Plasticity in Insect Olfaction: To Smell or Not to Smell?

Annual Review of Entomology

Volumn 61, Issue , 2016, Pages 317-333

  Gadenne, Christophe ^a   Barrozo, Romina B ^b   Anton, Sylvia ^a  

^a UNIVERSITÉ D'ANGERS   (France)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Antenna; Antennal lobe; Behavior; Hormones; Modulation; Odor

Indexed keywords

ANIMAL; CELL PLASTICITY; INSECT; NERVE CELL PLASTICITY; ODOR; PHYSIOLOGY; SMELLING;

ANIMALS; CELL PLASTICITY; INSECTS; NEURONAL PLASTICITY; OLFACTORY PERCEPTION; SMELL;

EID: 84961775191     PISSN: 00664170     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-ento-010715-023523     Document Type: Review

References (132)

1. Abrieux A, Debernard S, Maria A, Gaertner C, Anton S, et al. 2013. Involvement of the G-proteincoupled dopamine/ecdysteroid receptor DopEcR in the behavioral response to sex pheromone in an insect. PLOS ONE 8:e72785
2. Abrieux A, Duportets L, Debernard S, Gadenne C, Anton S. 2014. The GPCR membrane receptor, DopEcR, mediates the actions of both dopamine and ecdysone to control sex pheromone perception in an insect. Front. Behav. Neurosci. 8:312
3. Addesso KN, McAuslane HJ. 2009. Pepper weevil attraction to volatiles from host and nonhost plants. Environ. Entomol. 38:216-24
4. Anderson P, Anton S. 2014. Experience-based modulation of behavioural responses to plant volatiles and other sensory cues in insect herbivores. Plant Cell Environ. 37:1826-35
5. Anton S, Gadenne C. 1999. Effect of juvenile hormone on the central nervous processing of sex pheromone in an insect. PNAS 96:5764-67
6. Anton S, Homberg U. 1999. Antennal lobe structure. See Ref. 53, pp. 98-125
7. Arnold SEJ, Stevenson PC, Belmain SR. 2012. Odour-mediated orientation of beetles is influenced by age, sex and morph. PLOS ONE 7:e49071
8. Barron AB, Schulz DJ, Robinson GE. 2002. Octopamine modulates responsiveness to foraging-related stimuli in honey bees (Apis mellifera). J. Comp. Physiol. A 188:603-10
9. Barrozo RB, Gadenne C, Anton S. 2010. Switching attraction to inhibition: mating-induced reversed role of sex pheromone in an insect. J. Exp. Biol. 213:2933-39
10. Barrozo RB, Jarriault D, Deisig N, Gemeno C, Monsempes C, et al. 2011. Mating-induced differential coDing of plant odour and sex pheromone in a male moth. Eur. J. Neurosci. 33:1841-50
11. Barrozo RB, Jarriault D, Simeone X, Gaertner C, Gadenne C, Anton S. 2010. Mating-induced transient inhibition of responses to sex pheromone in a male moth is not mediated by octopamine or serotonin. J. Exp. Biol. 213:1100-6
12. Barrozo RB, LazzariC. 2004. The response of the blood-sucking bug Triatoma infestans to carbon dioxide and other host odours. Chem. Senses 29:319-29
13. Barrozo RB, Minoli SA, Lazzari CR. 2004. Circadian rhythm of behavioural responsiveness to carbon dioxide in the blood-sucking bug Triatoma infestans (Heteroptera: Reduviidae). J. Insect Physiol. 50:249-54
14. Bentley MD, Day JF. 1989. Chemical ecology and behavioral aspects of mosquito oviposition. Annu. Rev. Entomol. 34:401-21
15. Bigot L, Shaik HA, Bozzolan F, Party V, Lucas P, et al. 2012. Peripheral regulation by ecdysteroids of olfactory responsiveness in male Egyptian cotton leaf worms, Spodoptera littoralis. Insect Biochem. Mol. Biol. 42:22-31
16. Bodin A, Barrozo RB, Couton L, Lazzari CR. 2008. Temporal modulation and adaptive control of the behavioural response to odours in Rhodnius prolixus. J. Insect Physiol. 54:1343-48
