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Molecules and Cells

, Volume 35, Issue 2, pp 87–92 | Cite as

Olfactory carbon dioxide detection by insects and other animals

  • Walton Jones
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Abstract

Carbon dioxide is a small, relatively inert, but highly volatile gas that not only gives beer its bubbles, but that also acts as one of the primary driving forces of anthropogenic climate change. While beer brewers experiment with the effects of CO2 on flavor and climate scientists are concerned with global changes to ambient CO2 levels that take place over the course of decades, many animal species are keenly aware of changes in CO2 concentration that occur much more rapidly and on a much more local scale. Although imperceptible to us, these small changes in CO2 concentration can indicate imminent danger, signal overcrowding, and point the way to food. Here I review several of these CO2-evoked behaviors and compare the systems insects, nematodes, and vertebrates use to detect environmental CO2.

Keywords

behavior carbon dioxide CO2 olfaction 

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References

  1. Ai, M., Min, S., Grosjean, Y., Leblanc, C., Bell, R., Benton, R., and Suh, G.S.B. (2010). Acid sensing by the Drosophila olfactory system. Nature 468, 691–695.PubMedCrossRefGoogle Scholar
  2. Badsha, F., Kain, P., Prabhakar, S., Sundaram, S., Padinjat, R., Rodrigues, V., and Hasan, G. (2012). Mutants in Drosophila TRPC channels reduce olfactory sensitivity to carbon dioxide. PLoS One 7, e49848.PubMedCrossRefGoogle Scholar
  3. Barrozo, R.B., and Lazzari, C.R. (2006). Orientation response of haematophagous bugs to CO2: the effect of the temporal structure of the stimulus. J. Comp. Phys. A 192, 827–831.CrossRefGoogle Scholar
  4. Bensafi, M., Iannilli, E., Gerber, J., and Hummel, T. (2008). Neural coding of stimulus concentration in the human olfactory and intranasal trigeminal systems. Neuroscience 154, 832–838.PubMedCrossRefGoogle Scholar
  5. Benton, A.H., and Lee, S.Y. (1965). Sensory reactions of Siphonaptera in relation to host-finding. Am. Midland Nat. 119–125.Google Scholar
  6. Benton, R., Vannice, K.S., Gomez-Diaz, C., and Vosshall, L.B. (2009). Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136, 149–162.PubMedCrossRefGoogle Scholar
  7. Bretscher, A.J., Busch, K.E., and de Bono, M. (2008). A carbon dioxide avoidance behavior is integrated with responses to ambient oxygen and food in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 105, 8044–8049.PubMedCrossRefGoogle Scholar
  8. Bretscher, A.J., Kodama-Namba, E., Busch, K.E., Murphy, R.J., Soltesz, Z., Laurent, P., and de Bono, M. (2011). Temperature, oxygen, and salt-sensing neurons in C. elegans are carbon dioxide sensors that control avoidance behavior. Neuron 69, 1099–1113.PubMedCrossRefGoogle Scholar
  9. Buehlmann, C., Hansson, B.S., and Knaden, M. (2012). Path integration controls nest-plume following in desert ants. Curr. Biol. 22, 645–649.PubMedCrossRefGoogle Scholar
  10. Croset, V., Rytz, R., Cummins, S.F., Budd, A., Brawand, D., Kaessmann, H., Gibson, T.J., and Benton, R. (2010). Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet. 6, e1001064.PubMedCrossRefGoogle Scholar
  11. de Bruyne, M., Foster, K., and Carlson, J.R. (2001). Odor coding in the Drosophila antenna. Neuron 30, 537–552.PubMedCrossRefGoogle Scholar
  12. Dessirier, J.M., Simons, C.T., Carstens, M.I., O’Mahony, M., and Carstens, E. (2000). Psychophysical and neurobiological evidence that the oral sensation elicited by carbonated water is of chemogenic origin. Chem. Senses 25, 277–284.PubMedCrossRefGoogle Scholar
