Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

In insects, olfaction plays a crucial role in many behavioral contexts, such as locating food, sexual partners, and oviposition sites. To successfully perform such behaviors, insects must respond to chemical stimuli at the right moment. Insects modulate their olfactory system according to their physiological state upon interaction with their environment. Here, we review the plasticity of behavioral responses to different odor types according to age, feeding state, circadian rhythm, and mating status. We also summarize what is known about the underlying neural and endocrinological mechanisms, from peripheral detection to central nervous integration, and cover neuromodulation from the molecular to the behavioral level. We describe forms of olfactory plasticity that have contributed to the evolutionary success of insects and have provided them with remarkable tools to adapt to their ever-changing environment. © Copyright 2016 by Annual Reviews. All rights reserved.

Registro:

Documento: Artículo
Título:Plasticity in Insect Olfaction: To Smell or Not to Smell?
Autor:Gadenne, C.; Barrozo, R.B.; Anton, S.
Filiación:Neuroéthologie-RCIM, INRA-Université d'Angers, UPRES EA 2647 USC INRA 1330, Beaucouzé Cedex, 49071, France
Laboratorio de Fisiología de Insectos, DBBE, FCEyN, Universidad de Buenos Aires, IBBEA, CONICET-UBA, Ciudad Universitaria, C1428EHA, Buenos Aires, Argentina
Palabras clave:Antenna; Antennal lobe; Behavior; Hormones; Modulation; Odor; animal; cell plasticity; insect; nerve cell plasticity; odor; physiology; smelling; Animals; Cell Plasticity; Insects; Neuronal Plasticity; Olfactory Perception; Smell
Año:2016
Volumen:61
Página de inicio:317
Página de fin:333
DOI: http://dx.doi.org/10.1146/annurev-ento-010715-023523
Título revista:Annual Review of Entomology
Título revista abreviado:Ann. Rev. Entomol.
ISSN:00664170
CODEN:ARENA
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00664170_v61_n_p317_Gadenne

Referencias:

  • Abrieux, A., Debernard, S., Maria, A., Gaertner, C., Anton, S., Involvement of the G-proteincoupled dopamine/ecdysteroid receptor DopEcR in the behavioral response to sex pheromone in an insect (2013) PLOS ONE, 8, p. e72785
  • Abrieux, A., Duportets, L., Debernard, S., Gadenne, C., Anton, S., The GPCR membrane receptor, DopEcR, mediates the actions of both dopamine and ecdysone to control sex pheromone perception in an insect (2014) Front. Behav. Neurosci., 8, p. 312
  • Addesso, K.N., McAuslane, H.J., Pepper weevil attraction to volatiles from host and nonhost plants (2009) Environ. Entomol., 38, pp. 216-224
  • Anderson, P., Anton, S., Experience-based modulation of behavioural responses to plant volatiles and other sensory cues in insect herbivores (2014) Plant Cell Environ., 37, pp. 1826-1835
  • Anton, S., Gadenne, C., Effect of juvenile hormone on the central nervous processing of sex pheromone in an insect (1999) PNAS, 96, pp. 5764-5767
  • Anton, S., Homberg, U., Antennal lobe structure (1999) See Ref., 53, pp. 98-125
  • Arnold, S.E.J., Stevenson, P.C., Belmain, S.R., Odour-mediated orientation of beetles is influenced by age, sex and morph (2012) PLOS ONE, 7, p. e49071
  • Barron, A.B., Schulz, D.J., Robinson, G.E., Octopamine modulates responsiveness to foraging-related stimuli in honey bees (Apis mellifera) (2002) J. Comp. Physiol. A, 188, pp. 603-610
