, Volume 160, Issue 3, pp 411–420 | Cite as

Effects of air pollution on biogenic volatiles and ecological interactions

  • Quinn S. McFrederick
  • Jose D. Fuentes
  • T’ai Roulston
  • James C. Kathilankal
  • Manuel Lerdau
Concepts, Reviews and Syntheses


Chemical signals play important roles in ecological interactions but are vulnerable to perturbation by air pollution. In polluted air masses, signals may travel shorter distances before being destroyed by chemical reactions with pollutants, thus losing their specificity. To determine which scent-mediated interactions are likely to be affected, we review existing literature to build a picture of what chemicals are commonly found in such interactions and the spatial scales at which interactions occur. We find that pollination, attraction of natural enemies of plant pests, aggregation pheromones, and mate attraction are likely to be affected. We review the scant literature on this topic and extend the hypothesis to include heretofore unexplored interactions. New research should investigate whether air pollution deleteriously affects populations of organisms that rely on scent plumes. Additionally, we need to investigate whether or not breakdown products created by the reaction of signaling chemicals with pollutants can provide usable signals, and whether or not there has been adaptation on the part of scent emitters or receivers to use either breakdown products or more robust chemical signals. The proposed research will necessarily draw on tools from atmospheric science, evolutionary biology, and ecology in furthering our understanding of the ecological implications of how air pollution modifies the scentscape.


Scent plumes Pollinators Ecosystem services Biogenic hydrocarbons Global change 



J.D.F. acknowledges support from the National Science Foundation (grant number ATM-0445012). J.C.K. received support from the Virginia Coastal Reserve (VCR) Long-Term Ecological Research (LTER) to participate in this research (grant number DEB-0621014). The US National Science Foundation supports the VCR-LTER research activities. Thanks to Rob Raguso for help with the historical aspects of this paper and to several anonymous reviewers, as well as Peter Fields, Esther Julier, Stephen Keller, Vijay Panjeti, Dan Sloan. and Dexter Sowell, for comments on an earlier draft. The experiments in this paper comply with the current laws of the country in which they were performed.


