Skip to main content

Advertisement

SpringerLink
Log in

Three-dimensional antennal lobe atlas of the oriental fruit moth, Cydia molesta (Busck) (Lepidoptera: Tortricidae): comparison of male and female glomerular organization

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The oriental fruit moth Cydia molesta is an important pest and the behavioural role of olfactory signals such as pheromones and plant volatiles have been studied extensively in both sexes. To understand odour processing further, however, detailed knowledge of the anatomy of the olfactory system is crucial. In the present study, an atlas of the antennal lobe (AL) is presented based on the three-dimensional reconstructions of both ALs of three male and three female brains by means of neuroanatomical and computational approaches. We identified 48–49 "ordinary" glomeruli and one large glomerulus situated at the entrance of the antennal nerve in males, and 49–52 "ordinary" glomeruli and one large glomerulus in the ventro-medial part of the AL in females. Anomalous supernumerary, anomalous missing and sexually dimorphic glomeruli were found in the studied individuals in greater numbers than in other lepidopteran species. Male and female maps were compared with respect to glomerular size and position with 45 glomeruli being matched, indicating a conserved glomerular pattern between the sexes. Three additional glomeruli were sexually dimorphic in size and five male-specific and six female-specific glomeruli were also found. Palp backfills resulted in the staining of a unique glomerulus in both sexes identified as the sexually dimorphic glomerulus 45. This glomerulus was never stained from antennal backfills, which stained the other glomeruli of the AL. The three-dimensional atlas can now be used to elucidate the functional role of individual glomeruli in both sexes of C. molesta.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

3D:

Three-dimensional

AL:

Antennal lobe

AN:

Antennal nerve

Cu:

Cumulus

MGC:

Macroglomerular complex

ORN:

Olfactory receptor neuron

PBS:

Phosphate buffer solution

Z8–12:Ac:

(Z)-8 dodecenyl acetate

E8–12:Ac:

(E)-8 dodecenyl acetate

Z8–12:OH:

(Z)-8 dodecen-1-ol

12:OH:

Dodecan-1-ol

References

  • Ai H, Kanzaki R (2004) Modular organization of the silkmoth antennal lobe macroglomerular complex revealed by voltage-sensitive dye. J Expe Biol 207:633–644

    Article  Google Scholar 

  • Ansebo L (2004) Odour perception in the codling moth Cydia pomonella L.—from brain to behaviour. PhD thesis, Swedish University of Agricultural Sciences, Alnarp

  • Anton S, Hansson B (1994) Central processing of sex pheromone, host odour, and oviposition deterrent information by interneurons in the antennal lobe of female Spodoptera littoralis (Lepidoptera: Noctuidae). J Comp Neurol 350:199–214

    Article  PubMed  CAS  Google Scholar 

  • Anton S, Hansson B (1995) Sex pheromone and plant-associated odour processing in the antennal lobe interneurons of male Spodoptera littoralis (Lepidoptera: Noctuidae). J Comp Physiol 176:773–789

    Article  CAS  Google Scholar 

  • Anton S, Homberg U (1999) Antennal lobe structure. In: Hansson BS (ed) Insect olfaction. Springer, Berlin, pp 98–125

    Google Scholar 

  • Baker TC, Meyer W, Roelofs WL (1981) Sex-pheromone dosage and blend specificity of response by oriental fruit moth males. Entomol Exp Appl 30:269–279

    Article  CAS  Google Scholar 

  • Ben-Yehuda S, Izhar Y, Wyosoki M, Argaman Q (1993) The grape berry moth, Lobesia botrana Denis & Schiffenmueller (Lepidoptera: Tortricidae), in pear orchards, in Israel. J Pest Manag 39:149–151

    Article  Google Scholar 

  • Berg BG, Almaas TJ, Bjaalic JG, Mustaparta H (1998) The macroglomerular complex of the antennal lobe in the tobacco budworm Heliothis virescens: specified subdivision in four compartments according to information about biologically significant compounds. J Comp Physiol 183:669–682

    Article  Google Scholar 

  • Berg BG, Galizia CG, Brandt R, Mustaparta H (2002) 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). J Comp Neurol 446:123–134

    Article  PubMed  Google Scholar 

  • Bhalerao S, Sen A, Reinhard S, Rodrigues V (2003) Olfactory neurons expressing identified receptor genes project to subsets of glomeruli within the antennal lobe of Drosophila melanogaster. J Neurosci 54:577–592

    Google Scholar 

  • Bozza T, Feinstein P, Zheng C, Mombaerts P (2002) Odorant receptor expression defines functional units in the mouse olfactory system. J Neurosci 22:3033–3043