  • Barrozo, R.B., Gadenne, C., Anton, S., Switching attraction to inhibition: Mating-induced reversed role of sex pheromone in an insect (2010) J. Exp. Biol., 213, pp. 2933-2939
  • Barrozo, R.B., Jarriault, D., Deisig, N., Gemeno, C., Monsempes, C., Mating-induced differential coDing of plant odour and sex pheromone in a male moth (2011) Eur. J. Neurosci., 33, pp. 1841-1850
  • Barrozo, R.B., Jarriault, D., Simeone, X., Gaertner, C., Gadenne, C., Anton, S., Mating-induced transient inhibition of responses to sex pheromone in a male moth is not mediated by octopamine or serotonin (2010) J. Exp. Biol., 213, pp. 1100-1106
  • Barrozo, R.B., Lazzari, C., The response of the blood-sucking bug Triatoma infestans to carbon dioxide and other host odours (2004) Chem. Senses, 29, pp. 319-329
  • Barrozo, R.B., Minoli, S.A., Lazzari, C.R., Circadian rhythm of behavioural responsiveness to carbon dioxide in the blood-sucking bug Triatoma infestans (Heteroptera: Reduviidae) (2004) J. Insect Physiol., 50, pp. 249-254
  • Bentley, M.D., Day, J.F., Chemical ecology and behavioral aspects of mosquito oviposition (1989) Annu. Rev. Entomol., 34, pp. 401-421
  • Bigot, L., Shaik, H.A., Bozzolan, F., Party, V., Lucas, P., Peripheral regulation by ecdysteroids of olfactory responsiveness in male Egyptian cotton leaf worms, Spodoptera littoralis (2012) Insect Biochem. Mol. Biol., 42, pp. 22-31
  • Bodin, A., Barrozo, R.B., Couton, L., Lazzari, C.R., Temporal modulation and adaptive control of the behavioural response to odours in Rhodnius prolixus (2008) J. Insect Physiol., 54, pp. 1343-1348
  • Bodin, A., Vinauger, C., Lazzari, C.R., Behavioural and physiological state dependency of host seeking in the blood-sucking insect Rhodnius prolixus (2009) J. Exp. Biol., 212, pp. 2386-2393
  • Bodin, A., Vinauger, C., Lazzari, C.R., State-dependency of host-seeking in Rhodnius prolixus: The post-ecdysis time (2009) J. Insect Physiol., 55, pp. 574-579
  • Bohbot, J.D., Durand, N.F., Vinyard, B.T., Dickens, J.C., Functional development of the octenol response in Aedes aegypti (2013) Front. Physiol., 4, p. 39
  • Bonizzoni, M., Dunn, W.A., Campbell, C.L., Olson, K.E., Dimon, M.T., RNA-seq analyses of blood-induced changes in gene expression in the mosquito vector species, Aedes aegypti (2011) BMC Genomics, 12, p. 82
  • Brady, J., Crump, A.J., The control of circadian activity rhythms in tsetse flies: Environment or physiological clock? (1978) Physiol. Entomol., 3, pp. 177-190
  • Brevault, T., Quilici, S., Flower and fruit volatiles assist host-plant location in the tomato fruit fly Neoceratitis cyanescens (2010) Physiol. Entomol., 35, pp. 9-18
  • Brown, M.R., Klowden, M.J., Crim, J.W., Young, L., Shrouder, L.A., Lea, A.O., Endogenous regulation of mosquito host-seeking behavior by a neuropeptide (1994) J. Insect Physiol., 40, pp. 399-406
  • Busto, G.U.G., Cervantes-Sandoval, I.I., Davis, R.L.R., Olfactory learning in Drosophila (2010) Annu. Rev. Physiol., 25, pp. 338-346
  • Castrovillo, P.J., Cardé, R.T., Environmental regulation of female calling and male pheromone responsive periodicities in the codling moth (Laspeyresia pomonella) (1979) J. Insect Physiol., 25, pp. 659-667
  • Crnjar, R., Yin, C.M., Stoffolano, J.G., Barbarossa, I.T., Liscia, A., Angioy, A.M., Influence of age on the electroantennogram response of the female blowfly (Phormia regina) (1990) J. Insect Physiol., 36, pp. 917-921