17. Bodin A, Vinauger C, Lazzari CR. 2009. Behavioural and physiological state dependency of host seeking in the blood-sucking insect Rhodnius prolixus. J. Exp. Biol. 212:2386-93
18. Bodin A, Vinauger C, Lazzari CR. 2009. State-dependency of host-seeking in Rhodnius prolixus: the post-ecdysis time. J. Insect Physiol. 55:574-79
19. Bohbot JD, Durand NF, Vinyard BT,Dickens JC. 2013. Functional development of the octenol response in Aedes aegypti. Front. Physiol. 4:39
20. Bonizzoni M, Dunn WA, Campbell CL, Olson KE, Dimon MT, et al. 2011. RNA-seq analyses of blood-induced changes in gene expression in the mosquito vector species, Aedes aegypti. BMC Genomics 12:82
21. Brady J, Crump AJ. 1978. The control of circadian activity rhythms in tsetse flies: environment or physiological clock? Physiol. Entomol. 3:177-90
22. Brevault T, Quilici S. 2010. Flower and fruit volatiles assist host-plant location in the tomato fruit fly Neoceratitis cyanescens. Physiol. Entomol. 35:9-18
23. Brown MR, Klowden MJ, Crim JW, Young L, Shrouder LA, Lea AO. 1994. Endogenous regulation of mosquito host-seeking behavior by a neuropeptide. J. Insect Physiol. 40:399-406
24. Busto GUG, Cervantes-Sandoval II, Davis RLR. 2010. Olfactory learning in Drosophila. Annu. Rev. Physiol. 25:338-46
25. Castrovillo PJ, Cardé RT. 1979. Environmental regulation of female calling and male pheromone responsive periodicities in the codling moth (Laspeyresia pomonella). J. Insect Physiol. 25:659-67
26. Crnjar R, Yin CM, Stoffolano JG, Barbarossa IT, Liscia A, Angioy AM. 1990. Influence of age on the electroantennogram response of the female blowfly (Phormia regina). J. Insect Physiol. 36:917-21
27. Das S, Dimopoulos G. 2008. Molecular analysis of light pulse stimulated blood feeDing inhibition in Anopheles gambiae. Am. J. Trop. Med. Hyg. 79:333
28. Davis EE. 1984. Development of lactic acid-receptor sensitivity and host-seeking behaviour in newly emerged female Aedes aegypti mosquitoes. J. Insect Physiol. 30:211-15
29. Davis EE. 1984. Regulation of sensitivity in the peripheral chemoreceptor systems for host-seeking behaviour by a haemolymph-borne factor in Aedes aegypti. J. Insect Physiol. 30:179-83
30. de Belle JS, Kanzaki R. 1999. Protocerebral olfactory processing. See Ref. 53, pp. 243-81
31. De Cristofaro A, Ioriatti C, Pasqualini E. 2004. 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. Bull. Insectol. 57:137-44
32. Devaud JM, Acebes A, Ramaswami M, Ferrús A. 2003. Structural and functional changes in the olfactory pathway of adult Drosophila take place at a critical age. J. Neurobiol. 56:13-23
33. Domingue MJ, Roelofs WL, Linn CE, Baker TC. 2006. Effects of egg-to-adult development time and adult age on olfactory neuron response to semiochemicals in European corn borers. J. Insect Physiol. 52:975-83
34. Dukas R. 2008. Evolutionary biology of insect learning. Annu. Rev. Entomol. 53:145-60
35. Duportets L, Barrozo RB, Bozzolan F, Gaertner C, Anton S, et al. 2010. Cloning of an octopamine/tyramine receptor and plasticity of its expression as a function of adult sexual maturation in the male moth Agrotis ipsilon. Insect Mol. Biol. 19:489-99
36. Duportets L, Dufour MC, Couillaud F,Gadenne C. 1998. Biosynthetic activity of corpora allata, growth of sex accessory glands and mating in the male moth Agrotis ipsilon (Hufnagel). J. Exp. Biol. 201:2425-32