    PubMed  CAS  Google Scholar 

  • Bucher D, Scholz M, Stetter M, Obermayer K, Pflüger HJ (2000) Correction methods for three-dimensional reconstructions from confocal images. I. Tissue shrinking and axial scaling. J Neurosci Methods 100:135–143

    Article  PubMed  CAS  Google Scholar 

  • Cardé AM, Baker TC, Cardé RT (1979) Identification of a four-component sex pheromone of the female oriental fruit moth Grapholita molesta (Lepidoptera: Tortricidae). J Chem Ecol 5:423–427

    Article  Google Scholar 

  • Carlsson MA, Galizia CG, Hansson BS (2002) Spatial representation of odours in the antennal lobe of the moth Spodoptera littoralis (Lepidoptera: Noctuidae). Chem Senses 27:231–244

    Article  PubMed  Google Scholar 

  • Charlton RE, Cardé RT (1981) Comparing the effectiveness of sexual communication disruption in the oriental fruit moth (Grapholita molesta) using different combinations and dosages of its pheromone blend. J Chem Ecol 7:501–508

    Article  CAS  Google Scholar 

  • Chiang AS, Liu YC, Chiu SL, Hu SH, Huang CY, Hsieh CH (2001) Three-dimensional mapping of brain neuropils in the cockroach, Diplotera punctata. J Comp Neurol 440:1–11

    Article  PubMed  CAS  Google Scholar 

  • Christensen TA, Hildebrand JG (2002) Pheromonal and host-odor processing in the insect antennal lobe: how different? Curr Opin Neurobiol 12:393–399

    Article  PubMed  CAS  Google Scholar 

  • Couto A, Alenius M, Dickson BJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15:1535–1547

    Article  PubMed  CAS  Google Scholar 

  • Couton L, Minoli S, Kiêu K, Anton S, Rospars JP (2009) Constancy and variability of identified glomeruli in antennal lobes: computational approach in Spodoptera littoralis. Cell Tissue Res. doi:10.1007/s00441-009-0831-9

  • Figueredo AJ, Baker TC (1991) Reduction of the response to sex pheromone in the oriental fruit moth, Grapholita molesta (Lepidoptera: Tortricidae) following successive pheromonal exposures. J Insect Behav 5:347–363

    Article  Google Scholar 

  • Fishilevich E, Vosshall LB (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15:1548–1553

    Article  PubMed  CAS  Google Scholar 

  • Flanagan D, Mercer AR (1989) An atlas and 3-D reconstruction of the antenal lobes in the worker honeybee, Apis mellifera L. (Hymenoptera: Apidae). Int J Insect Morphol Embryol 18:145–159

    Article  Google Scholar 

  • Gabel B, Thiéry D, Suchy V, Marion-Poll F, Hradsky P, Farkas P (1992) Floral volatiles of Tanacetum vulgare L. attractive to Lobesia botrana Den. and Schiff. females. J Chem Ecol 18:693–701

    Article  CAS  Google Scholar 

  • Galizia CG, McIlwrath SL, Menzel R (1999) A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res 295:383–394

    Article  PubMed  CAS  Google Scholar 

  • Galizia CG, Sachse S, Mustaparta H (2000) Calcium responses to pheromone and plant odours in the antennal lobe of the male and female moth Heliothis virescens. J Comp Physiol [A] 186:1049–1063

    Article  CAS  Google Scholar 

  • Gao Q, Yuan B, Chess A (2000) Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat Neurobiol 3:780–785

    CAS  Google Scholar 

  • Ghaninia M, Hansson BS, Ignell R (2007) The antennal lobe of the African malaria mosquito, Anopheles gambiae—innervation and three-dimensional reconstruction. Arthropod Struct Dev 36:23–39

    Article  PubMed  Google Scholar 

  • Greiner B, Gadenne C, Anton S (2004) Three-dimensional antennal lobe atlas of the male moth, Agrotis ipsilon: a tool to study structure-function correlation. J Comp Neurol 475:202–210

    Article  PubMed  Google Scholar 

  • Guerenstein PG, Hildebrand JG (2007) Roles and effects of environmental carbon dioxide in insect life. Annu Rev Entomol 53:20–40

    Google Scholar 

  • Guerenstein PG, Christensen TA, Hildebrand JG (2004) Sensory processing of ambient CO2 information in the brain of the moth Manduca sexta. J Comp Physiol [A] 190:707–725