  • Das, S., Dimopoulos, G., Molecular analysis of light pulse stimulated blood feeDing inhibition in Anopheles gambiae (2008) Am. J. Trop. Med. Hyg., 79, p. 333
  • Davis, E.E., Development of lactic acid-receptor sensitivity and host-seeking behaviour in newly emerged female Aedes aegypti mosquitoes (1984) J. Insect Physiol., 30, pp. 211-215
  • Davis, E.E., Regulation of sensitivity in the peripheral chemoreceptor systems for host-seeking behaviour by a haemolymph-borne factor in Aedes aegypti (1984) J. Insect Physiol., 30, pp. 179-183
  • De Belle, J.S., Kanzaki, R., Protocerebral olfactory processing (1999) See Ref., 53, pp. 243-281
  • De Cristofaro, A., Ioriatti, C., Pasqualini, E., 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) Bull. Insectol., 57, pp. 137-144
  • Devaud, J.M., Acebes, A., Ramaswami, M., Ferrús, A., Structural and functional changes in the olfactory pathway of adult Drosophila take place at a critical age (2003) J. Neurobiol., 56, pp. 13-23
  • Domingue, M.J., Roelofs, W.L., Linn, C.E., Baker, T.C., Effects of egg-to-adult development time and adult age on olfactory neuron response to semiochemicals in European corn borers (2006) J. Insect Physiol., 52, pp. 975-983
  • Dukas, R., Evolutionary biology of insect learning (2008) Annu. Rev. Entomol., 53, pp. 145-160
  • Duportets, L., Barrozo, R.B., Bozzolan, F., Gaertner, C., Anton, S., Cloning of an octopamine/tyramine receptor and plasticity of its expression as a function of adult sexual maturation in the male moth Agrotis ipsilon (2010) Insect Mol. Biol., 19, pp. 489-499
  • Duportets, L., Dufour, M.C., Couillaud, F., Gadenne, C., Biosynthetic activity of corpora allata, growth of sex accessory glands and mating in the male moth Agrotis ipsilon (Hufnagel) (1998) J. Exp. Biol., 201, pp. 2425-2432
  • Duportets, L., Maria, A., Vitecek, S., Gadenne, C., Debernard, S., Steroid hormone signaling is involved in the age-dependent behavioral response to sex pheromone in the adult male moth Agrotis ipsilon (2013) Gen. Comp. Endocrinol., 186, pp. 58-66
  • Edgecomb, R.S., Harth, C.E., Schneiderman, A.M., Regulation of feeDing behavior in adult Drosophila melanogaster varies with feeDing regime and nutritional state (1994) J. Exp. Biol., 197, pp. 215-235
  • Farhadian, S.F., Suarez-Farinas, M., Cho, C.E., Pellegrino, M., Vosshall, L.B., Post-fasting olfactory, transcriptional, and feeDing responses in Drosophila (2012) Physiol. Behav., 105, pp. 544-553
  • Fernandez, N.M., Klowden, M.J., Male accessory gland substances modify the host-seeking behavior of gravid Aedes aegypti mosquitoes (1995) J. Insect Physiol., 41, pp. 965-970
  • Fletcher, B.S., Giannakakis, A., Factors limiting the response of females of the Queensland fruit fly, Dacus tryoni, to the sex pheromone of the male (1973) J. Insect Physiol., 19, pp. 1147-1155
  • Fox, A.N., Pitts, R.J., Robertson, H.M., Carlson, J.R., Zwiebel, L.J., Candidate odorant receptors from the malaria vector mosquito Anopheles gambiae and evidence of down-regulation in response to blood feeding (2001) PNAS, 98, pp. 14693-14697
  • Gadenne, C., Anton, S., Central processing of sex pheromone stimuli is differentially regulated by juvenile hormone in a male moth (2000) J. Insect Physiol., 46, pp. 1195-1206
  • Gadenne, C., Dufour, M.C., Anton, S., Transient post-mating inhibition of behavioural and central nervous responses to sex pheromone in an insect (2001) Proc. R. Soc. B, 268, pp. 1631-1635