37. Duportets L, Maria A, Vitecek S, Gadenne C, Debernard S. 2013. Steroid hormone signaling is involved in the age-dependent behavioral response to sex pheromone in the adult male moth Agrotis ipsilon. Gen. Comp. Endocrinol. 186:58-66
38. Edgecomb RS, Harth CE, Schneiderman AM. 1994. Regulation of feeDing behavior in adult Drosophila melanogaster varies with feeDing regime and nutritional state. J. Exp. Biol. 197:215-35
39. Farhadian SF, Suarez-Farinas M, Cho CE, Pellegrino M, Vosshall LB. 2012. Post-fasting olfactory, transcriptional, and feeDing responses in Drosophila. Physiol. Behav. 105:544-53
40. Fernandez NM, Klowden MJ. 1995. Male accessory gland substances modify the host-seeking behavior of gravid Aedes aegypti mosquitoes. J. Insect Physiol. 41:965-70
41. Fletcher BS, Giannakakis A. 1973. Factors limiting the response of females of the Queensland fruit fly, Dacus tryoni, to the sex pheromone of the male. J. Insect Physiol. 19:1147-55
42. Fox AN, Pitts RJ, Robertson HM, Carlson JR, Zwiebel LJ. 2001. Candidate odorant receptors from the malaria vector mosquito Anopheles gambiae and evidence of down-regulation in response to blood feeding. PNAS 98:14693-97
43. Gadenne C, Anton S. 2000. Central processing of sex pheromone stimuli is differentially regulated by juvenile hormone in a male moth. J. Insect Physiol. 46:1195-206
44. Gadenne C, Dufour MC, Anton S. 2001. Transient post-mating inhibition of behavioural and central nervous responses to sex pheromone in an insect. Proc. R. Soc. B 268:1631-35
45. Gadenne C, Renou M, Sreng L. 1993. Hormonal control of sex pheromone responsiveness in the male black cutworm, Agrotis ipsilon. Experientia 49:721-24
46. Galizia CG, Szyszka P. 2008. Olfactory coDing in the insect brain: molecular receptive ranges, spatial and temporal coding. Entomol. Exp. Appl. 128:81-92
47. Grant AJ, O'Connell RJ. 2007. Age-related changes in female mosquito carbon dioxide detection. J. Med. Entomol. 44:617-23
48. Greiner B, Gadenne C, Anton S. 2002. Central processing of plant volatiles in Agrotis ipsilon males is age-independent in contrast to sex pheromone processing. Chem. Senses 27:45-48
49. Groh C, Ahrens D, Rössler W. 2006. Environment-and age-dependent plasticity of synaptic complexes in the mushroom bodies of honeybee queens. Brain Behav. Evol. 68:1-14
50. Groh C, Lu Z, Meinertzhagen IA, Rössler W. 2012. Age-related plasticity in the synaptic ultrastructure of neurons in the mushroom body calyx of the adult honeybee Apis mellifera. J. Comp. Neurol. 520:3509-27
51. Gronenberg W, Heeren S, Hölldobler B. 1996. Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus. J. Exp. Biol. 199:2011-19
52. Grotewiel MS, Martin I, Bhandari P, Cook-Wiens E. 2005. Functional senescence in Drosophila melanogaster. Ageing Res. Rev. 4:372-97
53. Hansson BS, ed. 1999. Insect Olfaction. Berlin: Springer
54. Hansson BS, ChristensenTA. 1999. Functional characteristics of the antennal lobe. See Ref. 53, pp. 126-64
55. Haynes KF, Birch MC. 1984. The periodicity of pheromone release and male responsiveness in the artichoke plume moth, Platyptilia carduidactyla. Physiol. Entomol. 9:287-95
56. Homberg U, Müller U. 1999. Neuroactive substances in the antennal lobe. See Ref. 53, pp. 181-207
57. Huetteroth W, Schachtner J. 2005. Standard three-dimensional glomeruli of the Manduca sexta antennal lobe: a tool to study developmental and adult neuronal plasticity. Cell Tissue Res. 319:513-24
