Changing odour landscapes: the effect of anthropogenic volatile pollutants on plant–pollinator olfactory communication

Functional Ecology

Volumn 31, Issue 1, 2017, Pages 56-64

  Jürgens, Andreas ^a,b   Bischoff, Mascha ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF KWAZULU NATAL   (South Africa)

Author keywords

air pollution; floral volatiles; flowering communities; olfactory signalling; plant insect communication

Indexed keywords

AGRICULTURAL PRACTICE; ANTHROPOGENIC EFFECT; ANTHROPOGENIC SOURCE; ATMOSPHERIC POLLUTION; CHEMICAL POLLUTANT; FLOWERING; ODOR; OLFACTORY CUE; PLANT-INSECT INTERACTION; PLANT-POLLINATOR INTERACTION; POLLUTANT SOURCE; REACTIVE OXYGEN SPECIES; RISK ASSESSMENT; SIGNALING; URBANIZATION; VOLATILE ORGANIC COMPOUND;

ANIMALIA; HEXAPODA; MAGNOLIOPHYTA;

EID: 85053361681     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12774     Document Type: Review

References (68)

1. Atema, J. (1996) Eddy chemotaxis and odor landscapes: exploration of nature with animal sensors. Biological Bulletin, 191, 129–138.
2. Atkinson, R. & Arey, J. (2003a) Gas-phase tropospheric chemistry of biogenic volatile organic compounds: a review. Atmospheric Environment, 37, 197–219.
3. Atkinson, R. & Arey, J. (2003b) Atmospheric degradation of volatile organic compounds. Chemical Reviews, 103, 4605–4638.
4. Baldwin, I.T., Halitschke, R., von Paschold, A., Dahl, C.C. & Preston, C.A. (2006) Volatile signaling in plant-plant interactions: ‘Talking trees’ In the genomics era. Science, 311, 812–815.
5. Beauchamp, J., Wisthaler, A., Hansel, A., Kleist, E., Miebach, M., Niinemets, Ü. et al. (2005) Ozone induced emissions of biogenic VOC from tobacco: relations between ozone uptake and emission of LOX products. Plant, Cell & Environment, 28, 1334–1343.
6. Beyaert, I. & Hilker, M. (2014) Plant odour plumes as mediators of plant–insect interactions. Biological Reviews, 89, 68–81.
7. Bidstrup, M. (2015) Life cycle thinking in impact assessment - Current practice and LCA gains. Environmental Impact Assessment Review, 54, 72–79.
8. Bischoff, M., Raguso, R.A., Jürgens, A. & Campbell, D.R. (2015) Context-dependent reproductive isolation mediated by floral scent and color. Evolution, 69, 1–13.
9. Blande, J.D., Holopainen, J.K. & Li, T. (2010) Air pollution impedes plant-to-plant communication by volatiles. Ecology Letters, 13, 1172–1181.
10. Blande, J.D., Holopainen, J.K. & Niinemets, Ü. (2014) Plant volatiles in polluted atmospheres: stress responses and signal degradation. Plant, Cell and Environment, 37, 1892–1904.
11. Blande, J.D., Tiiva, P., Oksanen, E. & Holopainen, J.K. (2007) Emission of herbivore-induced volatile terpenoids from two hybrid aspen (Populus tremula x tremuloides) clones under ambient and elevated ozone concentrations in the field. Global Change Biology, 13, 2538–2550.
12. Broadgate, W.J., Liss, P.S. & Penkett, S.A. (1997) Seasonal emissions of isoprene and other reactive hydrocarbon gases from the ocean. Geophysical Research Letters, 24, 2675–2678.
13. Burkle, L.A., Marlin, J.C. & Knight, T.M. (2013) Plant-pollinator interactions over 120 years: loss of species, co-occurrence, and function. Science, 339, 1611–1615.
14. Chittka, L. & Raine, N.E. (2006) Recognition of flowers by pollinators. Current Opinion in Plant Biology, 9, 428–435.
15. CML (2015) Database CML-IA v4.5. Institute of Environmental Sciences, Leiden University, Leiden, April 2015. http://cml.leiden.edu/software/data-cmlia.html.
16. Dicke, M. & Baldwin, I.T. (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the “cry for help”. Trends in Plant Science, 15, 167–175.
17. Dötterl, S., Glück, U., Jürgens, A., Woodring, J. & Aas, G. (2014) Floral reward, advertisement and attractiveness to honey bees in dioecious Salix caprea. PLoS ONE, 9, e93421.
18. Dötterl, S., Vater, M., Rupp, T. & Held, A. (2016) Ozone differentially affects perception of volatiles in western honey bees. Journal of Chemical Ecology, 42, 486–489.
19. Endler, J.A. (1992) Signals, signal conditions, and the direction of evolution. The American Naturalist, 139, S125–S153.
20. Farre-Armengol, G., Filella, I., Llusia, J. & Peñuelas, J. (2013) Floral volatile organic compounds: between attraction and deterrence of visitors under global change. Perspectives in Plant Ecology, Evolution and Systematics, 15, 56–67.
21. Farré-Armengol, G., Peñuelas, J., Li, T., Yli-Pirilä, P., Filella, I., Llusia, J. et al. (2016) Ozone degrades floral scent and reduces pollinator attraction to flowers. New Phytologist, 209, 152–160.
