization of altitude and speed in tethered flying gypsy moth males: influence of (+) and (‐)‐disparlure , 1983 .

[9]  Temporal characteristics of pheromone receptor cell responses in relation to orientation behaviour of moths , 1986 .

[10]  M. Beroza,et al.  Isolation, Identification, and Synthesis of the Sex Attractant of Gypsy Moth , 1960, Science.

[11]  T. Baker,et al.  COMPARISON OF MANOEUVRES USED BY WALKING VERSUS FLYING GRAPHOLITA MOLESTA MALES DURING PHEROMONE-MEDIATED UPWIND MOVEMENT , 1987 .

[12]  Q. Paynter,et al.  The effect of wind speed on the flight responses of tsetse flies to CO2: a wind‐tunnel study , 1996 .

[13]  M. J. Packer,et al.  Odour movement, wind direction, and the problem of host‐finding by tsetse flies , 1989 .

[14]  G. A. Kerkut,et al.  Comprehensive insect physiology, biochemistry, and pharmacology , 1985 .

[15]  E. Kramer,et al.  Orientation of the Male Silkmoth to the Sex Attractant Bombykol , 1975 .

[16]  K. Kaissling.  Antennae and Noses: Their Sensitivities as Molecule Detectors , 1990 .

[17]  A. Borst,et al.  A look into the cockpit of the fly: visual orientation, algorithms, and identified neurons , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  K. Kaissling,et al.  Chemo-electrical transduction in insect olfactory receptors. , 1986, Annual review of neuroscience.

[19]  William J. Bell,et al.  Chemical Ecology of Insects , 1985, Springer US.

[20]  J. Murlis.  Odor Plumes and the Signal They Provide , 1997 .

[21]  Ring T. Cardé,et al.  Strategies for recontacting a lost pheromone plume: casting and upwind flight in the male gypsy moth , 1994 .

[22]  C. Rowell,et al.  The perception of the visual flow field by flying locusts : a behavioural and neuronal analysis , 1992 .

[23]  J. Kennedy,et al.  Pheromone-Regulated Anemotaxis in Flying Moths , 1974, Science.

[24]  A. Ludlow,et al.  Finding of a sex pheromone source by gypsy moths released in the field , 1983, Nature.

[25]  A. Ludlow,et al.  Guidance system used in moth sex attraction , 1980, Nature.

[26]  K. Wiese,et al.  Sensory Systems of Arthropods , 1993 .

[27]  R. Cardé,et al.  Fine-scale structure of pheromone plumes modulates upwind orientation of flying moths , 1994, Nature.

[28]  Olfactory sexual communication in Lepidoptera: strategy, sensitivity and selectivity , 1984 .

[29]  Thomas C. Baker,et al.  Pheromone-Mediated Flight in Moths , 1997 .

[30]  A. Greenway,et al.  CONTAMINATION OF VEGETATION WITH SYNTHETIC SEX‐ATTRACTANT RELEASED FROM TRAPS FOR THE PEA MOTH, CYDIA NIGRICANA , 1981 .

[31]  Ernst Kramer,et al.  A Tentative Intercausal Nexus and Its Computer Model on Insect Orientation in Windborne Pheromone Plumes , 1997 .

[32]  Mukerrem Cakmak,et al.  North Carolina State Univ , 1997 .

[33]  W H Bossert,et al.  The analysis of olfactory communication among animals. , 1963, Journal of theoretical biology.

[34]  T. L. Payne,et al.  Mechanisms in Insect Olfaction , 1986 .

[35]  J. Murlis,et al.  Fine‐scale structure of odour plumes in relation to insect orientation to distant pheromone and other attractant sources , 1981 .

[36]  E. Kramer,et al.  The orientation of walking honeybees in odour fields with small concentration gradients , 1976 .

[37]  W. Roelofs,et al.  Response specificity of male moths to multicomponent pheromones , 1989 .

[38]  R. Cardé,et al.  Mechanisms of Flight of Male Moths to Pheromone , 1997 .

[39]  R. Preiss,et al.  Anemotactic orientation of gypsy moth males and its modification by the attractant pheromone (+)‐disparlure during walking , 1986 .

[40]  Joe N. Perry,et al.  Range of action of moth sex‐attractant sources , 1987 .

[41]  M. Wortmann,et al.  ON THE SO-CALLED CONSTANT-LIFT REACTION OF MIGRATORY LOCUSTS , 1989 .