  13. Dillman, A.R., Guillermin, M.L., Lee, J.H., Kim, B., Sternberg, P.W., and Hallem, E.A. (2012). Olfaction shapes host-parasite interactions in parasitic nematodes. Proc. Natl. Acad. Sci. USA 109, E2324–E2333.PubMedCrossRefGoogle Scholar
  14. Fallis, A.M., and Raybould, J.N. (1975). Response of two African simuliids to silhouettes and carbon dioxide. J. Med. Ent. 12, 349–351.Google Scholar
  15. Fülle, H.J., Vassar, R., Foster, D.C., Yang, R.B., Axel, R., and Garbers, D.L. (1995). A receptor guanylyl cyclase expressed specifically in olfactory sensory neurons. Proc. Natl. Acad. Sci. USA 92, 3571–3575.PubMedCrossRefGoogle Scholar
  16. Gibson, G., and Torr, S.J. (1999). Visual and olfactory responses of haematophagous Diptera to host stimuli. Med. Vet. Ent. 13, 2–23.CrossRefGoogle Scholar
  17. Gillies, M.T. (1980). The role of carbon dioxide in host-finding by mosquitoes (Diptera: Culicidae): a review. Bull. Entomol. Res. 70, 525–532.CrossRefGoogle Scholar
  18. Graber, M., and Kelleher, S. (1988). Side effects of acetazolamide: the champagne blues. Am. J. Med. 84, 979–980.PubMedCrossRefGoogle Scholar
  19. Guo, D., Zhang, J.J., and Huang, X.-Y. (2009). Stimulation of guanylyl cyclase-D by bicarbonate. Biochemistry 48, 4417–4422.PubMedCrossRefGoogle Scholar
  20. Hallem, E.A., and Sternberg, P.W. (2008). Acute carbon dioxide avoidance in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 105, 8038–8043.PubMedCrossRefGoogle Scholar
  21. Hallem, E.A., Dillman, A.R., Hong, A.V., Zhang, Y., Yano, J.M., DeMarco, S.F., and Sternberg, P.W. (2011a). A sensory code for host seeking in parasitic nematodes. Curr. Biol. 21, 377–383.PubMedCrossRefGoogle Scholar
  22. Hallem, E.A., Spencer, W.C., McWhirter, R.D., Zeller, G., Henz, S.R., Rätsch, G., Miller, D.M., Horvitz, H.R., Sternberg, P.W., and Ringstad, N. (2011b). Receptor-type guanylate cyclase is required for carbon dioxide sensation by Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 108, 254–259.PubMedCrossRefGoogle Scholar
  23. Han, J., and Luo, M. (2010). Loss of CO2 sensing by the olfactory system of CNGA3 knockout mice. Curr. Zool. 56, 793–799.Google Scholar
  24. Hansson, H.P. (1967). Histochemical demonstration of carbonic anhydrase activity. Histochemistry 11, 112–128.PubMedCrossRefGoogle Scholar
  25. Hu, J., Zhong, C., Ding, C., Chi, Q., Walz, A., Mombaerts, P., Matsunami, H., and Luo, M. (2007). Detection of near-atmospheric concentrations of CO2 by an olfactory subsystem in the mouse. Science 317, 953–957.PubMedCrossRefGoogle Scholar
  26. Jones, W.D., Volkan, P.C., Kadow, I.G., and Vosshall, L.B. (2007). Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445, 86–90.PubMedCrossRefGoogle Scholar
  27. Juilfs, D.M., Fülle, H.J., Zhao, A.Z., Houslay, M.D., Garbers, D.L., and Beavo, J.A. (1997). A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanylyl cyclase-D define a unique olfactory signal transduction pathway. Proc. Natl. Acad. Sci. USA 94, 3388–3395.PubMedCrossRefGoogle Scholar
  28. Kain, P., Chakraborty, T.S., Sundaram, S., Siddiqi, O., Rodrigues, V., and Hasan, G. (2008). Reduced odor responses from antennal neurons of G(q)alpha, phospholipase Cbeta, and rdgA mutants in Drosophila support a role for a phospholipid intermediate in insect olfactory transduction. J. Neurosci. 28, 4745–4755.PubMedCrossRefGoogle Scholar
  29. Kain, P., Chandrashekaran, S., Rodrigues, V., and Hasan, G. (2009). Drosophila mutants in phospholipid signaling have reduced olfactory responses as adults and larvae. J. Neurogenet. 23, 303–312.PubMedCrossRefGoogle Scholar