22. Fontaine, C., Dajoz, I., Meriguet, J. & Loreau, M. (2006) Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. PLoS Biology, 4, e1.
23. Fuentes, J.D., Lerdau, M., Atkinson, R., Baldocchi, D., Bottenheim, J.W., Ciccioli, P. et al. (2000) Biogenic hydrocarbons in the atmospheric boundary layer: a review. Bulletin of the American Meteorological Society, 81, 1537–1575.
24. Galen, C., Kaczorowski, R., Todd, S.L., Geib, J. & Raguso, R.A. (2011) Dosage-dependent impacts of a floral volatile compound on pollinators, larcenists, and the potential for floral evolution in the Alpine Skypilot Polemonium viscosum. The American Naturalist, 177, 258–272.
25. Gentner, D.R., Ormeño, E., Fares, S., Ford, T.B., Weber, R., Park, J.-H. et al. (2014) Emissions of terpenoids, benzenoids, and other biogenic gas-phase organic compounds from agricultural crops and their potential implications for air quality. Atmospheric Chemistry and Physics, 14, 5393–5413.
26. Gimeno, B.S., Bermejo, V., Sanz, J., De la Torre, D. & Gil, J.M. (2004) Assessment of the effects of ozone exposure and plant competition on the reproductive ability of three therophytic clover species from Iberian pastures. Atmospheric Environment, 38, 2295–2303.
27. Girling, R.D., Lusebrink, I., Farthing, E., Newman, T.A. & Poppy, G.M. (2013) Diesel exhaust rapidly degrades floral odours used by honeybees. Scientific Reports, 3, 2279
28. Guenther, A. (1997) Seasonal and spatial variations in natural volatile organic compound emissions. Ecological Applications, 7, 34–45.
29. Guenther, A., Hewitt, C.N., Erickson, D., Fall, R., Geron, C., Graedel, T. et al. (1995) A global-model of natural volatile organic-compound emissions. Journal of Geophysical Research, 100, 8873–8892.
30. Guenther, A., Karl, T., Harley, P., Wiedinmyer, C. & Palmer, P.I. (2006) Estimates of global terrestrial isoprene emissions using MEGAN (Model of Emissions of Gases and Aerosols from Nature). Atmospheric Chemistry and Physics Discussions, 6, 107–173.
31. Hansson, B. & Stensmyr, M.C. (2011) Evolution of insect olfaction. Neuron, 72, 698–711.
32. Hayes, F., Jones, M.L.M., Mills, G. & Ashmore, M. (2007) Meta-analysis of the relative sensitivity of semi-natural vegetation species to ozone. Environmental Pollution, 146, 754–762.
33. Heil, M. & Karban, R. (2010) Explaining evolution of plant communication by airborne signals. Trends in Ecology and Evolution, 25, 137–144.
34. Holopainen, J.K. & Gershenzon, J. (2010) Multiple stress factors and the emission of plant VOCs. Trends in Plant Science, 15, 176–184.
35. International Organization for Standardization (ISO) (2006) 14040 — Environmental Management — Life Cycle Assessment — Principles and Framework. International Organization for Standardization, Geneva, Switzerland.
36. Jepsen, M.R., Kuemmerle, T., Müller, D., Erb, K., Verburg, P.H., Haberl, H. et al. (2015) Transitions in European land-management regimes between 1800 and 2010. Land Use Policy, 49, 53–64.
37. Jürgens, A., Glück, U., Aas, G. & Dötterl, S. (2014) Diel fragrance pattern correlates with olfactory preferences of diurnal and nocturnal flower visitors in Salix caprea (Salicaceae). Botanical Journal of the Linnean Society, 175, 624–640.
38. Kesselmeier, J. & Staudt, M. (1999) Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. Journal of Atmospheric Chemistry, 33, 23–88.
39. Kessler, A., Halitschke, R. & Poveda, K. (2011) Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant–pollinator interactions. Ecology, 92, 1769–1780.
40. Knudsen, J.T., Eriksson, R., Gershenzon, J. & Stahl, B. (2006) Diversity and distribution of floral scent. Botanical Review, 72, 1–120.
41. Kremen, C., Williams, N.M. & Thorp, R.W. (2002) Crop pollination from native bees at risk from agricultural intensification. Proceedings of the National Academy of Sciences of the United States of America, 99, 16812–16816.
42. Laothawornkitkul, J., Taylor, J.E., Paul, N.D. & Hewitt, C.N. (2009) Biogenic volatile organic compounds in the Earth system. New Phytologist, 183, 27–51.
43. Li, T. & Blande, J.D. (2015) Associational susceptibility in broccoli: mediated by plant volatiles, impeded by ozone. Global Change Biology, 21, 1993–2004.
44. Lürling, M. & Scheffer, M. (2007) Info-disruption: pollution and the transfer of chemical information between organisms. Trends in Ecology and Evolution, 22, 374–379.