    Google Scholar 

  • Hansson BS, Ljunberg H, Hallberg E, Löfstedt C (1992) Functional specialization of olfactory glomeruli in a moth. Science 256:1313–1315

    Article  PubMed  CAS  Google Scholar 

  • Hickel ER, Ducroquet JPHJ (1998) Monitoring and control of Grapholita molesta in Alto Vale do Rio do Peixe. Agropecuaria Catarin 11:8–11

    Google Scholar 

  • Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595–631

    Article  PubMed  CAS  Google Scholar 

  • Hillier NK, Vickers NJ (2007) Physiology and antennal lobe projections of olfactory receptor neurons from sexually isomorphic sensilla on male Helitohis virescens. J Comp Physiol [A] 193:649–663

    Article  CAS  Google Scholar 

  • Hillier NK, Kleineidam C, Vickers NJ (2006) Physiology and glomerular projections of olfactory receptor neurons on the antenna of female Heliothis virescens (Lepidoptera: Noctuidae) responsive to behaviourally relevant odors. J Comp Physiol [A] 192:199–219

    Article  CAS  Google Scholar 

  • Huetteroth W, Schachtner J (2005) Standard three-dimensional glomeruli of the Manduca sexta antennal lobe: a tool to study both developmental and adult neuronal plasticity. Cell Tissue Res 319:513–524

    Article  PubMed  Google Scholar 

  • Ignell R, Anton S, Hansson B (2001) The antennal lobe of orthoptera: anatomy and evolution. Brain Behav Evol 57:1–17

    Article  PubMed  CAS  Google Scholar 

  • Ignell R, Dekker T, Ghaninia M, Hansson BS (2005) Neuronal architecture of the mosquito deutocerebrum. J Comp Neurol 493:207–240

    Article  PubMed  Google Scholar 

  • Il’ichev AL, Williams DG, Milner AD (2004) Mating disruption barriers in pome fruit for improved control of oriental fruit moth Grapholita molesta Busck (Lepidoptera: Tortricidae) in stone fruit under mating disruption. J Appl Entomol 128:126–132

    Article  Google Scholar 

  • Joerges J, Küttner A, Galizia CG, Menzel R (1997) Representations of odours and odour mixtures visualized in the honeybee brain. Nature 387:285–288

    Article  CAS  Google Scholar 

  • Jourdan F, Duveau A, Astic L, Holley A (1980) Spatial distribution of [14C]2-deoxyglucose uptake in the olfactory bulbs of rats stimulated with two different odours. Brain Res 188:139–154

    Article  PubMed  CAS  Google Scholar 

  • Katerinopoulos HE, Pagona G, Afratis A, Stratigakis N, Roditakis N (2005) Composition and insect attracting activity of the essential oil of Rosmarinus officinalis. J Chem Ecol 31:111–122

    Article  PubMed  CAS  Google Scholar 

  • Kauer JS (2002) On the scents of smell in the salamander. Nature 417:336–342

    Article  PubMed  CAS  Google Scholar 

  • Kent KS, Harrow ID, Quartararo P, Hildebrand JG (1986) An accessory olfactory pathway in Lepidoptera: the labial pit organ and its central projection in Manduca sexta and certain other sphinx moths and silk moths. Cell Tissue Res 245:237–245

    Article  PubMed  CAS  Google Scholar 

  • Klagges BRE, Heimbeck G, Godenschwege TA, Hofbauer A, Plufgfelder GO, Reifegerste R, Reisch D, Schaupp M, Buchner S, Buchner E (1996) Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurobiol 16:3154–3165

    CAS  Google Scholar 

  • Kleineidam CJ, Obermayer M, Halbich W, Rossler W (2005) A macroglomerulus in the antennal lobe of the leaf-cutting ant workers and its possible functional significance. Chem Senses 30:383–392

    Article  PubMed  CAS  Google Scholar 

  • Kovanci OB, Walgenbach JF, Kennedy GG (2004) Evaluation of extended-season mating disruption of the oriental fruit moth Grapholita molesta (Busck) (Lep., Tortricidae) in apples. J Appl Entomol 128:664–669

    Article  CAS  Google Scholar 

  • Lacey MJ, Sanders CJ (1992) Chemical composition of sex pheromone of oriental fruit moth and rates of release by individual female moths. J Chem Ecol 18:1421–1435

    Article  CAS  Google Scholar 

  • Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF, Stocker RF (1999) Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 405:543–552

    Article  PubMed  CAS  Google Scholar 

  • Linn CE, Roelofs WL (1983) Effect of varying proportions of the alcohol component on sex pheromone blend discrimination in male oriental fruit moths. Physiol Entomol 8:291–306

