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.
Similar content being viewed by others
References
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.
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.
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.
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.
Benton, A.H., and Lee, S.Y. (1965). Sensory reactions of Siphonaptera in relation to host-finding. Am. Midland Nat. 119–125.
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.
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.
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.
Buehlmann, C., Hansson, B.S., and Knaden, M. (2012). Path integration controls nest-plume following in desert ants. Curr. Biol. 22, 645–649.
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.
de Bruyne, M., Foster, K., and Carlson, J.R. (2001). Odor coding in the Drosophila antenna. Neuron 30, 537–552.
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.
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.
Fallis, A.M., and Raybould, J.N. (1975). Response of two African simuliids to silhouettes and carbon dioxide. J. Med. Ent. 12, 349–351.
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.
Gibson, G., and Torr, S.J. (1999). Visual and olfactory responses of haematophagous Diptera to host stimuli. Med. Vet. Ent. 13, 2–23.
Gillies, M.T. (1980). The role of carbon dioxide in host-finding by mosquitoes (Diptera: Culicidae): a review. Bull. Entomol. Res. 70, 525–532.
Graber, M., and Kelleher, S. (1988). Side effects of acetazolamide: the champagne blues. Am. J. Med. 84, 979–980.
Guo, D., Zhang, J.J., and Huang, X.-Y. (2009). Stimulation of guanylyl cyclase-D by bicarbonate. Biochemistry 48, 4417–4422.
Hallem, E.A., and Sternberg, P.W. (2008). Acute carbon dioxide avoidance in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 105, 8038–8043.
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.
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.
Han, J., and Luo, M. (2010). Loss of CO2 sensing by the olfactory system of CNGA3 knockout mice. Curr. Zool. 56, 793–799.
Hansson, H.P. (1967). Histochemical demonstration of carbonic anhydrase activity. Histochemistry 11, 112–128.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Nakagawa, T., and Vosshall, L.B. (2009). Controversy and consensus: noncanonical signaling mechanisms in the insect olfactory system. Curr. Opin. Neurobiol. 19, 284–292.
Omer, S.M., and Gillies, M.T. (1971). Loss of response to carbon dioxide in palpectomized female mosquitoes. Entomol. Exp. Appl. 14, 251–252.
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.
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.
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.
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.
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.
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.
Seeley, T.D. (1974). Atmospheric carbon dioxide regulation in honey-bee (Apis mellifera) colonies. J. Insect Physiol. 20, 2301–2305.
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.
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.
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.
Stange, G., and Stowe, S. (1999). Carbon-dioxide sensing structures in terrestrial arthropods. Microsc. Res. Tech. 47, 416–427.
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.
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.
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.
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.
Tashian, R.E. (1989). The carbonic anhydrases: widening perspectives on their evolution, expression and function. Bioessays 10, 186–192.
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.
Turner, S.L., and Ray, A. (2009). Modification of CO2 avoidance behaviour in Drosophila by inhibitory odorants. Nature 461, 277–281.
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.
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.
Weidenmüller, A., Kleineidam, C., and Tautz, J. (2002). Collective control of nest climate parameters in bumblebee colonies. Anim. Behav. 63, 1065–1071.
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.
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.
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.
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.
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.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Jones, W. Olfactory carbon dioxide detection by insects and other animals. Mol Cells 35, 87–92 (2013). https://doi.org/10.1007/s10059-013-0035-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10059-013-0035-8