Behavioral and neurophysiological responses of an insect to changing ratios of constituents in host plant-derived volatile mixtures

Journal of Experimental Biology

Volumn 213, Issue 19, 2010, Pages 3388-3397

  Najar Rodriguez, A J ^a   Galizia, C G ^b   Stierle, J ^b   Dorn, S ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Antennal lobe; Behavior; Calcium imaging; Insect; Odor mixtures; Odor ratios; Olfaction; Olfactory glomeruli

Indexed keywords

BENZONITRILE; INSECT ATTRACTANTS; NITRILE; PHEROMONE; VOLATILE ORGANIC COMPOUND;

ANIMAL; ANIMAL BEHAVIOR; ANTENNA (ORGAN); ARTICLE; CHEMISTRY; DRUG EFFECT; FEMALE; HOST PARASITE INTERACTION; INNERVATION; MOTH; ODOR; PARASITOLOGY; PHYSIOLOGY; PLANT; PRUNUS; VOLATILIZATION;

ANIMALS; ARTHROPOD ANTENNAE; BEHAVIOR, ANIMAL; FEMALE; HOST-PARASITE INTERACTIONS; MOTHS; NITRILES; ODORS; PHEROMONES; PLANTS; PRUNUS; VOLATILE ORGANIC COMPOUNDS; VOLATILIZATION;

CYDIA; GRAPHOLITA; GRAPHOLITA MOLESTA; HEXAPODA; LEPIDOPTERA; PRUNUS PERSICA;

EID: 77956836802     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.046284     Document Type: Article

References (73)

