Skip to main content
Log in

Fine structure and primary sensory projections of sensilla located in the labial-palp pit organ of Helicoverpa armigera (Insecta)

Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The fine structure and primary sensory projections of sensilla located in the labial-palp pit organ of the cotton bollworm Helicoverpa armigera (Insecta, Lepidoptera) are investigated by scanning electron and transmission electron microscopy combined with confocal laser scanning microscopy. The pit organ located on the third segment of the labial palp is about 300 μm deep with a 60-μm-wide opening, each structure containing about 1200 sensilla. Two sensillum types have been found, namely hair-shaped and club-shaped sensilla, located on the upper and lower half of the pit, respectively. Most sensilla possess a single dendrite. The dendrite housed by the club-shaped sensilla is often split into several branches or becomes lamellated in the outer segment. As reported previously, the sensory axons of the sensilla in the labial pit organ form a bundle entering the ipsilateral side of the subesophageal ganglion via the labial palp nerve and project to three distinct areas: the labial pit organ glomerulus in each antennal lobe, the subesophageal ganglion and the ventral nerve cord. In the antennal lobe, the labial pit organ glomerulus is innervated by sensory axons from the labial pit organ only; no antennal afferents target this unit. One neuron has been found extending fine processes into the subesophageal ganglion and innervating the labial palp via one branch passing at the base of the labial palp nerve. The soma of this assumed motor neuron is located in the ipsilateral cell body layer of the subesophageal ganglion. Our results provide valuable knowledge concerning the neural circuit encoding information about carbon dioxide and should stimulate further investigations directed at controlling pest species such as H. armigera.

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

Access this article

Price includes VAT (France)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Reference

  • Anton S, Loon JJA van, Meijerink J, Smid HM, Takken W, Rospars JP (2003) Central projections of olfactory receptor neurons from single antennal and palpal sensilla in mosquitoes. Arthropod Struct Dev 32:319–329

    Google Scholar 

  • Bogner F (1990) Sensory physiological investigation of carbon dioxide receptors in Lepidoptera. J Insect Physiol 36:951–957

    Article  Google Scholar 

  • Bogner F, Boppré M, Ernst K-D, Boeckh J (1986) CO2 sensitive receptors on labial palps of Rhodogastria moths (Lepidoptera: Artiidae): physiology, fine structure and central projection. J Comp Physiol [A] 158:741–749

    Article  CAS  Google Scholar 

  • de Bruyne M, Foster K, Carlson JR (2001) Odor coding in the Drosophila antenna. Neuron 30:537–552

    Article  PubMed  Google Scholar 

  • Gillies MT (1980) The role of carbon dioxide in host-finding by mosquitoes (Diptera: Culicidae): a review. Bull Entomol Res 70:525–532

    Article  Google Scholar 

  • Guerenstein PG, Hildebrand JG (2008) Roles and effects of environmental carbon dioxide in insect life. Annu Rev Entomol 53:161–178

    Article  PubMed  CAS  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 

  • Jones WD, Cayirlioglu P, Kadow IG, Vosshall LB (2007) Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 454:86–90

    Article  Google Scholar 

  • Keil TA (1996) Sensilla on the maxillary palps of Helicoverpa armigera caterpillars: in search of the CO2-receptor. Tissue Cell 28:703–717

    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 projections in Manduca sexta and certain other sphinx moths and silk moths. Cell Tissue Res 245:237–245

    Article  PubMed  CAS  Google Scholar 

  • Kleineidam C, Tautz J (1996) Perception of carbon dioxide and other “air-condition” parameters in the leaf cutting ant Atta cephalotes. Naturwissenschaften 83:566–568

    CAS  Google Scholar 

  • Kleineidam C, Romani R, Tautz J, Isidoro N (2000) Ultrastructure and physiology of the CO2 sensitive sensillum amplullaceum in the leaf-cutting ant Atta sexdens. Arthropod Struct Dev 29:43–55

    Article  PubMed  CAS  Google Scholar 

  • Kwon JY, Dahanukar A, Weiss LA, Carlson JR (2007) The molecular basis of CO2 reception in Drosophila. Proc Nat Acad Sci USA 104:3574–3578