58. Ignell R, Couillaud F, Anton S. 2001. Juvenile-hormone-mediated plasticity of aggregation behaviour and olfactory processing in adult desert locusts. J. Exp. Biol. 204:249-59
59. Jacquin-Joly E, Lucas P. 2005. Pheromone reception and transduction: mammals and insects illustrate converging mechanisms across phyla. Curr. Topics Neurochem. 4:75-105
60. Jang EB. 1995. Effects of mating and accessory gland injections on olfactory-mediated behavior in the female Mediterranean fruit fly, Ceratitis capitata. J. Insect Physiol. 41:705-10
61. Jang EB. 2002. Physiology of mating behavior in Mediterranean fruit fly (Diptera: Tephritidae): chemoreception and male accessory gland fluids in female post-mating behavior. Fla. Entomol. 85:89-93
62. Jarriault D, Barrozo RB, de Carvalho Pinto CJ, Greiner B, Dufour MC, et al. 2009. Age-dependent plasticity of sex pheromone response in the moth, Agrotis ipsilon: combined effects of octopamine and juvenile hormone. Horm. Behav. 56:185-91
63. Katsoyannos BI. 1982. Male sex pheromone of Rhagoletis cerasi L. (Diptera, Tephritidae): factors affecting release and response and its role in the mating behavior. Z. Angew. Entomol. 94:187-98
64. Keil TA. 1999. Morphology and development of the peripheral olfactory organs. See Ref. 53, pp. 5-48
65. Klowden MJ. 1990. The endogenous regulation of mosquito reproductive behavior. Experientia 46:660-70
66. Klowden MJ. 1997. Endocrine aspects ofmosquito reproduction. Arch. Insect Biochem. Physiol. 35:491-512
67. Klowden MJ. 2001. Sexual receptivity in Anopheles gambiae mosquitoes: absence of control by male accessory gland substances. J. Insect Physiol. 47:661-66
68. Klowden MJ, Blackmer JL. 1987. Humoral control of preoviposition behavior in the mosquito, Aedes aegypti. J. Insect Physiol. 33:689-92
69. Klowden MJ, Lea AO. 1979. Abdominal distention terminates subsequent host-seeking behaviour of Aedes aegypti following a blood meal. J. Insect Physiol. 25:583-85
70. Klowden MJ, Lea AO. 1979. Humoral inhibition of host-seeking in Aedes aegypti during oocyte maturation. J. Insect Physiol. 25:231-35
71. Krishnan B, Dryer SE, Hardin PE. 1999. Circadian rhythms in olfactory responses of Drosophila melanogaster. Nature 400:375-78
72. Kromann SH, Saveer AM, Binyameen M, BengtssonM, Birgersson G, et al. 2014. Concurrent modulation of neuronal and behavioural olfactory responses to sex and host plant cues in a male moth. Proc. R. Soc. B 282:20141884
73. Landolt PJ, Heath RR. 1988. Effects of age, mating, and time of day on behavioral-responses of female papaya fruit fly, Toxotrypana curvicauda Gerstaecker (Diptera, Tephritidae), to synthetic sex pheromone. Environ. Entomol. 17:47-51
74. Lange A, Orchard I, Barrett FM. 1989. Changes in hemolymph serotonin levels associated with feeDing in the bloodsucking bug, Rhodnius prolixus. J. Insect Physiol. 35:393-99
75. Latorre-Estivalis JM, Omondi BA, DeSouza O, Oliveira IHR, Ignell R, Lorenzo MG. 2015. Molecular basis of peripheral olfactory plasticity in Rhodnius prolixus, a Chagas disease vector. Front. Ecol. Evol. 3:74
76. Liang DS, Schal C. 1990. Circadian rhythmicity and development of the behavioral-response to sexpheromone in male brown-banded cockroaches, Supella longipalpa. Physiol. Entomol. 15:355-61