1. Anton, S., Ouml Fstedt, C. and Hansson, B. (1997). Central nervous processing of sex pheromones in two strains of the European corn borer Ostrinia nubilalis (Lepidoptera: Pyralidae). J. Exp. Biol. 200, 1073-1087.
2. Anton, S., Dufour, M.-C. and Gadenne, C. (2007). Plasticity of olfactory-guided behaviour and its neurobiological basis: lessons from moths to locusts. Entomol. Exp. Appl. 123, 1-11.
3. Baldwin, I. T., Halitschke, R., Paschold, A., von Dahl, C. C. and Preston, C. A. (2006). Volatile signaling in plant-plant interactions: 'talking trees' in the genomics era. Science 311, 812-815.
4. Bazhenov, M., Stopfer, M., Sejnowski, T. J. and Laurent, G. (2005). Fast odor learning improves reliability of odor responses in the locust antennal lobe. Neuron 46, 1-10.
5. Bengtsson, M., Bäckman, A.-C., Liblikas, I., Ramirez, M. I., Borg-Karlson, A. K., Ansebo, L., Anderson, P., Löfqvist, J. and Witzgall, P. (2001). Plant odor analysis of apple:antennal response of codling moth females to apple volatiles during phenological development. J. Agric. Food Chem. 49. 3736-3741.
6. Bertschy, C., Turlings, T. C. J., Belloti, A. and Dorn, S. (1997). Chemically mediated attraction of three parasitoid species to mealy-bug infested cassava leaves. Florida Entomol. 80, 383-395.
7. Bichäo, H., Borg-Karlson, A. K., Araujo, J. and Mustaparta, H. (2003). Identification of plant odours activating receptor neurones in the weevil Pissodes notatus F. (Coleoptera: Curculionidae). J. Comp. Physiol. A 189, 203-212.
8. Birkett, M. A., Bruce, T. J. S., Martin, J. L., Oakley, J. and Wadhams, L. J. (2004). Responses of female orange wheat blossom midge, Sitodiplosis mosellana, to wheat panicle volatiles. J. Chem. Ecol. 30, 1319-1328.
9. Bruce, T. J. A., Wadhams, L. J. and Woodcock, C. M. (2005). Insect host location: a volatile situation. Trends Plant Sci. 10, 269-274.
10. Cardé, R. T. (1996). Odour plumes and odour-mediated flight in insects. Ciba Found.Symp. 200, 54-70.
11. Cardé,, R. T. and Minks, A. K. (1995). Control of moth pests by mating disruptions; successes and constrains. Annu. Rev. Entomol. 40, 559-585.
12. Cardé,, R. T. and Willis, M. (2008). Navigational strategies used by insects to find distant, wind-borne sources of odor. J. Chem. Ecol. 34, 854-866.
13. Carlsson, M. A., Chong, K. Y., Daniels, W., Hansson, B. S. and Pearce, T. C. (2007). Component information is preserved in glomerular responses to binary odour mixtures in the moth Spodoptera littoralis. Chem. Senses 32, 433-443.
14. Christensen, T. A., Mustaparta, H. and Hilderbrand, J. G. (1989). Discrimination of sex pheromone blends in the olfactory system of the moth. Chem. Senses 14, 463-477.
15. Christensen, T. A., Mustaparta, H. and Hildebrand, J. G. (1991). Chemical communication in Heliothine moths. 2: central processing of intraspecific and interspecific olfactory messages in the male corn-earworm moth Helicoverpa zea. J. Comp. Physiol. A 169, 259-274.
16. Christensen, T. A., Waldrop, B. R., Harrow, I. D. and Hildebrand, J. G. (1993). Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta. J. Comp. Physiol. A 173, 385-399.
17. D'Alessandro, M., Brunner, V., von Merey, G. and Turlings, T. C. J. (2009). Strong attraction of the parasitoid Cotesia marginiventris towards minor volatile compounds of maize. J. Chem. Ecol. 35, 999-1008.
18. De Moraes, C., Lewis, W., Pare, P., Alborn, H. and Tumlinson, J. (1998). Herbivoreinfested plants selectively attract parasitoids. Nat. Lett. 393, 570-572.
19. Dötterl, S., Wolfe, L. M. and Jürgens, A. (2005). Qualitative and quantitative analyses of flower scent in Silene latifolia. Phytochemistry 66, 203-213.
20. Galizia, C. G. and Menzel, R. (2001). The role of glomeruli in the neural representation of odours: results from optical recording studies. J. Insect Physiol. 47, 115-130.
21. Galizia, C. G. and Vetter, R. S. (2005). Optical methods for analyzing odour-evoked activity in the insect brain. In Methods in Insect Sensory Neuroscience (ed. T. A. Christensen), pp. 349-392. Boca Raton, FL: CRC Press.
22. Galizia, C. G., Sachse, S., Rappert, A. and Menzel, R. (1999). The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat. Neurosci. 2, 473-478.
23. Geffen, M. N., Broome, B. M., Laurent, G. and Meister, M. (2009). Neural encoding of rapidly fluctuating odors. Neuron 61, 570-586.
24. Gu, H. and Dorn, S. (2000). Genetic variation in behavioral response to herbivoreinfested plants in the parasitic wasp, Cotesia glomerata (L.) (Hymenoptera: Braconidae). J. Insect Behav. 13, 141-156.
25. Hughes, J. and Dorn, S. (2002). Sexual differences in the flight performance of the oriental fruit moth, Cydia molesta. Entomol. Exp. Appl. 103, 171-182.