  • Gadenne, C., Renou, M., Sreng, L., Hormonal control of sex pheromone responsiveness in the male black cutworm, Agrotis ipsilon (1993) Experientia, 49, pp. 721-724
  • Galizia, C.G., Szyszka, P., Olfactory coDing in the insect brain: Molecular receptive ranges, spatial and temporal coding (2008) Entomol. Exp. Appl., 128, pp. 81-92
  • Grant, A.J., O'Connell, R.J., Age-related changes in female mosquito carbon dioxide detection (2007) J. Med. Entomol., 44, pp. 617-623
  • Greiner, B., Gadenne, C., Anton, S., Central processing of plant volatiles in Agrotis ipsilon males is age-independent in contrast to sex pheromone processing (2002) Chem. Senses, 27, pp. 45-48
  • Groh, C., Ahrens, D., Rössler, W., Environment-and age-dependent plasticity of synaptic complexes in the mushroom bodies of honeybee queens (2006) Brain Behav. Evol., 68, pp. 1-14
  • Groh, C., Lu, Z., Meinertzhagen, I.A., Rössler, W., Age-related plasticity in the synaptic ultrastructure of neurons in the mushroom body calyx of the adult honeybee Apis mellifera (2012) J. Comp. Neurol., 520, pp. 3509-3527
  • Gronenberg, W., Heeren, S., Hölldobler, B., Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus (1996) J. Exp. Biol., 199, pp. 2011-2019
  • Grotewiel, M.S., Martin, I., Bhandari, P., Cook-Wiens, E., Functional senescence in Drosophila melanogaster (2005) Ageing Res. Rev., 4, pp. 372-397
  • Hansson, B.S., (1999) Insect Olfaction, , Berlin: Springer
  • Hansson, B.S., Christensen, T.A., Functional characteristics of the antennal lobe (1999) See Ref., 53, pp. 126-164
  • Haynes, K.F., Birch, M.C., The periodicity of pheromone release and male responsiveness in the artichoke plume moth, Platyptilia carduidactyla (1984) Physiol. Entomol., 9, pp. 287-295
  • Homberg, U., Müller, U., Neuroactive substances in the antennal lobe (1999) See Ref., 53, pp. 181-207
  • Huetteroth, W., Schachtner, J., Standard three-dimensional glomeruli of the Manduca sexta antennal lobe: A tool to study developmental and adult neuronal plasticity (2005) Cell Tissue Res., 319, pp. 513-524
  • Ignell, R., Couillaud, F., Anton, S., Juvenile-hormone-mediated plasticity of aggregation behaviour and olfactory processing in adult desert locusts (2001) J. Exp. Biol., 204, pp. 249-259
  • Jacquin-Joly, E., Lucas, P., Pheromone reception and transduction: Mammals and insects illustrate converging mechanisms across phyla (2005) Curr. Topics Neurochem., 4, pp. 75-105
  • Jang, E.B., Effects of mating and accessory gland injections on olfactory-mediated behavior in the female Mediterranean fruit fly, Ceratitis capitata (1995) J. Insect Physiol., 41, pp. 705-710
  • Jang, E.B., Physiology of mating behavior in Mediterranean fruit fly (Diptera: Tephritidae): Chemoreception and male accessory gland fluids in female post-mating behavior (2002) Fla. Entomol., 85, pp. 89-93
  • Jarriault, D., Barrozo, R.B., De Carvalho Pinto, C.J., Greiner, B., Dufour, M.C., Age-dependent plasticity of sex pheromone response in the moth, Agrotis ipsilon: Combined effects of octopamine and juvenile hormone (2009) Horm. Behav., 56, pp. 185-191
  • Katsoyannos, B.I., Male sex pheromone of Rhagoletis cerasi L. (Diptera, Tephritidae): Factors affecting release and response and its role in the mating behaviour (1982) Z. Angew. Entomol., 94, pp. 187-198
  • Keil, T.A., Morphology and development of the peripheral olfactory organs (1999) See Ref., 53, pp. 5-48
  • Klowden, M.J., The endogenous regulation of mosquito reproductive behavior (1990) Experientia, 46, pp. 660-670