77. Lightle D, Ambrosino M, Lee JC. 2010. Sugar in moderation: Sugar diets affect short-term parasitoid behaviour. Physiol. Entomol. 35:179-85
78. Linn CE, Campbell MG, Poole KR, Wu W-Q, Roelofs WL. 1996. Effects of photoperiod on the circadian timing of pheromone response in male Trichoplusia ni: relationship to the modulatory action of octopamine. J. Insect Physiol. 42:881-91
79. Linn CE, Campbell MG, Roelofs WL. 1992. Photoperiod cues and the modulatory action of octopamine and 5-hydroxytryptamine on locomotor and pheromone in male gypsy moths, Lymantria dispar. Arch. Insect Biochem. Physiol. 20:265-84
80. Liu R, Lehane S, He X, Lehane M, Hertz-Fowler C, et al. 2010. Characterisations of odorant-binDing proteins in the tsetse fly Glossina morsitans morsitans. Cell. Mol. Life Sci. 67:919-29
81. LorenzoMG, LazzariCR. 1998. Activity pattern in relation to refuge exploitation and feeDing in Triatoma infestans (Hemiptera: Reduviidae). Acta Trop. 70:163-70
82. Luo S, Michaud JP, Li J, Liu X, Zhang Q. 2013. Odor learning in Microplitis mediator (Hymenoptera: Braconidae) is mediated by sugar type and physiological state. Biol. Control 65:207-11
83. Marinotti O, CalvoE,Nguyen QK,Dissanayake S, Ribeiro JMC,James AA. 2006. Genome-wide analysis of gene expression in adult Anopheles gambiae. Insect Mol. Biol. 15:1-12
84. Martel V, Anderson P, Hansson BS, Schlyter F. 2009. Peripheral modulation of olfaction by physiological state in the Egyptian leaf worm Spodoptera littoralis (Lepidoptera: Noctuidae). J. Insect Physiol. 55:793-97
85. Masante-Roca I, Anton S, Delbac L, Dufour M-C, Gadenne C. 2007. Attraction of the grapevine moth to host and non-host plant parts in the wind tunnel: effects of plant phenology, sex, and mating status. Entomol. Exp. Appl. 122:239-45
86. McQuillan HJ, Barron AB, Mercer AR. 2012. Age-and behaviour-related changes in the expression of biogenic amine receptor genes in the antennae of honey bees (Apis mellifera). J. Comp. Physiol. A 198:753-61
87. Mechaber WL, Capaldo CT, Hildebrand JG. 2002. Behavioral responses of adult female tobacco hornworms, Manduca sexta, to host plant volatiles change with age and mating status. J. Insect Sci. 2:5
88. Merlin C, Francois M-C, Queguiner I,Maibeche-CoisneM, Jacquin-Joly E. 2006. Evidence for a putative antennal clock in Mamestra brassicae: molecular cloning and characterization of two clock genes-period and cryptochrome-in antennae. Insect Mol. Biol. 15:137-45
89. Merlin C, Lucas P, Rochat D, François M, Mä?bèche-Coisne M, Jacquin-Joly E. 2007. An antennal circadian clock and circadian rhythms in peripheral pheromone reception in the moth Spodoptera littoralis. J. Biol. Rhythms 22:502-14
90. NaccaratiC, AudsleyN,Keen JN, Kim J-H, Howell GJ, et al. 2012. The host-seeking inhibitory peptide, Aea-HP-1, is made in the male accessory gland and transferred to the female during copulation. Peptides 34:150-57
91. Nässel DR. 1988. Serotonin and serotonin-immunoreactive neurons in the nervous system of insects. Prog. Neurobiol. 30:1-85
92. Niven JE, Laughlin SB. 2008. Energy limitation as a selective pressure on the evolution of sensory systems. J. Exp. Biol. 211:1792-804
93. Otter CJD, Tchikaya T, Schutte AM. 1991. Effects of age, sex and hunger on the antennal olfactory sensitivity of tsetse flies. Physiol. Entomol. 16:173-82
94. Page TL, Koelling E. 2003. Circadian rhythm in olfactory response in the antennae controlled by the optic lobe in the cockroach. J. Insect Physiol. 49:697-707