  30. Kleineidam, C., and Roces, F. (2000). Carbon dioxide concentrations and nest ventilation in nests of the leaf-cutting ant Atta vollenweideri. Insectes Soc. 47, 241–248.CrossRefGoogle Scholar
  31. Kwon, J.Y., Dahanukar, A., Weiss, L.A., and Carlson, J.R. (2007). The molecular basis of CO2 reception in Drosophila. Proc. Natl. Acad. Sci. USA 104, 3574–3578.PubMedCrossRefGoogle Scholar
  32. Leinders-Zufall, T., Cockerham, R.E., Michalakis, S., Biel, M., Garbers, D.L., Reed, R.R., Zufall, F., and Munger, S.D. (2007). Contribution of the receptor guanylyl cyclase GC-D to chemosensory function in the olfactory epithelium. Proc. Natl. Acad. Sci. USA 104, 14507–14512.PubMedCrossRefGoogle Scholar
  33. Lu, T., Qiu, Y.T., Wang, G., Kwon, J.Y., Rutzler, M., Kwon, H.-W., Pitts, R.J., van Loon, J., Takken, W., Carlson, J.R., et al. (2007). Odor coding in the maxillary palp of the malaria vector mosquito Anopheles gambiae. Curr. Biol. 17, 1533–1544.PubMedCrossRefGoogle Scholar
  34. Meyer, M.R., Angele, A., Kremmer, E., Kaupp, U.B., and Muller, F. (2000). A cGMP-signaling pathway in a subset of olfactory sensory neurons. Proc. Natl. Acad. Sci. USA 97, 10595–10600.PubMedCrossRefGoogle Scholar
  35. Munger, S.D., Leinders-Zufall, T., McDougall, L.M., Cockerham, R.E., Schmid, A., Wandernoth, P., Wennemuth, G., Biel, M., Zufall, F., and Kelliher, K.R. (2010). An olfactory subsystem that detects carbon disulfide and mediates food-related social learning. Curr. Biol. 20, 1438–1444.PubMedCrossRefGoogle Scholar
  36. Nakagawa, T., and Vosshall, L.B. (2009). Controversy and consensus: noncanonical signaling mechanisms in the insect olfactory system. Curr. Opin. Neurobiol. 19, 284–292.PubMedCrossRefGoogle Scholar
  37. Omer, S.M., and Gillies, M.T. (1971). Loss of response to carbon dioxide in palpectomized female mosquitoes. Entomol. Exp. Appl. 14, 251–252.CrossRefGoogle Scholar
  38. Pinto, M.C., Campbell-Lendrum, D.H., Lozovei, A.L., Teodoro, U., and Davies, C.R. (2001). Phlebotomine sandfly responses to carbon dioxide and human odour in the field. Med. Vet. Ent. 15, 132–139.CrossRefGoogle Scholar
  39. Robertson, H.M., and Kent, L.B. (2009). Evolution of the gene lineage encoding the carbon dioxide receptor in insects. J. Insect Sci. 9, 19.PubMedGoogle Scholar
  40. Robertson, H.M., Warr, C., and Carlson, J.R. (2003). Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 100 (Suppl 2), 14537–14542.PubMedCrossRefGoogle Scholar
  41. Sato, K., Pellegrino, M., Nakagawa, T., Nakagawa, T., Vosshall, L.B., and Touhara, K. (2008). Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452, 1002–1006.PubMedCrossRefGoogle Scholar
  42. Sato, K., Tanaka, K., and Touhara, K. (2011). Sugar-regulated cation channel formed by an insect gustatory receptor. Proc. Natl. Acad. Sci. USA 108, 11680–11685.PubMedCrossRefGoogle Scholar
  43. Scott, K., Brady, R., Cravchik, A., Morozov, P., Rzhetsky, A., Zuker, C.S., and Axel, R. (2001). A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104, 661–673.PubMedCrossRefGoogle Scholar
  44. Seeley, T.D. (1974). Atmospheric carbon dioxide regulation in honey-bee (Apis mellifera) colonies. J. Insect Physiol. 20, 2301–2305.PubMedCrossRefGoogle Scholar
  45. Stange, G. (1974). The influence of a carbonic anhydrase inhibitor on the function of the honeybee antennal CO2-receptors. J. Comp. Phys. A 91, 147–159.CrossRefGoogle Scholar
  46. 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. Phys. A 171, 317–324.CrossRefGoogle Scholar