  • Klowden, M.J., Endocrine aspects ofmosquito reproduction (1997) Arch. Insect Biochem. Physiol., 35, pp. 491-512
  • Klowden, M.J., Sexual receptivity in Anopheles gambiae mosquitoes: Absence of control by male accessory gland substances (2001) J. Insect Physiol., 47, pp. 661-666
  • Klowden, M.J., Blackmer, J.L., Humoral control of preoviposition behavior in the mosquito, Aedes aegypti (1987) J. Insect Physiol., 33, pp. 689-692
  • Klowden, M.J., Lea, A.O., Abdominal distention terminates subsequent host-seeking behaviour of Aedes aegypti following a blood meal (1979) J. Insect Physiol., 25, pp. 583-585
  • Klowden, M.J., Lea, A.O., Humoral inhibition of host-seeking in Aedes aegypti during oocyte maturation (1979) J. Insect Physiol., 25, pp. 231-235
  • Krishnan, B., Dryer, S.E., Hardin, P.E., Circadian rhythms in olfactory responses of Drosophila melanogaster (1999) Nature, 400, pp. 375-378
  • Kromann, S.H., Saveer, A.M., Binyameen, M., Bengtsson, M., Birgersson, G., Concurrent modulation of neuronal and behavioural olfactory responses to sex and host plant cues in a male moth (2014) Proc. R. Soc. B, 282, p. 20141884
  • Landolt, P.J., Heath, R.R., 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 (1988) Environ. Entomol., 17, pp. 47-51
  • Lange, A., Orchard, I., Barrett, F.M., Changes in hemolymph serotonin levels associated with feeDing in the bloodsucking bug, Rhodnius prolixus (1989) J. Insect Physiol., 35, pp. 393-399
  • Latorre-Estivalis, J.M., Omondi, B.A., DeSouza, O., Oliveira, I.H.R., Ignell, R., Lorenzo, M.G., Molecular basis of peripheral olfactory plasticity in Rhodnius prolixus, a Chagas disease vector (2015) Front. Ecol. Evol., 3, p. 74
  • Liang, D.S., Schal, C., Circadian rhythmicity and development of the behavioral-response to sexpheromone in male brown-banded cockroaches, Supella longipalpa (1990) Physiol. Entomol., 15, pp. 355-361
  • Lightle, D., Ambrosino, M., Lee, J.C., Sugar in moderation: Sugar diets affect short-term parasitoid behaviour (2010) Physiol. Entomol., 35, pp. 179-185
  • Linn, C.E., Campbell, M.G., Poole, K.R., Wu, W.-Q., Roelofs, W.L., Effects of photoperiod on the circadian timing of pheromone response in male Trichoplusia ni: Relationship to the modulatory action of octopamine (1996) J. Insect Physiol., 42, pp. 881-891
  • Linn, C.E., Campbell, M.G., Roelofs, W.L., Photoperiod cues and the modulatory action of octopamine and 5-hydroxytryptamine on locomotor and pheromone in male gypsy moths, Lymantria dispar (1992) Arch. Insect Biochem. Physiol., 20, pp. 265-284
  • Liu, R., Lehane, S., He, X., Lehane, M., Hertz-Fowler, C., Characterisations of odorant-binDing proteins in the tsetse fly Glossina morsitans morsitans (2010) Cell. Mol. Life Sci., 67, pp. 919-929
  • Lorenzo, M.G., Lazzari, C.R., Activity pattern in relation to refuge exploitation and feeDing in Triatoma infestans (Hemiptera: Reduviidae) (1998) Acta Trop., 70, pp. 163-170
  • Luo, S., Michaud, J.P., Li, J., Liu, X., Zhang, Q., Odor learning in Microplitis mediator (Hymenoptera: Braconidae) is mediated by sugar type and physiological state (2013) Biol. Control, 65, pp. 207-211
  • Marinotti, O., Calvo, E., Nguyen, Q.K., Dissanayake, S., Ribeiro, J.M.C., James, A.A., Genome-wide analysis of gene expression in adult Anopheles gambiae (2006) Insect Mol. Biol., 15, pp. 1-12