95. PayneTL, ShoreyHH,Gaston LK. 1970. Sex pheromones of noctuid moths: factors influencing antennal responsiveness in males of Trichoplusia ni. J. Insect Physiol. 16:1043-55
96. Pearson GA, Schal C. 1999. Electroantennogram responses of both sexes of grape root borer (Lepidoptera: Sesiidae) to synthetic female sex pheromone. Environ. Entomol. 28:943-46
97. Pham-Delegue MH, Trouiller J, Caillaud CM, Roger B, Masson C. 1993. Effect of queen pheromone on worker bees of different ages: behavioural and electrophysiological responses. Apidologie 24:267-81
98. Qiu YT, van Loon JJA, TakkenW,Meijerink J, Smid HM. 2006. Olfactory coDing in antennal neurons of the malaria mosquito, Anopheles gambiae. Chem. Senses 31:845-63
99. Randlkofer B, Obermaier E, Meiners T. 2007. Mother's choice of the oviposition site: balancing risk of egg parasitism and need of food supply for the progeny with an infochemical shelter? Chemoecology 17:177-86
100. Reddy GVP, Guerrero A. 2000. Behavioral responses of the diamondback moth, Plutella xylostella, to green leaf volatiles of Brassica oleracea subsp capitata. J. Agric. Food Chem. 48:6025-29
101. Reisenman CE. 2014. Hunger is the best spice: effects of starvation in the antennal responses of the blood-sucking bug Rhodnius prolixus. J. Insect Physiol. 71:8-13
102. ReisenmanCE, LeeY,Gregory T, Guerenstein PG. 2013. Effects of starvation on the olfactory responses of the blood-sucking bug Rhodnius prolixus. J. Insect Physiol. 59:717-21
103. Rinker DC, Pitts RJ, Zhou X, Suh E, Rokas A, et al. 2013. Blood meal-induced changes to antennal transcriptome profiles reveal shifts in odor sensitivities in Anopheles gambiae. PNAS 110:8260-65
104. Root CM, Ko KI, Jafari A, Wang JW. 2011. Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search. Cell 145:133-44
105. Rospars JP. 1988. Structure and development of the insect antennodeutocerebral system. Int. J. Insect Morphol. Embryol. 17:243-94
106. Rund SSC, Bonar NA, Champion MM, Ghazi JP, Houk CM, et al. 2013. Daily rhythms in antennal protein and olfactory sensitivity in the malaria mosquito Anopheles gambiae. Sci. Rep. 3:2494
107. Rund SSC, Gentile JE, Duffield GE. 2013. Extensive circadian and light regulation of the transcriptome in the malaria mosquito Anopheles gambiae. BMC Genomics 14:218
108. Rund SSC, Hou TY, Ward SM, Collins FH, Duffield GE. 2011. Genome-wide profiling of diel and circadian gene expression in the malaria vector Anopheles gambiae. PNAS 108:E421-30
109. Ruther J, Stahl LM, Steiner S, Garbe LA, Tolasch T. 2007. A male sex pheromone in a parasitic wasp and control of the behavioral response by the female's mating status. J. Exp. Biol. 210:2163-69
110. Saveer AM, Kromann SH, Birgersson G, BengtssonM, Lindblom T, et al. 2012. Floral to green: Mating switches moth olfactory coDing and preference. Proc. R. Soc. B 279:2314-22
111. Schuckel J, Siwicki KK, Stengl M. 2007. Putative circadian pacemaker cells in the antenna of the hawkmoth Manduca sexta. Cell Tissue Res. 330:271-78
112. Seabrook WD, Hirai K, Shorey HH, Gaston LK. 1979. Maturation and senescence of an insect chemosensory response. J. Chem. Ecol. 5:587-94
113. Seid MA, Traniello JFA. 2006. Age-related repertoire expansion and division of labor in Pheidole dentata (Hymenoptera: Formicidae): a new perspective on temporal polyethism and behavioral plasticity in ants. Behav. Ecol. Sociobiol. 60:631-44
