Coding and interaction of sex pheromone and plant volatile signals in the antennal lobe of the codling moth Cydia pomonella

SUMMARY In the codling moth Cydia pomonella (Lepidoptera: Tortricidae) plant volatiles attract males and females by upwind flight and synergise the male response to the female-produced sex pheromone, indicating a close relationship between the perception of social and environmental olfactory signals. We have studied the anatomical and functional organisation of the antennal lobe (AL), the primary olfactory centre, of C. pomonella with respect to the integration of sex pheromone and host-plant volatile information. A three-dimensional reconstruction of the glomerular structure of the AL revealed 50±2 and 49±2 glomeruli in males and females, respectively. These glomeruli are functional units involved in the coding of odour quality. The glomerular map of the AL was then integrated with electrophysiological recordings of the response of individual neurons in the AL of males and females to sex pheromone components and behaviourally active plant volatiles. By means of intracellular recordings and stainings, we physiologically characterised ca. 50 neurons in each sex, revealing complex patterns of activation and a wide variation in response dynamics to these test compounds. Stimulation with single chemicals and their two-component blends produced both synergistic and inhibitory interactions in projection neurons innervating ordinary glomeruli and the macroglomerular complex. Our results show that the sex pheromone and plant odours are processed in an across-fibre coding pattern. The lack of a clear segregation between the pheromone and general odour subsystems in the AL of the codling moth suggests a level of interaction that has not been reported from other insects.

[1]  C. Ioriatti,et al.  Flight tunnel response of codling moth Cydia pomonella to blends of codlemone, codlemone antagonists and pear ester , 2010 .

[2]  Philipp Kirsch,et al.  Sex Pheromones and Their Impact on Pest Management , 2010, Journal of Chemical Ecology.

[3]  Patrick W. Weddle,et al.  History of IPM in California pears--50 years of pesticide use and the transition to biologically intensive IPM. , 2009, Pest management science.

[4]  J. Rospars,et al.  Three-dimensional antennal lobe atlas of the oriental fruit moth, Cydia molesta (Busck) (Lepidoptera: Tortricidae): comparison of male and female glomerular organization , 2009, Cell and Tissue Research.

[5]  Jeffrey A. Riffell,et al.  Characterization and Coding of Behaviorally Significant Odor Mixtures , 2009, Current Biology.

[6]  B. Hansson,et al.  Reversed functional topology in the antennal lobe of the male European corn borer , 2008, Journal of Experimental Biology.

[7]  N. Vickers,et al.  Central Processing of Natural Odor Mixtures in Insects , 2008, Journal of Chemical Ecology.

[8]  T. Baker,et al.  Odor Detection in Insects: Volatile Codes , 2008, Journal of Chemical Ecology.

[9]  R. Kanzaki,et al.  Representation of a mixture of pheromone and host plant odor by antennal lobe projection neurons of the silkmoth Bombyx mori , 2008, Journal of Comparative Physiology A.

[10]  G. Galizia,et al.  Synergistic behavioral responses of female oriental fruit moths (Lepidoptera:Tortricidae) to synthetic host plant-derived mixtures are mirrored by odor-evoked calcium activity in their antennal lobes. , 2008, Journal of insect physiology.

[11]  D. Suckling,et al.  Positive Interaction of a Feeding Attractant and a Host Kairomone for Trapping the Codling Moth, Cydia pomonella (L.) , 2007, Journal of Chemical Ecology.

[12]  T. Pearce,et al.  Component information is preserved in glomerular responses to binary odor mixtures in the moth Spodoptera littoralis. , 2007, Chemical senses.

[13]  C. Ioriatti,et al.  Essential host plant cues in the grapevine moth , 2006, Naturwissenschaften.

[14]  N. Vickers,et al.  Physiology and glomerular projections of olfactory receptor neurons on the antenna of female Heliothis virescens (Lepidoptera: Noctuidae) responsive to behaviorally relevant odors , 2006, Journal of Comparative Physiology A.

[15]  B. Hansson,et al.  Neuronal architecture of the mosquito deutocerebrum , 2005, The Journal of comparative neurology.

[16]  B. Hansson,et al.  Responses to sex pheromone and plant odours by olfactory receptor neurons housed in sensilla auricillica of the codling moth, Cydia pomonella (Lepidoptera: Tortricidae). , 2005, Journal of insect physiology.

[17]  Barry J. Dickson,et al.  Molecular, Anatomical, and Functional Organization of the Drosophila Olfactory System , 2005, Current Biology.

[18]  A. Knight,et al.  Monitoring Codling Moth (Lepidoptera: Tortricidae) in Apple with Blends of Ethyl (E, Z)-2,4-Decadienoate and Codlemone , 2005 .