  1. Ando T, Inomata S, Yamamoto M (2004) Lepidopteran sex pheromones. In: Schulz S (ed) Chemistry of pheromones and other semiochemicals I, vol 239. Springer, Berlin, pp 51–96CrossRefGoogle Scholar
  2. Angioy AM, Desogus A, Barbarossa IT, Anderson P, Hansson BS (2003) Extreme sensitivity in an olfactory system. Chem Senses 28:279–284PubMedCrossRefGoogle Scholar
  3. Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29:1123–1144PubMedCrossRefGoogle Scholar
  4. Arndt U (1995) Air-pollutants and pheromones—a problem. Chemosphere 30:1023–1031CrossRefGoogle Scholar
  5. Atkinson R (1994) Gas phase tropospheric chemistry of organic compounds. J Phys Chem Ref Data Monogr No 2:216Google Scholar
  6. Blum MS (1996) Semiochemical parsimony in the Arthropoda. Annu Rev Entomol 41:353–374PubMedCrossRefGoogle Scholar
  7. Brennan P, Kendrick KM (2006) Mammalian social odours: attraction and individual recognition. Philos Trans R Soc Lond B 361:2061–2078CrossRefGoogle Scholar
  8. Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274PubMedCrossRefGoogle Scholar
  9. Byers JA (1995) Host tree chemistry affecting colonization in bark beetles. In: Carde RT, Bell WJ (eds) Chemical ecology of insects. Chapman and Hall, New York, pp 154–213Google Scholar
  10. Byers JA (2006) Pheromone component patterns of moth evolution revealed by computer analysis of the pherolist. J Anim Ecol 75:399–407CrossRefGoogle Scholar
  11. Cape JN (2007) Secondary air pollutants and forests—new perspectives. ScientificWorldJournal 7:9–14PubMedCrossRefGoogle Scholar
  12. Carde RT, Haynes KF (2004) Structure of the pheromone communication channel in moths. In: Carde RT, Millar JG (eds) Advances in insect chemical ecology. Cambridge University Press, Cambridge, pp 283–332Google Scholar
  13. Conner WE, Alley KM, Barry JR, Harper AE (2007) Has vertebrate chemesthesis been a selective agent in the evolution of arthropod chemical defenses? Biol Bull 213:267–273PubMedCrossRefGoogle Scholar
  14. Conover MR (2007) Predator–prey dynamics: the role of olfaction. CRC, Boca RatonGoogle Scholar
  15. Dani FR, Jones GR, Destri S, Spencer SH, Turillazzi S (2001) Deciphering the recognition signature within the cuticular chemical profile of paper wasps. Anim Behav 62:165–171CrossRefGoogle Scholar
  16. De Moraes C, Mescher M, Tumlinson J (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580PubMedCrossRefGoogle Scholar
  17. Dicke M, Grostal P (2001) Chemical detection of natural enemies by arthropods: an ecological perspective. Annu Rev Ecol Syst 32:1–23CrossRefGoogle Scholar
  18. do Nascimento RR, Morgan ED (1996) Chemicals involved in the communication system of social insects: their source and methods of isolation and identification, with special emphasis on ants. Quimica Nova 19:156–165Google Scholar
  19. Dobson HEM (1994) Floral volatiles in insect biology. In: Bernays E (ed) Insect–plant interactions, vol 5. CRC, Boca Raton, pp 47–82Google Scholar
  20. Dobson HEM (2006) Relationship between floral fragrance composition and type of pollinator. In: Dudarev N, Pichersky E (eds) Biology of floral scent. CRC, Boca Raton, pp 147–198Google Scholar
  21. Fiore AM, Jacob DJ, Bey I, Yantosca RM, Field BD, Fusco AC, Wilkinson JG (2002) Background ozone over the United States in summer: origin, trend, and contribution to pollution episodes. J Geophys Res Atmos 107 (article 4166)Google Scholar
  22. Frost CJ, Appel M, Carlson JE, De Moraes CM, Mescher MC, Schultz JC (2007) Within-plant signaling via volatiles overcomes vascular constraints on systemic signaling and primes responses against herbivores. Ecol Lett 10:490–498PubMedCrossRefGoogle Scholar
  23. Frost CJ, Mescher MC, Dervinis C, Davis JM, Carlson JE, De Moraes CM (2008) Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytol 180:722–733PubMedCrossRefGoogle Scholar
  24. Fuentes JD, Lerdau M, Atkinson R, Baldocchi D, Bottenheim JW, Ciccioli P, Lamb B, Geron C, Gu L, Guenther A, Sharkey TD, Stockwell W (2000) Biogenic hydrocarbons in the atmospheric boundary layer: a review. Bull Am Meteorol Soc 81:1537–1575CrossRefGoogle Scholar