    Article  PubMed  CAS  Google Scholar 

  • Lee J-K, Altner H (1986) Primary sensory projections of the labial palp-pit organ of Pieris rapae L. (Lepidoptera: Pieridae). Int J Insect Morphol Embryol 15:439–448

    Article  CAS  Google Scholar 

  • Lee J-K, Selzer R, Altner H (1985) Lamellated outer dendritic segments of a chemoreceptor within wall-pore sensilla in the labial palp-pit organ of the butterfly, Pieris rapae L. (Insecta, Lepidoptera). Cell Tissue Res 240:333–342

    Article  Google Scholar 

  • Lu T, Qiu YT, Wang G, Kwon JY, Rutzler M, Kwon HW, Pitts RJ, Loop JJA van, Takken W, Carlson JR, Zwiebel LJ (2007) Odor coding in the maxillary palp of the malaria vector mosquito Anopheles gambiae. Current Biol 17:1533–1544

    Google Scholar 

  • Rasch C, Rembold H (1994) Carbon-dioxide—highly attractive signal for larvae of Helicoverpa armigera. Naturwissenschaften 81:228–229

    Google Scholar 

  • Shanbhag SR, Müller B, Steinbrecht RA (1999) Atlas of olfactory organs of Drosophila melanogaster. 1. Types, external organization, innervation and distribution of olfactory sensilla. Int J Insect Morphol Embryol 28:377–397

    Article  Google Scholar 

  • Seeley TD (1974) Atmospheric carbon dioxide regulation in honeybee (Apis mellifera) colonies. J Insect Physiol 20:2301–2305

    Article  PubMed  CAS  Google Scholar 

  • Southwick EE, Moritz RFA (1987) Social control of air ventilation in colonies of honey bees, Apis mellifera. J Insect Physiol 33:623–626

    Article  Google Scholar 

  • Stange G (1992) High resolution measurement of atmospheric carbon dioxide concentration changes by the labial palp organ of the moth Heliothis armigera (Lepidoptera: Noctuidae). J Comp Physiol [A] 171:317–324

    Google Scholar 

  • Stange G (1997) Effects of changes in atmospheric carbon dioxide on the location of hosts by the moth, Cactoblastis cactorum. Oecologia 110:539–545

    Article  Google Scholar 

  • Stange G, Stowe S (1999) Carbon-dioxide sensing structures in terrestrial arthropods. Microsc Res Tech 47:416–427

    Article  PubMed  CAS  Google Scholar 

  • Stange G, Wong C (1993) Moth response to climate. Nature 365:699

    Article  Google Scholar 

  • Stange G, Monro J, Stowe S, Osmond CB (1995) The CO2 sense of the moth Cactoblastis cactorum and its probable role in the biological control of the CAM plant Opuntia stricta. Oecologia 102:341–52

    Article  Google Scholar 

  • Suh GSB, Wong AM, Hergarden AC, Wang JW, Simon AF, Benzer S, Axel R, Anderson DJ (2004) A single population of olfactory sensory neurons mediates an innate avoidance behavior in Drosophila. Nature 431:854–859

    Article  PubMed  CAS  Google Scholar 

  • Syed Z, Leal WS (2007) Maxillary palps are broad spectrum odorant detectors in Culex quinquefasciatus. Chem Senses 32:727–738

    Article  PubMed  CAS  Google Scholar 

  • Thom C, Guerenstein PG, Mechaber WL, Hildebrand JG (2004) Floral CO2 reveals flower profitability to moths. J Chem Ecol 30:1285–1288

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Feng-Ming Yan or Gui-Rong Wang.

Additional information

This work was supported by the following granting bodies: National Science Foundation of China (grant no. 31230062 to G.R.W.), Special Fund for Agro-scientific Researches of the Public Interests (grant no. 201203036 to F.M.Y.) and Opening Project of State Key Laboratory for Biology of Plant Disease and Insect Pests (grant no. SKL20120P09 to X.C.Z.).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhao, XC., Tang, QB., Berg, B.G. et al. Fine structure and primary sensory projections of sensilla located in the labial-palp pit organ of Helicoverpa armigera (Insecta). Cell Tissue Res 353, 399–408 (2013). https://doi.org/10.1007/s00441-013-1657-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-013-1657-z

Keywords

Navigation