Abstract
Insect herbivore enemies such as parasitoids and predators are important in controlling herbivore pests. From agricultural systems we know that land-use intensification can negatively impact biological control as an important ecosystem service. The aim of our study was to investigate the importance of management regime for natural enemy pressure and biological control possibilities in forests dominated by European beech. We hypothesize that the volatile blend released from herbivore-infested beech trees functions as a signal, attracting parasitoids and herbivore enemies. Furthermore, we hypothesize that forest management regime influences the composition of species attracted by these herbivore-induced beech volatiles. We installed flight-interception traps next to Lymantria dispar caterpillar-infested young beech trees releasing herbivore-induced volatiles and next to non-infested control trees. Significantly more parasitoids were captured next to caterpillar-infested trees compared to non-infested controls, irrespective of forest type. However, the composition of the trophic guilds in the traps did vary in response to forest management regime. While the proportion of chewing insects was highest in non-managed forests, the proportion of sucking insects peaked in forests with low management and of parasitoids in young, highly managed, forest stands. Neither the number of naturally occurring beech saplings nor herbivory levels in the proximity of our experiment affected the abundance and diversity of parasitoids caught. Our data show that herbivore-induced beech volatiles attract herbivore enemies under field conditions. They further suggest that differences in the structural complexity of forests as a consequence of management regime only play a minor role in parasitoid activity and thus in indirect tree defense.
Similar content being viewed by others
References
Bernasconi Ockroy ML et al (2001) Response of natural populations of predators and parasitoids to artificially induced volatile emissions in maize plants (Zea mays L.). Agric For Entomol 3:201–209
Bianchi FJ, Booij CJ, Tscharntke T (2006) Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc Biol Sci 273:1715–1727
Boch S et al (2013) High plant species richness indicates management-related disturbances rather than the conservation status of forests. Basic Appl Ecol 14:496–505
Böhme J (2005) Die Käfer Mitteleuropas, Band K-Katalog: Faunistische Übersicht. Elsevier, Spektrum, Heroldsberg
Braasch J, Wimp GM, Kaplan I (2012) Testing for phytochemical synergism: arthropod community responses to induced plant volatile blends across crops. J Chem Ecol 38:1264–1275
Brunet J, Fritz Ö, Richnau G (2010) Biodiversity in European beech forests—a review with recommendations for sustainable forest management. Ecol Bull 53:77–94
Büchel K, Austel N, Mayer M, Gershenzon J, Fenning TM, Meiners T (2013) Smelling the tree and the forest: elm background odours affect egg parasitoid orientation to herbivore induced terpenoids. BioControl 59:29–43
Büchel K et al (2011) How plants give early herbivore alert: Volatile terpenoids attract parasitoids to egg-infested elms. Basic Appl Ecol 12:403–412
Carroll MJ, Schmelz EA, Meagher RL, Teal PEA (2006) Attraction of Spodoptera frugiperda larvae to volatiles from herbivore-damaged maize seedlings. J Chem Ecol 32:1911–1924
Chaplin-Kramer R, O’Rourke ME, Blitzer EJ, Kremen C (2011) A meta-analysis of crop pest and natural enemy response to landscape complexity. Ecol Lett 14:922–932
Clavijo McCormick A, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17:303–310
Clavijo McCormick A et al (2014) Herbivore-induced volatile emission in black poplar: regulation and role in attracting herbivore enemies. Plant Cell Environ 37:1909–1923
Danner H et al (2011) Four terpene synthases produce major compounds of the gypsy moth feeding-induced volatile blend of Populus trichocarpa. Phytochemistry 72:897–908
Degen T, Bakalovic N, Bergvinson D, Turlings TC (2012) Differential performance and parasitism of caterpillars on maize inbred lines with distinctly different herbivore-induced volatile emissions. PLoS ONE 7:e47589
Dicke M (2009) Behavioural and community ecology of plants that cry for help. Plant, Cell Environ 32:654–665
Didham RK, Ghazoul J, Stork NE, Davis AJ (1996) Insects in fragmented forests: a functional approach. Trends Ecol Evol 11:255–260
Dindorf T et al (2006) Significant light and temperature dependent monoterpene emissions from European beech (Fagus sylvatica L.) and their potential impact on the European volatile organic compound budget. J Geophys Res Atmos 111:D16305
Dodd LE et al (2012) Forest structure affects trophic linkages: how silvicultural disturbance impacts bats and their insect prey. For Ecol Manage 267:262–270
Dormann CF (2007) Promising the future? Global change projections of species distributions. Basic Appl Ecol 8:387–397
Fischer M et al (2010) Implementing large-scale and long-term functional biodiversity research: the Biodiversity Exploratories. Basic Appl Ecol 11:473–485
Fontana A, Reichelt M, Hempel S, Gershenzon J, Unsicker SB (2009) The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. J Chem Ecol 35:833–843