[19]  Sylvia Anton,et al.  Three-dimensional antennal lobe atlas of male and female moths, Lobesia botrana (Lepidoptera: Tortricidae) and glomerular representation of plant volatiles in females , 2005, Journal of Experimental Biology.

[20]  John G Hildebrand,et al.  Spatial and Temporal Organization of Ensemble Representations for Different Odor Classes in the Moth Antennal Lobe , 2004, The Journal of Neuroscience.

[21]  A. Borg-Karlson,et al.  Antennal and behavioural response of codling moth Cydia pomonella to plant volatiles , 2004 .

[22]  Birgit Greiner,et al.  Three‐dimensional antennal lobe atlas of the male moth, Agrotis ipsilon: A tool to study structure–function correlation , 2004, The Journal of comparative neurology.

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

[24]  M. Bengtsson,et al.  Host Plant Volatiles Synergize Response to Sex Pheromone in Codling Moth, Cydia pomonella , 2004, Journal of Chemical Ecology.

[25]  S. Dorn,et al.  A female-specific attractant for the codling moth, Cydia pomonella, from apple fruit volatiles , 2004, Naturwissenschaften.

[26]  M. Coracini,et al.  Attraction of codling moth males to apple volatiles , 2004 .

[27]  M. Carlsson,et al.  Olfactory activation patterns in the antennal lobe of the sphinx moth, Manduca sexta , 2003, Journal of Comparative Physiology A.

[28]  J. Hildebrand,et al.  Pheromonal and host-odor processing in the insect antennal lobe: how different? , 2002, Current Opinion in Neurobiology.

[29]  H. Mustaparta.  Encoding of plant odour information in insects: peripheral and central mechanisms , 2002 .

[30]  M. M. Sadek,et al.  Glomerular representation of plant volatiles and sex pheromone components in the antennal lobe of the female Spodoptera littoralis. , 2002, The Journal of experimental biology.

[31]  C Giovanni Galizia,et al.  Digital atlases of the antennal lobe in two species of tobacco budworm moths, the oriental Helicoverpa assulta (male) and the American Heliothis virescens (male and female) , 2002, The Journal of comparative neurology.

[32]  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.

[33]  C. Galizia,et al.  Spatial representation of odours in the antennal lobe of the moth Spodoptera littoralis (Lepidoptera: Noctuidae). , 2002, Chemical senses.

[34]  P. Anderson,et al.  Identification of further sex pheromone synergists in the codling moth, Cydia pomonella , 2001 .

[35]  A. Knight,et al.  Attractants from Bartlett pear for codling moth, Cydia pomonella (L.), larvae , 2001, Naturwissenschaften.

[36]  B. Campbell,et al.  A pear-derived kairomone with pheromonal potency that attracts male and female codling moth, Cydia pomonella (L.) , 2001, Naturwissenschaften.

[37]  A. Borg-Karlson,et al.  Plant odor analysis of apple: antennal response of codling moth females to apple volatiles during phenological development. , 2001, Journal of agricultural and food chemistry.

[38]  P. Anderson,et al.  Antennal response of codling moth males, Cydia pomonella L. (Lepidoptera: Tortricidae), to the geometric isomers of codlemone and codlemone acetate , 2000, Journal of Comparative Physiology A.

[39]  J. Rospars,et al.  Sexually dimorphic and isomorphic glomeruli in the antennal lobes of the sphinx moth Manduca sexta. , 2000, Chemical senses.

[40]  John G. Hildebrand,et al.  Response Characteristics of an Identified, Sexually Dimorphic Olfactory Glomerulus , 2000, The Journal of Neuroscience.

[41]  B. Hansson,et al.  Physiological mismatching between neurons innervating olfactory glomeruli in a moth , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[42]  S. Dorn,et al.  Sexual dimorphism in the olfactory orientation of adult Cydia pomonella in response to α‐farnesene , 1999 .

[43]  U. Koch,et al.  Behavioral observations of codling moth, Cydia pomonella, in orchards permeated with synthetic pheromone , 1999, BioControl.

[44]  N. Vickers,et al.  Combinatorial odor discrimination in the brain: Attractive and antagonist odor blends are represented in distinct combinations of uniquely identifiable glomeruli , 1998, The Journal of comparative neurology.

[45]  S. Schulz,et al.  Autodetection and chemistry of female and male pheromone in both sexes of the tiger moth Panaxia quadripunctaria , 1998, Journal of Comparative Physiology A.

[46]  R. Menzel,et al.  Representations of odours and odour mixtures visualized in the honeybee brain , 1997, Nature.