26. Il'ichev, A. L., Williams, D. G. and Drago, A. (2003). Distribution of the oriental fruit moth Grapholita molesta Busck (Lep., Tortricidae) infestation on newly planted peaches before and during 2 years of mating disruption. J. Appl. Entomol. 127, 348-353.
27. Ivaldi-Sender, C. (1974). Techniques simple pour un élevage permanent de la tordeuse orientale, Grapholita molest (Busck) (Lepidoptera: Tortricidae), sur milieu artificiel. Ann. Zool. Ecol. Anim. 6, 337-343.
28. Jarriault, D., Gadenne, C., Rospars, J.-P. and Anton, S. (2009). Quantitative analysis of sex-pheromone coding in the antennal lobe of the moth Agrotis ipsilon: a tool to study network plasticity. J. Exp. Biol. 212, 1191-1201.
29. Johnson, C. B., Kazantis, A., Skoula, M., Mitteregger, U. and Novak, J. (2004). Seasonal, population and ontogenic variation in the volatile oil content and composition of individuals of Origanum vulgare subsp. hirtum, assesed by GC headspace analysis and by SPME sampling of individual oil glands. Phytochem. Anal. 15, 286-292.
30. Kaupp, U. B. (2010). Olfactory signalling in vertebrates and insects: differences and commonalities. Nature 11, 188-200.
31. Keil, S., Gu, H. and Dorn, S. (2001). Response of Cydia pomonella to selection on mobility: laboratory evaluation and field verification. Ecol. Entomol. 26, 495-501.
32. Laurent, G., Stopfer, M., Friedrich, R. W., Rabinovich, M. I., Volkovskii, A. and Abarbanel, H. D. I. (2001). Odor encodign as an active, dynamical process: experiments, computation and theory. Annu. Rev. Neurosci. 24, 263-297.
33. Le Berre, E., Béno, N., Ishii, A., Chabanet, C., Etiévant, P. and Thomas-Danguin, T. (2008). Just noticeable differences in component concentrations modify theodor quality of a blending mixture. Chem. Senses 33, 389-395.
34. Linn, C. E., Campbell, M. G. and Roelofs, W. L. (1988). Temperature modulation of behavioral thresholds controlling male moth sex pheromone response specificity. Physiol. Entomol. 13, 59-67.
35. Linn, C., Jr, Campbell, M. and Roelofs, W. (1991). The effects of different blend ratios and temperature on the active space of the oriental fruit moth sex pheromone. Physiol. Entomol. 16, 211-222.
36. Linster, C., Sachse, S. and Galizia, C. G. (2005). Computational modelling suggests that response properties rather than spatial position determine connectivity between olfactory glomeruli. J. Neurophysiol. 93, 3410-3417.
37. Löfstedt, C., Herrebout, W. M. and Menken, S. B. J. (1991). Sex pheromones and their potential role in the evolution of reproductive isolation in small ermine moth (Yponomeutidae). Chemoecology 2, 20-28.
38. Minks, A. K. and Card́, A. M. (1988). Disruption of pheromone communication in moths:is the natural blend really most efficacious? Entomol. Exp. Appl. 49, 25-36.
39. Murlis, J., Elkinton, J. S. and Cardé, R. T. (1992). Odor plumes and how insects usethem. Annu. Rev. Entomol. 37, 505-532.
40. Mustaparta, H. (2002). Encoding of plant odour information in insects: peripheral and central mechanisms. Entomol. Exp. Appl. 104, 1-13.
41. Natale, D., Mattiacci, L., Hern, A., Pasqualini, E. and Dorn, S. (2003). Response offemale Cydia molesta (Lepidoptera: Tortricidae) to plant derived volatiles. Bull. Entomol.Res. 93, 335-342.
42. Olsen, S. and Wilson, R. (2008). Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452, 956-960.
43. Olsen, S. R., Bhandawat, V. and Wilson, R. I. (2007). Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54, 89-103.
44. Pelz, D., Roeske, T., Syed, Z., de Bruyne, M. and Galizia, C. (2006). The molecular receptive range of an olfactory receptor in vivo (Drosophila melanogaster Or22a). J. Neurobiol. 66, 1544-1563.
45. Piñero, J. C. and Dorn, S. (2007). Synergism between aromatic compounds and green leaf volatiles derived from the host plant underlies female attraction in the oriental fruit moth. Entomol. Exp. Appl. 125, 185-194.
46. Piñero, J. C. and Dorn, S. (2009). Response of female oriental fruit moth to volatiles from apple and peach trees at three phenological stages. Entomol. Exp. Appl. 131,67-74.
47. Piñero, J. C., Galizia, C. G. and Dorn, S. (2008). Synergistic behavioural responses of female oriental fruit moths (Lepidoptera: Tortricidae) to synthetic host-plant derived mixtures are mirrored by odour-evoked calcium activity in their antennal lobes. J.Insect Physiol. 54, 333-343.
48. Reisenman, C. E., Heinbockel, T. and Hilderbrand, J. G. (2008). Inhibitory interactions among olfactory glomeruli do not necessarily reflect spatial proximity. J. Neurophysiol. 100, 554-564.
49. Riffel, J. A., Abrell, L. and Hildebrand, J. G. (2008). Physical processees and realtime chemical measurement of the insect olfactory environment. J. Chem. Ecol. 34, 837-853.
