Behavioral strategies underlying pheromone-modulated flight in moths: lessons from simulation studies

Abstract Several mechanisms have been proposed to underlie the characteristic `zigzag' tracks produced by moths flying up an odor plume. To test which, if any, of these are capable of reproducing the animals' behavior, we constructed behavioral-level simulations. The simulations are as tightly constrained as possible by the known biology, and incorporate realistic physical effects such as air turbulence, and delays due to sensory transduction and axonal condition, to mimic the dynamics of sensory information encountered by real moths. Formulated as schemas, the models all share a common set of sensory and motor systems, but differ in the interposed control systems. We analyzed the behavior of the models with the same methods we use for real moths. Even the simplest of the models was capable of successful orientation some of the time, and of producing flight tracks similar to those of moths. Individuals which succeeded in tracking the odor plume produced average behavior not significantly different from that of real moths. As a population, however, none of the models was as successful as the moths. The best of the models had a success rate in tracking the plume of about 30%, compared to the average of 70% seen in the insects.

[1]  E. A. Arbas,et al.  Organization of goal-oriented locomotion: pheromone-modulated flight behavior of moths , 1993 .

[2]  W. J. Bell,et al.  Comprehensive Insect Physiology, Biochemistry and Pharmacology , 1985 .

[3]  H. Breer,et al.  Rapid kinetics of second messenger formation in olfactory transduction , 1990, Nature.

[4]  A. Ludlow,et al.  An analysis of anemotactic zigzagging flight in male moths stimulated by pheromone , 1978 .

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

[6]  Steven Vogel,et al.  How much air passes through a silkmoth's antenna? , 1983 .

[7]  A Cobas,et al.  Prey-catching and predator-avoidance in frog and toad: defining the schemas. , 1992, Journal of theoretical biology.

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

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

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

[11]  E. A. Arbas,et al.  Variability in odor-modulated flight by moths , 1998, Journal of Comparative Physiology A.

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

[13]  Randall Beer,et al.  Intelligence as Adaptive Behavior , 1990 .

[14]  T. Collett,et al.  Binocular, Directionally Selective Neurones, Possibly Involved in the Optomotor Response of Insects , 1966, Nature.

[15]  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.

[16]  F. Claire Rind The Role of an Identified Brain Neurone in Mediating Optomotor Movements in a Moth , 1983 .

[17]  Mark A. Willis,et al.  Adaptive Control of Odor-Guided Locomotion: Behavioral Flexibility as an Antidote to Environmental Unpredictability1 , 1996, Adapt. Behav..

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

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

[20]  Ring T. Cardé,et al.  Chemo-orientation in Flying Insects , 1984 .

[21]  T. Baker,et al.  Pheromone‐mediated optomotor anemotaxis and altitude control exhibited by male oriental fruit moths in the field , 1996 .

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

[23]  F. Claire Rind,et al.  A DIRECTIONALLY SENSITIVE MOTION DETECTING NEURONE IN THE BRAIN OF A MOTH , 1983 .

[24]  A. Kühn Die Orientierung der Tiere im Raum , 1919 .

[25]  T. J. Breen,et al.  Biostatistical Analysis (2nd ed.). , 1986 .

[26]  J. Murlis,et al.  Night flight towards a sex pheromone source by male Spodoptera littoralis (Boisd.) (Lepidoptera, Noctuidae) , 1977, Nature.

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

[28]  M. Arbib Levels of modeling of mechanisms of visually guided behavior , 1987, Behavioral and Brain Sciences.

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

[30]  Thomas C. Baker,et al.  The effects of unilateral antennectomy on the flight behaviour of male Heliothis virescens in a pheromone plume , 1991 .

[31]  Anthony Richard Ludlow,et al.  Applications of computer modelling to behavioural coordination , 1983 .

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