    Article  CAS  Google Scholar 

  • Ljunberg H, Anderson P, Hansson BS (1993) Physiology and morphology of pheromone-specific sensilla on the antennae of male and female Spodoptera littoralis (Lepidoptera: Noctuidae). J Insect Physiol 39:253–260

    Article  Google Scholar 

  • Masante-Roca I, Gadenne C, Anton S (2005) Three-dimensional antennal lobe atlas of male and female moths, Lobesia botrana (Lepidoptera: Tortricidae) and glomerular representation of plant volatiles in females. J Exp Biol 208:1147–1159

    Article  PubMed  Google Scholar 

  • Meijerink J, Carlsson MA, Hansson BS (2003) Spatial representation of odorant structure in the moth antennal lobe: a study of structure-response relationships at low doses. J Comp Neurol 467:11–21

    Article  PubMed  Google Scholar 

  • Mustaparta H (2005) Innate and changed responses to plant odours in moths and weevils. Chem Senses 30:1297–1298

    Article  Google Scholar 

  • Natale D, Mattiacci L, Pasqualini E, Dorn S (2004) Apple and peach fruit volatiles and the apple constituint butyl hexanoate attract female oriental fruit moth, Cydia molesta, in the laboratory. J Appl Entomol 128:22–27

    Article  Google Scholar 

  • Ochieng SA, Anderson P, Hansson BS (1995) Antennal lobe projection patterns of olfactory receptor neurons involved in sex pheromone detection in Spodoptera littoralis (Lepidoptera: Noctuidae). Tissue Cell 27:221–232

    Article  PubMed  CAS  Google Scholar 

  • Piñero JC, 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

    Article  CAS  Google Scholar 

  • Piñero JC, Galizia CG, Dorn S (2007) 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. J Insect Physiol 54:333–343

    Article  PubMed  CAS  Google Scholar 

  • Reis FW, Nora I, Melzer R (1988) Population dynamics of Grapholita molesta, Busck, 1916, and its adaptation on apple in south Brazil. Acta Hort 232:204–208

    Google Scholar 

  • Roelofs WL, Comeau A, Selle R (1969) Sex pheromone of the oriental fruit moth. Nature 224:723

    Article  CAS  Google Scholar 

  • Rospars JP (1983) Invariance and sex-specific variations of the glomerular organization in the antennal lobes of a moth, Mamestra brassicae, and a butterfly, Pieris brassicae. J Comp Neurol 220:80–96

    Article  PubMed  CAS  Google Scholar 

  • Rospars JP (1988) Structure and development of the insect antennodeutocerebral system. Int J Insect Morphol Embryol 17:243–294

    Article  Google Scholar 

  • Rospars JP, Chambille I (1981) The deutocerebrum of the cockroach Blaberus craniifer Burm. Quantitative study and automated identification of the glomeruli. J Neurobiol 12:221–247

    Article  PubMed  CAS  Google Scholar 

  • Rospars JP, Chambille I (1989) Identified glomeruli in the antennal lobes of insects: invariance, sexual variation and postembryonic development. In: Singh RN, Strausfeld NJ (eds) Neurobiology of sensory systems. Plenum, New York, pp 355–375

    Google Scholar 

  • Rospars JP, Hildebrand JG (1992) Anatomical identification of glomeruli in the antennal lobes of the male sphinx moth Manduca sexta. Cell Tissue Res 270:205–227

    Article  PubMed  CAS  Google Scholar 

  • Rospars JP, Hildebrand JG (2000) Sexually dimorphic and isomorphic glomeruli in the antennal lobes of the sphinx moth Manduca sexta. Chem Senses 25:119–129

    Article  PubMed  CAS  Google Scholar 

  • Rothschild GHL, Vickers RA (1991) Biology, ecology and control of the oriental fruit moth. In: Van der Geest LPS, Evenhus HH (eds) World crop pest, tortricid pests: their biology, natural enemies and control, vol 5. Elsevier, Amsterdam, pp 389–412

    Google Scholar 

  • Rumbo ER, Vickers RA (1997) Prolonged adaptation as possible mating disruption mechanism in oriental fruit moth, Cydia (= Grapholita) molesta. J Chem Ecol 23:445–457

    Article  CAS  Google Scholar 

  • Sadek MM, Hansson BS, Rospars JP, Anton S (2002) Glomerular representation of plant volatiles and sex pheromone components in the antennal lobe of the female Spodoptera littoralis. J Exp Biol 205:1363–1376