45. McFrederick, Q.S., Kathilankal, J.C. & Fuentes, J.D. (2008) Air pollution modifies floral scent trails. Atmospheric Environment, 42, 2336–2348.
46. McFrederick, Q.S., Fuentes, J.D., Roulston, T., Kathilankal, J.C. & Lerdau, M. (2009) Effects of air pollution on biogenic volatiles and ecological interactions. Oecologia, 160, 411–420.
47. Nevitt, G.A., Veit, R.R. & Kareiva, P. (1995) Dimethyl sulphide as a foraging cue for Antarctic procellariiform seabirds. Nature, 376, 680–682.
48. Oderbolz, D.C., Aksoyoglu, S., Keller, J., Barmpadimos, I., Steinbrecher, R., Skjøth, C.A. et al. (2013) A comprehensive emission inventory of biogenic volatile organic compounds in Europe: improved seasonality and land-cover. Atmospheric Chemistry and Physics, 13, 1689–1712.
49. Ollerton, J., Winfree, R. & Tarrant, S. (2011) How many flowering plants are pollinated by animals? Oikos, 120, 321–326.
50. Paoletti, E., Marco, A., Beddows, D., Harrison, R. & Manning, W. (2014) Ozone levels in European and USA cities are increasing more than at rural sites, while peak values are decreasing. Environmental Pollution, 192, 295–299.
51. Patrício-Roberto, G.B. & Campos, M.J.O. (2014) Aspects of landscape and pollinators—what is important to bee conservation? Diversity, 6, 158–175.
52. Picot, S.D., Watson, J.J. & Jones, J.W. (1992) A global inventory of volatile organic compound emissions from anthropogenic sources. Journal of Geophysical Research, 97, 9897–9912.
53. Pinto, D.M., Nerg, A.M. & Holopainen, J.K. (2007b) The role of ozone-reactive compounds, terpenes, and green leaf volatiles (GLVs), in the orientation of Cotesia plutellae. Journal of Chemical Ecology, 33, 2218–2228.
54. Pinto, D.M., Blande, J.D., Nykänen, R., Dong, W.-X., Nerg, A.-M. & Holopainen, J.K. (2007a) Ozone degrades common herbivore-induced plant volatiles: does this affect herbivore prey location by predators and parasitoids? Journal of Chemical Ecology, 33, 683–694.
55. 3) polluted atmospheres: the ecological effects. Journal of Chemical Ecology, 36, 22–34.
56. Raguso, R.A. (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annual Review of Ecology Evolution and Systematics, 39, 549–569.
57. Riffell, J.A., Shlizerman, E., Sanders, E., Abrell, L., Medina, B., Hinterwirth, A.J. et al. (2014) Flower discrimination by pollinators in a dynamic chemical environment. Science, 344, 1515–1518.
58. Schaab, G., Steinbrecher, R., Lacaze, B. & Lenz, R. (2000) Assessment of long-term vegetation changes on potential isoprenoid emission for a Mediterranean-type ecosystem in France. Journal of Geophysical Research-Atmospheres, 105, 28863–28873.
59. Schiestl, F.P. (2015) Ecology and evolution of floral volatile mediated information transfer in plants. New Phytologist, 206, 571–577.
60. Schröder, R. & Hilker, M. (2008) The relevance of background odor in resource location by insects: a behavioral approach. BioScience, 58, 308–316.
61. Shiojiri, K., Ozawa, R., Matsui, K., Sabelis, M.W. & Takabayashi, J. (2012) Intermittent exposure to traces of green leaf volatiles triggers a plant response. Scientific Reports, 2, 378.
62. Van der Niet, T., Jürgens, A. & Johnson, S.D. (2010) Pollinators, floral morphology and scent chemistry in the southern African orchid genus Schizochilus. South African Journal of Botany, 76, 726–738.
63. Wilson, J.K., Kessler, A. & Woods, H.A. (2015) Noisy communication via airborne infochemicals. BioScience, 65, 667–677.
64. Wright, G.A. & Schiestl, F.P. (2009) The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Functional Ecology, 23, 841–851.
65. Wright, G.A., Thomson, M.G. & Smith, B.H. (2005) Odour concentration affects odour identity in honeybees. Proceedings of the Royal Society of London B: Biological Sciences, 272, 2417–2422.
66. Wright, G.A., Lutmerding, A., Dudareva, N. & Smith, B.H. (2005) Intensity and the ratios of compounds in the scent of snapdragon flowers affect scent discrimination by honey bees (Apis mellifera). Journal of Comparative Physiology A., 191, 105–114.
67. Yuan, J.S., Himanen, S.J., Holopainen, J.K., Chen, F. & Stewart, C.N. (2009) Smelling global climate change: mitigation of function for plant volatile organic compounds. Trends in Ecology & Evolution, 24, 323–331.
68. Zielinska, B., Sagebiel, J., McDonald, J.D., Whitney, K. & Lawson, D.R. (2004) Emission rates and comparative chemical composition from selected in-use diesel and gasoline-fuelled vehicles. Journal of the Air and Waste Management Association, 54, 1138–1150.