[42]  Joe N. Perry,et al.  A mathematical model for the flight of pea moth to pheromone traps through a crop , 1984 .

[43]  Wenner-Grenska samfundet,et al.  Olfaction and taste , 1963 .

[44]  R. Cardé,et al.  TEMPERATURE MODIFICATION OF MALE SEX PHEROMONE RESPONSE AND FACTORS AFFECTING FEMALE CALLING IN HOLOMELINA IMMACULATA (LEPIDOPTERA: ARCTIIDAE) , 1973, The Canadian Entomologist.

[45]  J. Kennedy.  Zigzagging and casting as a programmed response to wind‐borne odour: a review , 1983 .

[46]  T. Baker,et al.  A pulsed cloud of sex pheromone elicits upwind flight in male moths , 1985 .

[47]  J. Parlange,et al.  Turbulent Dispersion of Disparlure in the Forest and Male Gypsy Moth Response , 1976 .

[48]  H. Mustaparta.  Chemical information processing in the olfactory system of insects. , 1990, Physiological reviews.

[49]  R. H. Wright.  The Olfactory Guidance of Flying Insects , 1958, The Canadian Entomologist.

[50]  E. Kramer,et al.  Sensory basis of pheromone-mediated orientation in moths , 1990 .

[51]  Thomas C. Baker,et al.  Field and laboratory electroantennographic measurements of pheromone plume structure correlated with oriental fruit moth behaviour , 1989 .

[52]  T. Baker,et al.  Adaptation of antennal neurons in moths is associated with cessation of pheromone-mediated upwind flight. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[53]  J. Richerson,et al.  Differences in Pheromone Release and Sexual Behavior Between Laboratory-reared and Wild Gypsy Moth Adults , 1974 .

[54]  John G. Hildebrand,et al.  Frequency coding by central olfactory neurons in the sphinx moth Manduca sexta , 1988 .

[55]  Mark A. Willis,et al.  Effects of intermittent and continuous pheromone stimulation on the flight behaviour of the oriental fruit moth, Grapholita molesta , 1984 .

[56]  J. Hildebrand,et al.  Olfactory information processing in the brain: encoding chemical and temporal features of odors. , 1996, Journal of neurobiology.

[57]  E. Kramer,et al.  Control of Flight Speed by Minimization of the Apparent Ground Pattern Movement , 1984 .

[58]  Ring T. Cardé,et al.  Rate and diel periodicity of pheromone emission from female gypsy moths, (Lymantria dispar) determined with a glass-adsorption collection system , 1982 .

[59]  A. Ludlow,et al.  Guidance of flying male moths by wind‐borne sex pheromone , 1981 .

[60]  R. Cardé,et al.  Influence of plume structure and pheromone concentration on upwind flight of Cadra cautella males , 1995 .

[61]  M. Schnee,et al.  ANALYSIS OF INDIVIDUAL GYPSY MOTH SEX PHEROMONE PRODUCTION BY SAMPLE CONCENTRATING GAS CHROMATOGRAPHY , 1983, The Canadian Entomologist.

[62]  John Murtis,et al.  Odor Plumes and How Insects Use Them , 1992 .

[63]  Peter Witzgall,et al.  Modulation of Pheromone-Mediated Flight in Male Moths , 1997 .

[64]  Physiology and systems analysis of gravity orientation in two insect species (Carausius morosus, Calandra granaria). , 1975, Fortschritte der Zoologie.

[65]  T. Baker,et al.  Optomotor anemotaxis polarizes self‐steered zigzagging in flying moths , 1984 .

[66]  W. Roelofs,et al.  Pheromone Components and Active Spaces: What Do Moths Smell and Where Do They Smell It? , 1987, Science.

[67]  E. A. Arbas,et al.  Active Behavior and Reflexive Responses: Another Perspective on Odor-Modulated Locomotion , 1997 .

[68]  E. R. Rumbo,et al.  Adaptation Processes in Insect Olfactory Receptors , 1987, Annals of the New York Academy of Sciences.

[69]  Measured behavioural latency in response to sex-pheromone loss in the large silk moth Antheraea polyphemus. , 1988, The Journal of experimental biology.

[70]  R. Cardé,et al.  Effects of host‐odour plume altitude and changing wind velocity on upwind flight manoeuvres of a specialist braconid parasitoid , 1996 .

[71]  Responses of Male Redbacked Cutworm, Euxoa ochrogaster (Lepidoptera: Noctuidae), to Sex Pheromone Components in a Flight Tunnell1 , 1983 .