Abstract
Plant volatiles mediate interactions with herbivores, herbivore enemies, and abiotic stresses, but these interactions mostly have been studied with individual isolated plants. It is not yet known how intra- and interspecific plant competition influence volatile emission. In a greenhouse experiment, we investigated the volatile emission by red clover (Trifolium pratense) growing alone, with a conspecific, or with an individual of the naturally co-occurring orchard grass, Dactylis glomerata. The individual and combined effects of above- and below ground plant contact were investigated. When T. pratense grew together with a conspecific, both total and herbivore-induced emission of volatiles was significantly reduced as compared to T. pratense growing with D. glomerata or growing alone. This reduction in emission occurred despite the fact that there was a significant reduction in T. pratense biomass due to competition with D. glomerata. The suppression of T. pratense volatile emission growing next to a conspecific was a general pattern observed for all major herbivore-induced volatiles and independent of whether plants were in contact above ground, below ground, or both above- and below ground. The reduction in volatile emission from plants growing with conspecifics may serve to reduce attack by specialist herbivores and minimize exploitation of herbivore attack information by neighbors.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adams, R. 2007. Identification of essential oil components by Gas Chromatography/Mass Spectrometry. Allured Publishing Corporation, Carol stream, Illinois. 698 p.
Andow, D. A. 1991. Vegetational diversity and arthropod population response. Annu. Rev. Entomol. 36:561–586.
Arimura, G., Shiojiri, K., and Karban, R. 2010. Acquired immunity to herbivory and allelopathy caused by airborne plant emissions. Phytochemistry 71:1642–1649.
Ballare, C. L. 2009. Illuminated behaviour: phytochrome as a key regulator of light foraging and plant anti-herbivore defence. Plant Cell Environ. 32:713–725.
Biedrzycki, M. L., Jilany, T. A., Dudley, S. A., and Bais, H. P. 2010. Root exudates mediate kin recognition in plants. Commun. Integr. Biol. 3:28–35.
Chen, B. J. W., During, H. J., and Anten, N. P. R. 2012. Detect thy neighbor: Identity recognition at the root level in plants. Plant Sci. 195:157–167.
Cipollini, D. 2004. Stretching the limits of plasticity: Can a plant defend against both competitors and herbivores? Ecology 85:28–37.
Cipollini, D. 2007. Consequences of the overproduction of methyl jasmonate on seed production, tolerance to defoliation and competitive effect and response of Arabidopsis thaliana. New Phytol. 173:146–153.
Crawley, M. J. 1989. Insect herbivores and plant-population dynamics. Annu. Rev. Entomol. 34:531–564.
Crawley, M. J. 2007. The R Book. John Wiley & Sons, Ltd, New York.
Darwin, C. 1859. The Origin of Species. John Murray, London.
Dicke, M. and Baldwin, I. T. 2010. The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci. 15:167–175.
Dudareva, N., Negre, F., Nagegowda, D. A., and Orlova, I. 2006. Plant volatiles: Recent advances and future perspectives. Crit. Rev. Plant Sci. 25:417–440.
Farrer, E. C. and Goldberg, D. E. 2011. Patterns and mechanisms of conspecific and heterospecific interactions in a dry perennial grassland. J. Ecol. 99:265–276.
Fontana, A., Reichelt, M., Hempel, S., Gershenzon, J., and Unsicker, S. B. 2009. The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata. J. Chem. Ecol. 35:833–843.
Fortner, A. M. and Weltzin, J. F. 2007. Competitive hierarchy for four common old-field plant species depends on resource identity and availability. J. Torrey Bot. Soc. 134:166–176.
Frost, C. J., Appel, M., Carlson, J. E., de Moraes, C. M., Mescher, M. C., and Schultz, J. C. 2007. Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol. Lett. 10:490–498.
Goldberg, D. E. and Barton, A. M. 1992. Patterns and consequences of interspecific competition in natural communities: a review of field experiments with plants. Am. Nat. 139:771–801.
Halitschke, R., Stenberg, J. A., Kessler, D., Kessler, A., and Baldwin, I. T. 2008. Shared signals - ‘alarm calls’ from plants increase apparency to herbivores and their enemies in nature. Ecol. Lett. 11:24–34.
Hautier, Y., Niklaus, P. A., and Hector, A. 2009. Competition for light causes plant biodiversity loss after eutrophication. Science 324:636–638.
Heil, M. and Karban, R. 2010. Explaining evolution of plant communication by airborne signals. Trends Ecol. Evol. 25:137–144.
Heil, M. and Silva Bueno, J. C. 2007. Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc. Natl. Acad. Sci. U. S. A. 104:5467–5472.
Herms, D. A. and Mattson, W. J. 1992. The dilemma of plants - to grow or defend. Q. Rev. Biol. 67:283–335.
Himanen, S. J., Blande, J. D., Klemola, T., Pulkkinen, J., Heijari, J., and Holopainen, J. K. 2010. Birch (Betula spp.) leaves adsorb and re-release volatiles specific to neighbouring plants - a mechanism for associational herbivore resistance? New Phytol. 186:722–732.