  • Martel, V., Anderson, P., Hansson, B.S., Schlyter, F., Peripheral modulation of olfaction by physiological state in the Egyptian leaf worm Spodoptera littoralis (Lepidoptera: Noctuidae) (2009) J. Insect Physiol., 55, pp. 793-797
  • Masante-Roca, I., Anton, S., Delbac, L., Dufour, M.-C., Gadenne, C., Attraction of the grapevine moth to host and non-host plant parts in the wind tunnel: Effects of plant phenology, sex, and mating status (2007) Entomol. Exp. Appl., 122, pp. 239-245
  • McQuillan, H.J., Barron, A.B., Mercer, A.R., Age-and behaviour-related changes in the expression of biogenic amine receptor genes in the antennae of honey bees (Apis mellifera) (2012) J. Comp. Physiol. A, 198, pp. 753-761
  • Mechaber, W.L., Capaldo, C.T., Hildebrand, J.G., Behavioral responses of adult female tobacco hornworms, Manduca sexta, to host plant volatiles change with age and mating status (2002) J. Insect Sci., 2, p. 5
  • Merlin, C., Francois, M.-C., Queguiner, I., Maibeche-Coisne, M., Jacquin-Joly, E., Evidence for a putative antennal clock in Mamestra brassicae: Molecular cloning and characterization of two clock genes-period and cryptochrome-in antennae (2006) Insect Mol. Biol., 15, pp. 137-145
  • Merlin, C., Lucas, P., Rochat, D., François, M., Mäbèche-Coisne, M., Jacquin-Joly, E., An antennal circadian clock and circadian rhythms in peripheral pheromone reception in the moth Spodoptera littoralis (2007) J. Biol. Rhythms, 22, pp. 502-514
  • Naccarati, C., Audsley, N., Keen, J.N., Kim, J.-H., Howell, G.J., The host-seeking inhibitory peptide, Aea-HP-1, is made in the male accessory gland and transferred to the female during copulation (2012) Peptides, 34, pp. 150-157
  • Nässel, D.R., Serotonin and serotonin-immunoreactive neurons in the nervous system of insects (1988) Prog. Neurobiol., 30, pp. 1-85
  • Niven, J.E., Laughlin, S.B., Energy limitation as a selective pressure on the evolution of sensory systems (2008) J. Exp. Biol., 211, pp. 1792-1804
  • Otter, C.J.D., Tchikaya, T., Schutte, A.M., Effects of age, sex and hunger on the antennal olfactory sensitivity of tsetse flies (1991) Physiol. Entomol., 16, pp. 173-182
  • Page, T.L., Koelling, E., Circadian rhythm in olfactory response in the antennae controlled by the optic lobe in the cockroach (2003) J. Insect Physiol., 49, pp. 697-707
  • Payne, T.L., Shorey, H.H., Gaston, L.K., Sex pheromones of noctuid moths: Factors influencing antennal responsiveness in males of Trichoplusia ni (1970) J. Insect Physiol., 16, pp. 1043-1055
  • Pearson, G.A., Schal, C., Electroantennogram responses of both sexes of grape root borer (Lepidoptera: Sesiidae) to synthetic female sex pheromone (1999) Environ. Entomol., 28, pp. 943-946
  • Pham-Delegue, M.H., Trouiller, J., Caillaud, C.M., Roger, B., Masson, C., Effect of queen pheromone on worker bees of different ages: Behavioural and electrophysiological responses (1993) Apidologie, 24, pp. 267-281
  • Qiu, Y.T., Van Loon, J.J.A., Takken, W., Meijerink, J., Smid, H.M., Olfactory coDing in antennal neurons of the malaria mosquito, Anopheles gambiae (2006) Chem. Senses, 31, pp. 845-863
  • Randlkofer, B., Obermaier, E., Meiners, T., Mother's choice of the oviposition site: Balancing risk of egg parasitism and need of food supply for the progeny with an infochemical shelter? (2007) Chemoecology, 17, pp. 177-186
  • Reddy, G.V.P., Guerrero, A., Behavioral responses of the diamondback moth, Plutella xylostella, to green leaf volatiles of Brassica oleracea subsp capitata (2000) J. Agric. Food Chem., 48, pp. 6025-6029