[47]  M. Bengtsson,et al.  Pheromone Release by Individual Females of Codling Moth, Cydia pomonella , 1997, Journal of Chemical Ecology.

[48]  C. Löfstedt,et al.  Discrimination among pheromone component blends by interneurons in male antennal lobes of two populations of the turnip moth, Agrotis segetum. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[49]  C. Löfstedt,et al.  Sex pheromones and attractants in the Eucosmini and Grapholitini (Lepidoptera, Tortricidae) , 1996, CHEMOECOLOGY.

[50]  C. J. Otter,et al.  Electrophysiological and behavioural responses of chestnut moths, Cydia fagiglandana and C. splendana (Lep., Tortricidae), to sex attractants and odours of host plants , 1996 .

[51]  B. Hansson,et al.  Chemical communication in heliothine moths , 1995, Journal of Comparative Physiology A.

[52]  B. Hansson,et al.  Sex pheromone and plant-associated odour processing in antennal lobe interneurons of male Spodoptera littoralis (Lepidoptera: Noctuidae) , 1995, Journal of Comparative Physiology A.

[53]  B. Hansson,et al.  Antennal lobe projection patterns of olfactory receptor neurons involved in sex pheromone detection in Spodoptera littoralis (Lepidoptera: Noctuidae). , 1995, Tissue & cell.

[54]  B. Hansson,et al.  Central processing of sex pheromone, host odour, and oviposition deterrent information by interneurons in the antennal lobe of female Spodoptera littoralis (Lepidoptera: Noctuidae) , 1994, The Journal of comparative neurology.

[55]  T. Christensen,et al.  Structure and function of antennal lobe neurons in the male turnip moth, Agrotis segetum (Lepidoptera: Noctuidae) , 1994, Journal of Comparative Physiology A.

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

[57]  J. Rospars,et al.  Anatomical identification of glomeruli in the antennal lobes of the male sphinx moth Manduca sexta , 1992, Cell and Tissue Research.

[58]  C. Löfstedt,et al.  Functional specialization of olfactory glomeruli in a moth. , 1992, Science.

[59]  J. Hildebrand,et al.  Functionally distinct subdivisions of the macroglomerular complex in the antennal lobe of the male sphinx moth Manduca sexta , 1991, The Journal of comparative neurology.

[60]  E. A. Arbas,et al.  Physiology and morphology of projection neurons in the antennal lobe of the male mothManduca sexta , 1989, Journal of Comparative Physiology A.

[61]  B. Hansson,et al.  Comparison of male and female olfactory cell response to pheromone compounds and plant volatiles in the turnip moth, Agrotis segetum , 1989 .

[62]  D. Schneider,et al.  Sexual dimorphism in neuronal projections from the antennae of silk moths (Bombyx mori, Antheraea polyphemus) and the gypsy moth (Lymantria dispar) , 1987, Cell and Tissue Research.

[63]  John G. Hildebrand,et al.  Male-specific, sex pheromone-selective projection neurons in the antennal lobes of the mothManduca sexta , 1987, Journal of Comparative Physiology A.

[64]  J. Hildebrand,et al.  An accessory olfactory pathway in Lepidoptera: the labial pit organ and its central projections in Manduca sexta and certain other sphinx moths and silk moths , 1986, Cell and Tissue Research.

[65]  C. Wearing,et al.  α-Farnesene, a naturally occurring oviposition stimulant for the codling moth, Laspeyresia pomonella , 1973 .

[66]  W. Roelofs,et al.  Sex Attractant of the Codling Moth: Characterization with Electroantennogram Technique , 1971, Science.

[67]  C Giovanni Galizia,et al.  Parallel olfactory systems in insects: anatomy and function. , 2010, Annual review of entomology.

[68]  L. Gut,et al.  Codling moth management and chemical ecology. , 2008, Annual review of entomology.

[69]  Bill S. Hansson,et al.  Insect olfactory neuroethology – An electrophysiological perspective , 2004 .

[70]  G. Anfora,et al.  Electrophysiological responses of Cydia pomonella to codlemone and pear ester ethyl (E,Z)-2,4-decadienoate: peripheral interactions in their perception and evidences for cells responding to both compounds , 2004 .

[71]  M. Raccurt,et al.  Immunocytochemical localization of S-100 protein in stellate cells (folliculo-stellate cells) of the adenohypophysis in the monkeys Macaca irus and Cercopithecus aethiops , 2004, Cell and Tissue Research.

[72]  J. Hildebrand,et al.  GABA-mediated synaptic inhibition of projection neurons in the antennal lobes of the sphinx moth,Manduca sexta , 2004, Journal of Comparative Physiology A.

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