Holopainen, J. K. and Gershenzon, J. 2010. Multiple stress factors and the emission of plant VOCs. Trends Plant Sci. 15:176–184.
Joulain, D. and König, W. A. 1998. The Atlas of Spectral Data of Sesquiterpene Hydrocarbons. EB-Verlag, Hamburg.
Kalberer, N. M., Turlings, T. C. J., and Rahier, M. 2001. Attraction of a leaf beetle (Oreina cacaliae) to damaged host plants. J. Chem. Ecol. 27:647–661.
Karban, R. and Baldwin, I. T. 1997. Induced Responses to Herbivory: The University of Chicago Press. 319 pp.
Karban, R. and Shiojiri, K. 2009. Self-recognition affects plant communication and defense. Ecol. Lett. 12:502–506.
Karban, R., Shiojiri, K., Ishizaki, S., Wetzel, W. C., and Evans, R. Y. 2013. Kin recognition affects plant communication and defense. Proc. Royal Soc. B. 280:20123062.
Keddy, P. A. 2001. Competition. Population and Community Biology Series, vol. 26. Kluwer Academic Publishers, Dordrecht, p 576.
Kegge, W. and Pierik, R. 2010. Biogenic volatile organic compounds and plant competition. Trends Plant Sci. 15:126–132.
Kigathi, R. N., Unsicker, S. B., Reichelt, M., Kesselmeier, J., Gershenzon, J., and Weisser, W. W. 2009. Emission of volatile organic compounds after herbivory from Trifolium pratense (L.) under laboratory and field conditions. J. Chem. Ecol. 35:1335–1348.
Lepik, A., Abakumova, M., Zobel, K., and Semchenko, M. 2012. Kin recognition is density-dependent and uncommon among temperate grassland plants. Funct. Ecol. 26:1214–1220.
Ninkovic, V. 2003. Volatile communication between barley plants affects biomass allocation. J. Exp. Bot. 54:1931–1939.
Novoplansky, A. 2009. Picking battles wisely: plant behaviour under competition. Plant Cell Environ. 32:726–741.
Ormeno, E., Bousquet-Melou, A., Mevy, J.-P., Greff, S., Robles, C., Bonin, G., and Fernandez, C. 2007a. Effect of intraspecific competition and substrate type on terpene emissions from some Mediterranean plant species. J. Chem. Ecol. 33:277–286.
Ormeno, E., Fernandez, C., and Mevy, J. P. 2007b. Plant coexistence alters terpene emission and content of Mediterranean species. Phytochemistry 68:840–852.
Pare, P. W. and Tumlinson, J. H. 1999. Plant volatiles as a defense against insect herbivores. Plant Physiol. 121:325–331
Pierik, R., Visser, E. J. W., de Kroon, H., and Voesenek, L. 2003. Ethylene is required in tobacco to successfully compete with proximate neighbours. Plant Cell Environ. 26:1229–1234.
Root, R. B. 1973. Organization of a plant-arthropod association in simple and diverse habitats - fauna of collards (Brassica-oleracea). Ecol. Monogr. 43:95–120.
Runyon, J. B., Mescher, M. C., and de Moraes, C. M. 2006. Volatile chemical cues guide host location and host selection by parasitic plants. Science 313:1964–1967.
Scanion, J. T. and Willis, D. E. 1985. Calculation of flame ionization detector relative response factors using the effective carbon number concept. J. Chromatogr. Sci. 23:333–340.
Tilman, D. 1994. Competition and biodiversity in spatially structured habitats. Ecology 75:2–16.
Unsicker, S. B., Kunert, G., and Gershenzon, J. 2009. Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr. Opin. Plant Biol. 12:479–485.
van Dam, N. M., Hadwich, K., and Baldwin, I. T. 2000. Induced responses in Nicotiana attenuata affect behavior and growth of the specialist herbivore Manduca sexta. Oecologia 122:371–379.
Walters, D. and Heil, M. 2007. Costs and trade-offs associated with induced resistance. Physiol. Mol. Plant Pathol. 71:3–17.
Wilson, J. B. 1988. Shoot competition and root competition. J. Appl. Ecol. 25:279–296.
Acknowledgments
This research was funded by the International Max Planck Research School in Jena and the Max Planck Society. Wolfgang Weisser was supported by the Deutsche Forschungsgemeinschaft, DFG (FOR 456). We thank Beate Rothe, Isabel Georgy, Simone Spreer, Birgit Arnold, Andreas Weber, and the greenhouse team for help with the experiment and plant rearing, Michael Reichelt and Tobias Köllner for assistance with chemical analysis, Ian Baldwin for comments on an earlier draft, and Jens Schumacher for advice on the statistical analyses.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 2118 kb)
Rights and permissions
About this article
Cite this article
Kigathi, R.N., Weisser, W.W., Veit, D. et al. Plants Suppress Their Emission of Volatiles When Growing with Conspecifics. J Chem Ecol 39, 537–545 (2013). https://doi.org/10.1007/s10886-013-0275-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-013-0275-2