Changes in Odor Background Affect the Locomotory Response to Pheromone in Moths

Many animals rely on chemical cues to recognize and locate a resource, and they must extract the relevant information from a complex and changing odor environment. For example, in moths, finding a mate is mediated by a sex pheromone, which is detected in a rich environment of volatile plant compounds. Here, we investigated the effects of a volatile plant background on the walking response of male Spodoptera littoralis to the female pheromone. Males were stimulated by combining pheromone with one of three plant compounds, and their walking paths were recorded with a locomotion compensator and analyzed. We found that the addition of certain volatile plant compounds disturbed the orientation toward the sex pheromone. The effect on locomotion was correlated with the capacity of the plant compound to antagonize pheromone detection by olfactory receptor neurons, suggesting a masking effect of the background over the pheromone signal. Moths were more sensitive to changes in background compared to a constant background, suggesting that a background odor also acts as a distracting stimulus. Our experiments show that the effects of odorant background on insect responses to chemical signals are complex and cannot be explained by a single mechanism.

[1]  J. Kesselmeier,et al.  Biogenic Volatile Organic Compounds (VOC): An Overview on Emission, Physiology and Ecology , 1999 .

[2]  Christine Woodcock,et al.  Insect host location: a volatile situation. , 2005, Trends in plant science.

[3]  Á. Guerrero,et al.  Interactions of insect pheromones and plant semiochemicals. , 2004, Trends in plant science.

[4]  Mark A. Willis,et al.  The role of vision in odor-plume tracking by walking and flying insects , 2011, Journal of Experimental Biology.

[5]  B. Hansson,et al.  Function and morphology of the antennal lobe: new developments. , 2000, Annual review of entomology.

[6]  M. Renou,et al.  Plant terpenes affect intensity and temporal parameters of pheromone detection in a moth. , 2009, Chemical senses.

[7]  A. Blejec,et al.  A General Odorant Background Affects the Coding of Pheromone Stimulus Intermittency in Specialist Olfactory Receptor Neurones , 2011, PloS one.

[8]  C. Escera,et al.  The cognitive locus of distraction by acoustic novelty in the cross-modal oddball task , 2008, Cognition.

[9]  S. Berti Cognitive control after distraction: event-related brain potentials (ERPs) dissociate between different processes of attentional allocation. , 2008, Psychophysiology.

[10]  Zainulabeuddin Syed,et al.  Mosquitoes smell and avoid the insect repellent DEET , 2008, Proceedings of the National Academy of Sciences.

[11]  T. Phillips,et al.  Host plant influences on sex pheromone behavior of phytophagous insects. , 1997, Annual review of entomology.

[12]  S. Anton,et al.  Switching attraction to inhibition: mating-induced reversed role of sex pheromone in an insect , 2010, Journal of Experimental Biology.

[13]  C. Löfstedt,et al.  The odour makes the difference: male moths attracted by sex pheromones ignore the threat by predatory bats , 2004 .

[14]  Donald M. Wilkie,et al.  How rats process spatiotemporal information in the face of distraction , 2002, Behavioural Processes.

[15]  J. H. Tumlinson,et al.  Volatile Semiochemicals Released from Undamaged Cotton Leaves (A Systemic Response of Living Plants to Caterpillar Damage) , 1996, Plant physiology.

[16]  H. Jactel,et al.  Non-host volatiles mediate associational resistance to the pine processionary moth , 2011, Oecologia.

[17]  R. Barrozo,et al.  The response of the blood-sucking bug Triatoma infestans to carbon dioxide and other host odours. , 2004, Chemical senses.

[18]  J. Thorson,et al.  Insect Olfactory Sensilla: Structural, Chemical and Electrical Aspects of the Functional Organisation , 1980 .

[19]  F. Marion-Poll,et al.  Brief Exposure to Sensory Cues Elicits Stimulus-Nonspecific General Sensitization in an Insect , 2012, PloS one.