  25. Fuentes JD, Wang D, Bowling DR, Potosnak M, Monson RK, Goliff WS, Stockwell WR (2007) Biogenic hydrocarbon chemistry within and above a mixed deciduous forest. J Atmos Chem 56:165–185CrossRefGoogle Scholar
  26. Gate IM, McNeill S, Ashmore MR (1995) Effects of air pollution on the searching behaviour of an insect parasitoid. Water Air Soil Pollut 85:1425–1430CrossRefGoogle Scholar
  27. Gohlke R (1959) Time-of-flight mass spectrometry and gas–liquid partition chromatography. Anal Chem 31:535–541CrossRefGoogle Scholar
  28. Gordon DM, Paul RE, Thorpe K (1993) What is the function of encounter patterns in ant colonies? Anim Behav 45:1083–1100CrossRefGoogle Scholar
  29. Heil M (2004) Direct defense or ecological costs: responses of herbivorous beetles to volatiles released by wild lima bean (Phaseolus lunatus). J Chem Ecol 30:1289–1295PubMedCrossRefGoogle Scholar
  30. Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104:5467–5472PubMedCrossRefGoogle Scholar
  31. Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595–631PubMedCrossRefGoogle Scholar
  32. Hurst J, Beynon R (2004) Scent wars: the chemobiology of competitive signalling in mice. Bioessays 26:1288–1298PubMedCrossRefGoogle Scholar
  33. IPCC (2007) Climate change 2007: the physical basis. 4th assessment of the working group 1 of the Intergovernmental Panel on Climate Change. IPCC, GenevaGoogle Scholar
  34. Karban R, Baldwin IT, Baxter KJ, Laue G, Felton GW (2000) Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia 125:66–71CrossRefGoogle Scholar
  35. Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394Google Scholar
  36. Keeling CI, Plettner E, Slessor KN (2004) Hymenopteran semiochemicals. Top Curr Chem 239:133–177CrossRefGoogle Scholar
  37. Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144PubMedCrossRefGoogle Scholar
  38. Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328PubMedCrossRefGoogle Scholar
  39. Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120CrossRefGoogle Scholar
  40. Kost C, Heil M (2006) Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants. J Ecol 94:619–628CrossRefGoogle Scholar
  41. Kurtovic A, Widmer A, Dickson BJ (2007) A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446:542–546PubMedCrossRefGoogle Scholar
  42. Liljefors T, Thelin B, Vanderpers JNC (1984) Structure activity relationships between stimulus molecule and response of a pheromone receptor cell in turnip moth, Agrotis-Segetum—modifications of the acetate group. J Chem Ecol 10:1661–1675CrossRefGoogle Scholar
  43. Marenco A, Gouget H, Nedelec P, Pages J, Karcher F (1994) Evidence of a long-term increase in tropospheric ozone from Pic du Midi data series: consequences: positive radiative forcing. J Geophys Res 99:16617–16632CrossRefGoogle Scholar
  44. McFrederick QS, Kathilankal JC, Fuentes JD (2008) Air pollution modifies floral scent trails. Atmos Environ 42:2336–2348CrossRefGoogle Scholar
  45. Millar JG (2004) Pheromones of true bugs. In: The chemistry of pheromones and other semiochemicals, vol 240. Springer, Berlin, pp 37–84Google Scholar
  46. Mondor EB, Tremblay MN, Awmack CS, Lindroth RL (2004) Divergent pheromone-mediated insect behaviour under global atmospheric change. Glob Chang Biol 10:1820–1824CrossRefGoogle Scholar
  47. Moorhouse J, Yeadon R, Beevor P, Nesbitt B (1969) Method for use in studies of insect chemical communication. Nature 223:1174–1175CrossRefGoogle Scholar
  48. Novotny M, Ma W, Wiesler D, Zidek L (1999) Positive identification of the puberty-accelerating pheromone of the house mouse: the volatile ligands associating with the major urinary protein. Proc R Soc Lond B 266:2017–2022CrossRefGoogle Scholar
  49. Pare PW, Tumlinson JH (1999) Plant volatiles as a defense against insect herbivores. Plant Physiol 121:325–331PubMedCrossRefGoogle Scholar
  50. Pinto DM, Blande JD, Nykanen R, Dong WX, Nerg AM, Holopainen JK (2007a) Ozone degrades common herbivore-induced plant volatiles: does this affect herbivore prey location by predators and parasitoids? J Chem Ecol 33:683–694PubMedCrossRefGoogle Scholar