114. Sengupta P. 2013. The belly rules the nose: feeDing state-dependent modulation of peripheral chemosensory responses. Curr. Opin. Neurobiol. 23:68-75
115. Shorey HH, Morin KL, Gaston LK. 1968. Sex pheromones of noctuid moths. XV. Timing of development of pheromone-responsiveness and other indicators of reproductive age in males of eight species. Ann. Entomol Soc. Am. 61:857-61
116. Siju KP, Hansson B, Ignell R. 2008. Immunocytochemical localization of serotonin in the central and peripheral chemosensory system of mosquitoes. Arthropod Struct. Dev. 37:248-59
117. Siju KP,Hill SR,Hansson BS, Ignell R. 2010. Influence of blood meal on the responsiveness of olfactory receptor neurons in antennal sensilla trichodea of the yellow fever mosquito, Aedes aegypti. J. Insect Physiol. 56:659-65
118. Silvegren G, Löfstedt C, Rosen WQ. 2005. Circadian mating activity and effect of pheromone preexposure on pheromone response rhythms in the moth Spodoptera littoralis. J. Insect Physiol. 51:277-86
119. TakkenW, van Loon J, Adam W. 2001. Inhibition of host-seeking response and olfactory responsiveness in Anopheles gambiae following blood feeding. J. Insect Physiol. 47:303-10
120. Tanoue S, Krishnan P, Krishnan B, Dryer SE, Hardin PE. 2004. Circadian clocks in antennal neurons are necessary and sufficient for olfaction rhythms in Drosophila. Curr. Biol. 14:638-49
121. Turgeon JJ, McNeil JN, Roelofs WL. 1983. Responsiveness of Pseudaletia unipuncta males to the female sex pheromone. Physiol. Entomol. 8:339-44
122. Van der Goes van Naters WM, Den Otter CJ, Maes FW. 1998. Olfactory sensitivity in tsetse flies: a daily rhythm. Chem. Senses 23:351-57
123. Vergoz V, McQuillanHJ, Geddes LH, Pullar K,Nicholson BJ, et al. 2009. Peripheralmodulation of worker bee responses to queen mandibular pheromone. PNAS 106:20930-35
124. Vitecek S, Maria A, Blais C, Duportets L, Gaertner C, et al. 2013. Is the rapid post-mating inhibition of pheromone response triggered by ecdysteroids or other factors from the sex accessory glands in the male moth Agrotis ipsilon? Horm. Behav. 63:700-8
125. Wang S, Zhang S, Sato K, Srinivasan MV. 2005. Maturation of odor representation in the honeybee antennal lobe. J. Insect Physiol. 51:1244-54
126. Warnes ML, Finlayson LH. 1986. Electroantennogram responses of the stable fly, Stomoxys calcitrans, to carbon dioxide and other odors. Physiol. Entomol. 11:469-73
127. Wilson RI, Mainen ZF. 2006. Early events in olfactory processing. Annu. Rev. Neurosci. 29:163-201
128. Winnington AP, Napper RM, Mercer AR. 1996. Structural plasticity of identified glomeruli in the antennal lobes of the adult worker honey bee. J. Comp. Neurol. 365:479-90
129. Worster AS, Seabrook WD. 1989. Electrophysiological investigation of diel variations in the antennal sensitivity of the male spruce budworm moth Choristoneura fumiferana (Lepidoptera: Tortricidae). J. Insect Physiol. 35:1-5
130. Wyatt TD. 2014. Pheromones and Animal Behavior. Cambridge, UK: Cambridge Univ. Press
131. Yeh C, Klowden MJ. 1990. Effects of male accessory gland substances on the pre-oviposition behaviour of Aedes aegypti mosquitoes. J. Insect Physiol. 36:799-803
132. ZhukovskayaMI. 1995. Circadian rhythm of sex pheromone perception in themale American cockroach, Periplaneta americana L. J. Insect Physiol. 41:941-46