  • Reisenman, C.E., Hunger is the best spice: Effects of starvation in the antennal responses of the blood-sucking bug Rhodnius prolixus (2014) J. Insect Physiol., 71, pp. 8-13
  • Reisenman, C.E., Lee, Y., Gregory, T., Guerenstein, P.G., Effects of starvation on the olfactory responses of the blood-sucking bug Rhodnius prolixus (2013) J. Insect Physiol., 59, pp. 717-721
  • Rinker, D.C., Pitts, R.J., Zhou, X., Suh, E., Rokas, A., Blood meal-induced changes to antennal transcriptome profiles reveal shifts in odor sensitivities in Anopheles gambiae (2013) PNAS, 110, pp. 8260-8265
  • Root, C.M., Ko, K.I., Jafari, A., Wang, J.W., Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search (2011) Cell, 145, pp. 133-144
  • Rospars, J.P., Structure and development of the insect antennodeutocerebral system (1988) Int. J. Insect Morphol. Embryol., 17, pp. 243-294
  • Rund, S.S.C., Bonar, N.A., Champion, M.M., Ghazi, J.P., Houk, C.M., Daily rhythms in antennal protein and olfactory sensitivity in the malaria mosquito Anopheles gambiae (2013) Sci. Rep., 3, p. 2494
  • Rund, S.S.C., Gentile, J.E., Duffield, G.E., Extensive circadian and light regulation of the transcriptome in the malaria mosquito Anopheles gambiae (2013) BMC Genomics, 14, p. 218
  • Rund, S.S.C., Hou, T.Y., Ward, S.M., Collins, F.H., Duffield, G.E., Genome-wide profiling of diel and circadian gene expression in the malaria vector Anopheles gambiae (2011) PNAS, 108, pp. E421-E430
  • Ruther, J., Stahl, L.M., Steiner, S., Garbe, L.A., Tolasch, T., A male sex pheromone in a parasitic wasp and control of the behavioral response by the female's mating status (2007) J. Exp. Biol., 210, pp. 2163-2169
  • Saveer, A.M., Kromann, S.H., Birgersson, G., Bengtsson, M., Lindblom, T., Floral to green: Mating switches moth olfactory coDing and preference (2012) Proc. R. Soc. B, 279, pp. 2314-2322
  • Schuckel, J., Siwicki, K.K., Stengl, M., Putative circadian pacemaker cells in the antenna of the hawkmoth Manduca sexta (2007) Cell Tissue Res., 330, pp. 271-278
  • Seabrook, W.D., Hirai, K., Shorey, H.H., Gaston, L.K., Maturation and senescence of an insect chemosensory response (1979) J. Chem. Ecol., 5, pp. 587-594
  • Seid, M.A., Traniello, J.F.A., Age-related repertoire expansion and division of labor in Pheidole dentata (Hymenoptera: Formicidae): A new perspective on temporal polyethism and behavioral plasticity in ants (2006) Behav. Ecol. Sociobiol., 60, pp. 631-644
  • Sengupta, P., The belly rules the nose: FeeDing state-dependent modulation of peripheral chemosensory responses (2013) Curr. Opin. Neurobiol., 23, pp. 68-75
  • Shorey, H.H., Morin, K.L., Gaston, L.K., Sex pheromones of noctuid moths (1968) XV. Timing of Development of Pheromone-responsiveness and Other Indicators of Reproductive Age in Males of Eight Species. Ann. Entomol Soc. Am., 61, pp. 857-861
  • Siju, K.P., Hansson, B., Ignell, R., Immunocytochemical localization of serotonin in the central and peripheral chemosensory system of mosquitoes (2008) Arthropod Struct. Dev., 37, pp. 248-259
  • Siju, K.P., Hill, S.R., Hansson, B.S., Ignell, R., Influence of blood meal on the responsiveness of olfactory receptor neurons in antennal sensilla trichodea of the yellow fever mosquito, Aedes aegypti (2010) J. Insect Physiol., 56, pp. 659-665