[20]  Listening in Pheromone Plumes: Disruption of Olfactory-Guided Mate Attraction in a Moth by a Bat-Like Ultrasound , 2007, Journal of insect science.

[21]  T. Baker,et al.  Host plant volatiles synergize responses of sex pheromone-specific olfactory receptor neurons in male Helicoverpa zea , 2002, Journal of Comparative Physiology A.

[22]  J. Byers,et al.  Avoidance of nonhost plants by a bark beetle, Pityogenes bidentatus, in a forest of odors , 2004, Naturwissenschaften.

[23]  John H. Loughrin,et al.  Diurnal cycle of emission of induced volatile terpenoids by herbivore-injured cotton plant. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Daniel T. Blumstein,et al.  Increased amplitude and duration of acoustic stimuli enhance distraction , 2010, Animal Behaviour.

[25]  R. W. Elwood,et al.  Factors Influencing Shell Investigation in the Hermit Crab, Pagurus bernhardus , 2010 .

[26]  Á. Guerrero,et al.  Behavioral responses ofSpodoptera littoralis males to sex pheromone components and virgin females in wind tunnel , 1996, Journal of Chemical Ecology.

[27]  M. Arx,et al.  Host plant volatiles serve to increase the response of male European grape berry moths, Eupoecilia ambiguella, to their sex pheromone , 2009, Journal of Comparative Physiology A.

[28]  K. Kaissling,et al.  Physiology of pheromone reception in insects (an example of moths) , 2004 .

[29]  Monika Hilker,et al.  The Relevance of Background Odor in Resource Location by Insects: A Behavioral Approach , 2008 .

[30]  Daniel T. Blumstein,et al.  Anthropogenic noise affects risk assessment and attention: the distracted prey hypothesis , 2010, Biology Letters.

[31]  L. Vosshall,et al.  Insect Odorant Receptors Are Molecular Targets of the Insect Repellent DEET , 2008, Science.

[32]  Masayuki Sakuma,et al.  Virtual reality experiments on a digital servosphere: guiding male silkworm moths to a virtual odour source , 2002 .

[33]  Frédéric Marion-Poll,et al.  Object-oriented approach to fast display of electrophysiological data under MS-Windows™ , 1995, Journal of Neuroscience Methods.

[34]  P. Anderson,et al.  Electrophysiological response to herbivore‐induced host plant volatiles in the moth Spodoptera littoralis , 1999 .

[35]  Bill S. Hansson,et al.  Physiology and morphology of pheromone-specific sensilla on the antennae of male and female Spodoptera littoralis (Lepidoptera: Noctuidae) , 1993 .

[36]  Natalia Dudareva,et al.  Regulation of Circadian Methyl Benzoate Emission in Diurnally and Nocturnally Emitting Plants , 2001, The Plant Cell Online.

[37]  Philippe Lucas,et al.  Ca2+ stabilizes the membrane potential of moth olfactory receptor neurons at rest and is essential for their fast repolarization. , 2007, Chemical senses.

[38]  Andrej Blejec Statistical method for detection of firing rate changes in spontaneously active neurons , 2005, Neurocomputing.

[39]  E. Pichersky,et al.  New Perspectives in Pollination Biology: Floral Fragrances. A day in the life of a linalool molecule: Chemical communication in a plant‐pollinator system. Part 1: Linalool biosynthesis in flowering plants , 1999 .

[40]  F. Zalom,et al.  Host-plant green-leaf volatiles synergize the synthetic sex pheromones of the corn earworm and codling moth (Lepidoptera) , 1993, CHEMOECOLOGY.

[41]  K. Kaissling Sensory Transduction in Insect Olfactory Receptors , 1974 .

[42]  M. Reichstein,et al.  Physiological and physicochemical controls on foliar volatile organic compound emissions. , 2004, Trends in plant science.

[43]  Jian-Yu Deng,et al.  Enhancement of Attraction to Sex Pheromones of Spodoptera exigua by Volatile Compounds Produced by Host Plants , 2004, Journal of Chemical Ecology.