50. Riffel, J. A., Lei, H. and Hildebrand, J. G. (2009a). Neural correlates of behavior in the moth Manduca sexta in response to complex odors. Proc. Natl. Acad. Sci. USA 106, 19219-19226.
51. Riffel, J. A., Lei, H., Christensen, T. A. and Hildebrand, J. G. (2009b). Characterization and coding of behaviorally significant odor mixtures. Curr. Biol. 24, 335-340.
52. Rothschild, G. H. L. and Vickers, R. A. (1991). Biology, ecology and control of the oriental fruit moth. In World Crop Pests. Tortricid Pests: their Biology, Natural Enemies and Control, vol.5 (ed. L. van der Geest and H. Evenhuis), pp. 389-412. Amsterdam, The Netherlands: Elsevier.
53. Sachse, S. and Galizia, C. G. (2002). Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J. Neurophysiol. 87, 1106-1117.
54. Silbering, A. F. and Galizia, C. G. (2007). Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J. Neurosci. 27, 11966-11977.
55. Silbering, A. F., Okada, R., Ito, K. and Galizia, C. G. (2008). Olfactory information processing in the Drosophila antennal lobe: anything goes? J. Neurosci. 28, 13075-13087.
56. Silva, I. M., Eiras, A. E., Kline, D. L. and Bernier, U. R. (2005). Laboratory evaluation of mosquito traps baited with a synthetic human odor blend to capture Aedes aegypti. J. Am. Mosq. Control Assoc. 21, 229-233.
57. Skiri, H. T., Galizia, C. G. and Mustaparta, H. (2004). Representation of primary plant odorants in the antennal lobe of the moth Heliothis virescens using calcium imaging. Chem. Senses 29, 253-267.
58. Steullet, P., Krützfeldt, D. R., Hamidani, G., Flavus, T., Ngo, V. and Derby, C. D. (2002). Dual antennal chemosensory pathways mediate odor-associate learning and odor discrimination in the Caribbean spiny lobster Panulirus argus. J. Exp. Biol. 205, 851-867.
59. Takken, W., Dekker, T. and Wijnholds, Y. G. (1997). Odor-mediated flight behavior of Anopheles gambiae Giles sensu stricto and An. stephensi Liston in response to CO2, acetone, and 1-octenol-3-ol (Diptera: Culicidae). J. Insect Behav. 10, 395-407.
60. Tasin, M., Bäckman, A.-C., Bengtsson, M., Ioriatti, C. and Witzgall, P. (2006a).Essential host plant cues in the grapevine moth. Naturwissenschaften 93, 141-144.
61. Tasin, M., B̈ckman, A.-C., Bengtsson, M., Varela, N., Ioriatti, C. and Witzgall, P. (2006b). Wind tunnel attraction of grapevine moth females, Lobesia botrana, to natural and artificial grape odour. Chemoecology 16, 87-92.
62. Tasin, M., Bäckman, A.-C., Coracini, M., Casado, D., Ioriatti, C. and Witzgall, P. (2007). Synergism and redundancy in a plant volatile blend attracting grapevine moth females. Phytochemistry 68, 203-209.
63. Tasin, M., Bäckman, A.-C., Anfora, G., Carlin, S., Ioriatti, C. and Witzgall, P. (2010). Attraction of female grapevine moth to common and specific olfactory cues from 2 host plants. Chem. Senses 35, 57-64.
64. Vallat, A. and Dorn, S. (2005). Changes in volatile emissions from apple trees and associated response of adults female codling moths over the fruit-growing season. J. Agric.Food Chem. 53, 4083-4090.
65. Vallat, A., Gu, H. and Dorn, S. (2005). How rainfall, relative humidity and temperature influence volatile emissions from apple trees in situ. Phytochemistry 66, 1540-1550.
66. Verhoeven, K. J. F., Simonse, L. and McIntyre, L. M. (2005). Implementing false discovery rate control: increasing your power. Oikos 108, 643-647.
67. Vickers, N. J., Christensen, T. A. and Hildebrand, J. G. (1998). Combinatorial odor discrimination in the brain: attractive and antagonist odor blends are represented in distinct combinations of uniquely identifiable glomeruli. J. Comp. Neurol. 400, 35-56.
68. Visser, J. H. (1986). Host odour perception in phytophagous insects. Annu. Rev. Entomol. 31, 121-144.
69. Wang, Q., Gu, H. and Dorn, S. (2003). Selection on olfactory response to semiochemicals froma plant-host complex in a parasitic wasp. Heredity 91, 430-435.
70. Wang, Q., Gu, H. and Dorn, S. (2004). Genetic relationship between olfactory response and fitness in Cotesia glomerata L. Heredity 92, 579-584.
71. Webster, B., Bruce, T., Dufour, S., Birkemeyer, C., Birkett, M., Hardie, J. and Pickett, J. (2008). Identification of volatile compounds used in host location by the black bean aphid, Aphis fabae. J. Chem. Ecol. 34, 1153-1161.
72. Witzgall, P., Stelinski, L., Gut, L. and Thomson, D. (2008). Codling moth management and chemical ecology. Annu. Rev. Entomol. 53, 503-522.
73. Wright, G., Lutmerding, A., Dudareva, N. and Smith, B. H. (2005). Intensity and the ratios of compounds in the scent of snapdragon flowers affect scent discrimination by honeybees (Apis mellifera). J. Comp. Physiol. A 191, 105-114.