  47. Stange, G., and Diesendorf, M. (1973). The response of the honeybee antennal CO2-receptors to N2O and Xe. J. Comp. Phys. A 86, 139–158.CrossRefGoogle Scholar
  48. Stange, G., and Stowe, S. (1999). Carbon-dioxide sensing structures in terrestrial arthropods. Microsc. Res. Tech. 47, 416–427.PubMedCrossRefGoogle Scholar
  49. Stange, G., Monro, J., Stowe, S., and Osmond, C. (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, 341–352.CrossRefGoogle Scholar
  50. Steullet, P., and Guerin, P.M. (1992). Perception of breath components by the tropical bont tick, Amblyomma variegatum Fabricius (Ixodidae). I. CO2-excited and CO2-inhibited receptors. J. Comp. Phys. A 170, 665–676.CrossRefGoogle Scholar
  51. Suh, G.S.B., Wong, A.M., Hergarden, A.C., Wang, J.W., Simon, A.F., Benzer, S., Axel, R., and Anderson, D.J. (2004). A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431, 854–859.PubMedCrossRefGoogle Scholar
  52. Sun, L., Wang, H., Hu, J., Han, J., Matsunami, H., and Luo, M. (2009). Guanylyl cyclase-D in the olfactory CO2 neurons is activated by bicarbonate. Proc. Natl. Acad. Sci. USA 106, 2041–2046.PubMedCrossRefGoogle Scholar
  53. Tashian, R.E. (1989). The carbonic anhydrases: widening perspectives on their evolution, expression and function. Bioessays 10, 186–192.PubMedCrossRefGoogle Scholar
  54. Thom, C., Guerenstein, P.G., Mechaber, W.L., and Hildebrand, J.G. (2004). Floral CO2 reveals flower profitability to moths. J. Chem. Ecol. 30, 1285–1288.PubMedCrossRefGoogle Scholar
  55. Turner, S.L., and Ray, A. (2009). Modification of CO2 avoidance behaviour in Drosophila by inhibitory odorants. Nature 461, 277–281.PubMedCrossRefGoogle Scholar
  56. Voskamp, K.E., Everaarts, E., and Den otter, C.J. (1999). Olfactory responses to attractants and repellents in tsetse. Med. Vet. Ent. 13, 386–392.CrossRefGoogle Scholar
  57. Wang, Y.Y., Chang, R.B., and Liman, E.R. (2010). TRPA1 is a component of the nociceptive response to CO2. J. Neurosci. 30, 12958–12963.PubMedCrossRefGoogle Scholar
  58. Weidenmüller, A., Kleineidam, C., and Tautz, J. (2002). Collective control of nest climate parameters in bumblebee colonies. Anim. Behav. 63, 1065–1071.CrossRefGoogle Scholar
  59. Wicher, D., Schäfer, R., Bauernfeind, R., Stensmyr, M.C., Heller, R., Heinemann, S.H., and Hansson, B.S. (2008). Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452, 1007–1011.PubMedCrossRefGoogle Scholar
  60. Yao, C.A., and Carlson, J.R. (2010). Role of G-proteins in odorsensing and CO2-sensing neurons in Drosophila. J. Neurosci. 30, 4562–4572.PubMedCrossRefGoogle Scholar
  61. Young, J.M., Waters, H., Dong, C., Fülle, H.J., and Liman, E.R. (2007). Degeneration of the olfactory guanylyl cyclase D gene during primate evolution. PLoS One 2, e884.PubMedCrossRefGoogle Scholar
  62. Ziesmann, J. (1996). The physiology of an olfactory sensillum of the termite Schedorhinotermes lamanianus: carbon dioxide as a modulator of olfactory sensitivity. J. Comp. Phys. A 179, 123–133.CrossRefGoogle Scholar
  63. Zimmer, M., Gray, J.M., Pokala, N., Chang, A.J., Karow, D.S., Marletta, M.A., Hudson, M.L., Morton, D.B., Chronis, N., and Bargmann, C.I. (2009). Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases. Neuron 61, 865–879.PubMedCrossRefGoogle Scholar

Copyright information

© The Korean Society for Molecular and Cellular Biology and Springer Netherlands 2013

Authors and Affiliations

  1. 1.Department of Biological SciencesKorea Advanced Institute of Science and TechnologyDaejeonKorea

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