    PubMed  CAS  Google Scholar 

  • Skiri HT, Ro H, Berg BG, Mustaparta H (2005) Consistent organization of glomeruli in the antennal lobes of related species of heliothine moths. J Comp Neurol 491:367–380

    Article  PubMed  Google Scholar 

  • Smid HM, Bleeker MAK, Loon JJA van, Vet LEM (2003) Three-dimensional organization of the glomeruli in the antennal lobe of the parasitoid wasps Cotesia glomerata and C. rubecula. Cell Tissue Res 312:237–248

    PubMed  Google Scholar 

  • Stelinski LL, Vogel KJ, Gut LJ, Miller JR (2005) Seconds-long preexposures to pheromone from rubber septum or polyethelene tube dispensers alters subsequent behavioral responses of male Grapholita molesta (Lepidoptera: Tortricidae) in a sustained-flight tunnel. Environ Entomol 34:696–704

    Article  Google Scholar 

  • Stelinski LL, Il’ichev AL, Gut LJ (2006) Antennal and behavioural responses of virgin and mated oriental fruit moth (Lepidoptera: Tortricidae) females to their sex pheromone. Ann Entomol Soc Am 99:898–904

    Article  CAS  Google Scholar 

  • Stocker RF, Lienhard MC, Borst A, Fischbach KF (1990) Neuronal architecture of the antennal lobe in D. melanogaster. Cell Tissue Res 262:9–34

    Article  PubMed  CAS  Google Scholar 

  • Todd JL, Baker TC (1996) Antennal lobe partitioning of behaviourally active odors in female cabbage looper moths. Naturwissenschaften 83:324–326

    Article  CAS  Google Scholar 

  • Todd JL, Anton S, Hansson BS, Baker TC (1995) Functional organization of the macroglomerular complex related to behaviourally expressed olfactory redundancy in male cabbage looper moths. Physiol Entomol 20:349–361

    Article  Google Scholar 

  • Vickers NJ, Christensen TA, Hildebrand JG (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

    Article  PubMed  CAS  Google Scholar 

  • Vosshall LB, Wong AM, Axel R (2000) An olfactory sensory map in the fly brain. Cell 102:147–159

    Article  PubMed  CAS  Google Scholar 

  • Wang JW, Wong AM, Flores J, Vosshall LB, Axel R (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112:271–282

    Article  PubMed  CAS  Google Scholar 

  • Zube C, Kleineidam CJ, Kirschner S, Neef J, Rossler W (2008) Organization of the olfactory pathway and odor processing in the antennal lobe of the ant Camponotus floridanus. J Comp Neurol 506:425–441

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Romina Barrozo for helpful comments on the manuscript and with the preparation of figures. The monoclonal antibody developed by Erich Buchner was obtained from the Developmental Studies Hybridoma Bank developed under the auspices of the NICHD and maintained by the University of Iowa, Department of Biological Sciences, Iowa City, IA 52242, USA.

Author information

Authors and Affiliations

  1. Department of Crop Protection Centre UdL-IRTA, Av. Alcalde Rovira Roure 191, 25198, Lleida, Spain

    Nélia Varela & Jesús Avilla

  2. INRA, UMR 1272 Physiologie de l’Insecte, 78000, Versailles, France

    Louise Couton, Jean-Pierre Rospars & Sylvia Anton

  3. Department of Crop and Forest Science, University of Lleida, Av. Alcalde Rovira Roure 191, 25198, Lleida, Spain

    César Gemeno

  4. INRA, UMR 1272, Route de St. Cyr, 78026, Versailles Cedex, France

    Sylvia Anton

Authors
  1. Nélia Varela
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Louise Couton
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. César Gemeno
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jesús Avilla
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jean-Pierre Rospars
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sylvia Anton
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sylvia Anton.

Additional information

Nélia Varela and Louise Couton contributed equally to this work.

This study was supported by research grants from INRA (Projet Jeune Equipe and Projet S.P.E.) to S.A. and J.P.R. and by the Spanish Ministry of Science and Technology (research grant AGL2004-05812/AGR to J.A. and C.G., Spanish Science and Education Department, MEC). N.V. was financed by fellowship no. BES-2005-7605 (MEC, Spain).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Varela, N., Couton, L., Gemeno, C. et al. Three-dimensional antennal lobe atlas of the oriental fruit moth, Cydia molesta (Busck) (Lepidoptera: Tortricidae): comparison of male and female glomerular organization. Cell Tissue Res 337, 513–526 (2009). https://doi.org/10.1007/s00441-009-0839-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-009-0839-1

Keywords

Search

Navigation