  • Silvegren, G., Löfstedt, C., Rosen, W.Q., Circadian mating activity and effect of pheromone preexposure on pheromone response rhythms in the moth Spodoptera littoralis (2005) J. Insect Physiol., 51, pp. 277-286
  • Takken, W., Van Loon, J., Adam, W., Inhibition of host-seeking response and olfactory responsiveness in Anopheles gambiae following blood feeding (2001) J. Insect Physiol., 47, pp. 303-310
  • Tanoue, S., Krishnan, P., Krishnan, B., Dryer, S.E., Hardin, P.E., Circadian clocks in antennal neurons are necessary and sufficient for olfaction rhythms in Drosophila (2004) Curr. Biol., 14, pp. 638-649
  • Turgeon, J.J., McNeil, J.N., Roelofs, W.L., Responsiveness of Pseudaletia unipuncta males to the female sex pheromone (1983) Physiol. Entomol., 8, pp. 339-344
  • Van Der Goes Van Naters, W.M., Den Otter, C.J., Maes, F.W., Olfactory sensitivity in tsetse flies: A daily rhythm (1998) Chem. Senses, 23, pp. 351-357
  • Vergoz, V., McQuillan, H.J., Geddes, L.H., Pullar, K., Nicholson, B.J., Peripheralmodulation of worker bee responses to queen mandibular pheromone (2009) PNAS, 106, pp. 20930-20935
  • Vitecek, S., Maria, A., Blais, C., Duportets, L., Gaertner, C., 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? (2013) Horm. Behav., 63, pp. 700-708
  • Wang, S., Zhang, S., Sato, K., Srinivasan, M.V., Maturation of odor representation in the honeybee antennal lobe (2005) J. Insect Physiol., 51, pp. 1244-1254
  • Warnes, M.L., Finlayson, L.H., Electroantennogram responses of the stable fly, Stomoxys calcitrans, to carbon dioxide and other odors (1986) Physiol. Entomol., 11, pp. 469-473
  • Wilson, R.I., Mainen, Z.F., Early events in olfactory processing (2006) Annu. Rev. Neurosci., 29, pp. 163-201
  • Winnington, A.P., Napper, R.M., Mercer, A.R., Structural plasticity of identified glomeruli in the antennal lobes of the adult worker honey bee (1996) J. Comp. Neurol., 365, pp. 479-490
  • Worster, A.S., Seabrook, W.D., Electrophysiological investigation of diel variations in the antennal sensitivity of the male spruce budworm moth Choristoneura fumiferana (Lepidoptera: Tortricidae) (1989) J. Insect Physiol., 35, pp. 1-5
  • Wyatt, T.D., (2014) Pheromones and Animal Behavior, , Cambridge, UK: Cambridge Univ. Press
  • Yeh, C., Klowden, M.J., Effects of male accessory gland substances on the pre-oviposition behaviour of Aedes aegypti mosquitoes (1990) J. Insect Physiol., 36, pp. 799-803
  • Zhukovskaya, M.I., Circadian rhythm of sex pheromone perception in themale American cockroach, Periplaneta americana L (1995) J. Insect Physiol., 41, pp. 941-946

Citas:

---------- APA ----------
Gadenne, C., Barrozo, R.B. & Anton, S. (2016) . Plasticity in Insect Olfaction: To Smell or Not to Smell?. Annual Review of Entomology, 61, 317-333.
http://dx.doi.org/10.1146/annurev-ento-010715-023523
---------- CHICAGO ----------
Gadenne, C., Barrozo, R.B., Anton, S. "Plasticity in Insect Olfaction: To Smell or Not to Smell?" . Annual Review of Entomology 61 (2016) : 317-333.
http://dx.doi.org/10.1146/annurev-ento-010715-023523
---------- MLA ----------
Gadenne, C., Barrozo, R.B., Anton, S. "Plasticity in Insect Olfaction: To Smell or Not to Smell?" . Annual Review of Entomology, vol. 61, 2016, pp. 317-333.
http://dx.doi.org/10.1146/annurev-ento-010715-023523
---------- VANCOUVER ----------
Gadenne, C., Barrozo, R.B., Anton, S. Plasticity in Insect Olfaction: To Smell or Not to Smell?. Ann. Rev. Entomol. 2016;61:317-333.
http://dx.doi.org/10.1146/annurev-ento-010715-023523