  51. Pinto DM, Nerg AM, Holopainen JK (2007b) The role of ozone-reactive compounds, terpenes, and green leaf volatiles (GLVs), in the orientation of Cotesia plutellae. J Chem Ecol 33:2218–2228PubMedCrossRefGoogle Scholar
  52. Pinto DM, Tiiva P, Miettinen P, Joutsensaari J, Kokkola H, Nerg AM, Laaksonen A, Holopainen JK (2007c) The effects of increasing atmospheric ozone on biogenic monoterpene profiles and the formation of secondary aerosols. Atmos Environ 41:4877–4887CrossRefGoogle Scholar
  53. Pinto DM, Himanen SJ, Nissinen A, Nerg A-M, Holopainen JK (2008) Host location behavior of Cotesia plutellae Kurdjumov (Hymenoptera: Braconidae) in ambient and moderately elevated ozone in field conditions. Environ Pollut 156:227–231PubMedCrossRefGoogle Scholar
  54. Prinn RG, Huang J, Weiss RF, Cunnold DM, Fraser PJ, Simmonds PG, McCulloch A, Harth C, Salameh P, O’Doherty S, Wang RHJ, Porter L, Miller BR (2001) Evidence for substantial variations of atmospheric hydroxyl radicals in the past two decades. Science 292:1882–1888PubMedCrossRefGoogle Scholar
  55. Raguso RA (2001) Floral scent, olfaction and scent driven foraging behavior. In: Chittka L, Thompson JD (eds) Cognitive ecology of pollination: animal behavior and floral evolution. Cambridge University Press, West Nyack, pp 83–105Google Scholar
  56. Reissell A, Aschmann SM, Atkinson R, Arey J (2002) Products of the OH radical- and O-3-initiated reactions of myrcene and ocimene. J Geophys Res Atmos 107 (article 4138)Google Scholar
  57. Schneider D (1957) Elektrophysiologische untersuchungen von chemo- und mechanorezeptoren der antenne des seidenspinners (Bombyx mori L.). Z Vergl Physiol 40:8–41CrossRefGoogle Scholar
  58. Seinfeld JH, Pandis SN (1996) Atmospheric chemistry and physics: from air pollution to climate change. Wiley, New YorkGoogle Scholar
  59. Theis N (2006) Fragrance of Canada thistle (Cirsium arvense) attracts both floral herbivores and pollinators. J Chem Ecol 32:917–927PubMedCrossRefGoogle Scholar
  60. Theis N, Lerdau M (2003) The evolution of function in plant secondary metabolites. Int J Plant Sci 164:S93–S102CrossRefGoogle Scholar
  61. Turlings TCJ, Loughrin JH, McCall PJ, Rose USR, Lewis WJ, Tumlinson JH (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc Natl Acad Sci USA 92:4169–4174PubMedCrossRefGoogle Scholar
  62. Vander Meer RK, Morel L (1998) Nestmate recognition in ants. In: Vander Meer RK, Bred MD, Espelie K, Winston MI (eds) Pheromone communication in social insects: ants, wasps, bees and termites. Westview Press, Boulder, pp 79–103Google Scholar
  63. Vourc’h G, De Garine-Wichatitsky M, Labbe A, Rosolowski D, Martin JL, Fritz H (2002) Monoterpene effect on feeding choice by deer. J Chem Ecol 28:2411–2427PubMedCrossRefGoogle Scholar
  64. Vuorinen T, Nerg AM, Holopainen JK (2004) Ozone exposure triggers the emission of herbivore-induced plant volatiles, but does not disturb tritrophic signalling. Environ Pollut 131:305–311PubMedCrossRefGoogle Scholar
  65. Wermelinger B (2004) Ecology and management of the spruce bark beetle Ips typographus—a review of recent research. For Ecol Manag 202:67–82CrossRefGoogle Scholar
  66. Williams NH (1983) Floral fragrances as cues in animal behavior. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Scientific and Academic Editions, New York, pp 50–72Google Scholar
  67. Wu SL, Mickley LJ, Jacob DJ, Rind D, Streets DG (2008) Effects of 2000–2050 changes in climate and emissions on global tropospheric ozone and the policy-relevant background surface ozone in the United States. J Geophys Res Atmos 113:D18312Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Quinn S. McFrederick
    • 1
  • Jose D. Fuentes
    • 2
  • T’ai Roulston
    • 2
  • James C. Kathilankal
    • 2
  • Manuel Lerdau
    • 1
    • 2
  1. 1.Department of BiologyUniversity of VirginiaCharlottesvilleUSA
  2. 2.Department of Environmental SciencesUniversity of VirginiaCharlottesvilleUSA

Personalised recommendations