Ghirardo A, Heller W, Fladung M, Schnitzler JP, Schroeder H (2012) Function of defensive volatiles in pedunculate oak (Quercus robur) is tricked by the moth Tortrix viridana. Plant Cell Environ 35:2192–2207
Gladbach DJ, Holzschuh A, Scherber C, Thies C, Dormann CF, Tscharntke T (2011) Crop–noncrop spillover: arable fields affect trophic interactions on wild plants in surrounding habitats. Oecologia 166:433–441
Goodwin BJ, Fahrig L (2002) Effect of landscape structure on the movement behaviour of a specialized goldenrod beetle, Trirhabda borealis. Can J Zool 80:24–35
Gossner MM (2009) Light intensity affects spatial distribution of Heteroptera in deciduous forests. Eur J Entomol 106:241–252
Haddad NM, Crutsinger GM, Gross K, Haarstad J, Tilman D (2011) Plant diversity and the stability of foodwebs. Ecol Lett 14:42–46
Halitschke R, Stenberg JA, Kessler D, Kessler A, Baldwin IT (2008) Shared signals—‘alarm calls’ from plants increase apparency to herbivores and their enemies in nature. Ecol Lett 11:24–34
Hannunen S (2002) Vegetation architecture and redistribution of insects moving on the plant surface. Ecol Model 155:149–157
Hare JD (2011) Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu Rev Entomol 56:161–180
Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61
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 104:5467–5472
Herbst C et al (2013) Land use intensification in grasslands: higher trophic levels are more negatively affected than lower trophic levels. Entomol Exp Appl 147:269–281
Hilszczanski J et al (2005) Parasitoids (Hymenoptera, Ichneumonoidea) of saproxylic beetles are affected by forest successional stage and dead wood characteristics in boreal spruce forest. Biol Conserv 126:456–464
Holzke C, Dindorf T, Kesselmeier J, Kuhn U, Koppmann R (2006) Terpene emissions from European beech (Fagus sylvatica L.): pattern and emission behaviour over two vegetation periods. J Atmos Chem 55:81–102
Jäkel A, Roth M (2004) Conversion of single-layered Scots pine monocultures into close-to-nature mixed hardwood forests: effects on parasitoid wasps as pest antagonists. Eur J Forest Res 123:203–212
Jonsson M, Buckley HL, Case BS, Wratten SD, Hale RJ, Didham RK (2012) Agricultural intensification drives landscape-context effects on host–parasitoid interactions in agroecosystems. J Appl Ecol 49:706–714
Joó É et al (2010) Variation in biogenic volatile organic compound emission pattern of Fagus sylvatica L. due to aphid infection. Atmos Environ 44:227–234
Joulain D, König WA (1998) The atlas of spectral data of sesquiterpene hydrocarbons. EB-Verlag, Hamburg
Kigathi RN, Weisser WW, Veit D, Gershenzon J, Unsicker SB (2013) Plants suppress their emission of volatiles when growing with conspecifics. J Chem Ecol 39:537–545
Klein AM, Steffan DI, Tscharntke T (2002) Predator–prey ratios on cocoa along a land-use gradient in Indonesia. Biodivers Conserv 11:683–693
Klemola T, Ammunét T, Andersson T, Klemola N, Ruohomäki K (2012) Larval parasitism rate increases in herbivore-damaged trees: a field experiment with cyclic birch feeding moths. Oikos 121:1525–1531
Lambin EF et al (2001) The causes of land-use and land-cover change: moving beyond the myths. Glob Environ Change Hum Policy Dimens 11:261–269
Lange M et al (2011) The impact of forest management on litter-dwelling invertebrates: a subtropical–temperate contrast. Biodivers Conserv 20:2133–2147
Letourneau DK, Bothwell SG, Stireman JO (2012) Perennial habitat fragments, parasitoid diversity and parasitism in ephemeral crops. J Appl Ecol 49:1405–1416
Meiners T, Obermaier E (2004) Hide and seek on two spatial scales—vegetation structure effects herbivore oviposition and egg parasitism. Basic Appl Ecol 5:87–94
Mulder C et al (2011) A belowground perspective on Dutch agroecosystems: how soil organisms interact to support ecosystem services. In: Woodward G (ed) Advances in ecological research, vol 44. Elsevier, San Diego, pp 277–357
Mumm R, Dicke M (2010) Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Can J Zool 88:628–667
Obermaier E, Heisswolf A, Poethke HJ, Randlkofer B, Meiners T (2008) Plant architecture and vegetation structure: two ways for insect herbivores to escape parasitism. Eur J Entomol 105:233–240
Paillet Y et al (2010) Biodiversity differences between managed and unmanaged forests: meta-analysis of species richness in Europe. Conserv Biol 24:101–112
R Development Team (2013) R: a language and environment for statistical computing, 3.0.2 edn. R Foundation for Statistical Computing, Vienna
Rand TA, van Veen FJF, Tscharntke T (2012) Landscape complexity differentially benefits generalized fourth, over-specialized third, trophic-level natural enemies. Ecography 35:97–104
Randlkofer B, Obermaier E, Casas J, Meiners T (2010) Connectivity counts: disentangling effects of vegetation structure elements on the searching movement of a parasitoid. Ecol Entomol 35:446–455
Robert CA et al (2013) Genetically engineered maize plants reveal distinct costs and benefits of constitutive volatile emissions in the field. Plant Biotechnol J 11:628–639
Sala OE et al (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774
Scanion JT, Willis DE (1985) Calculation of flame ionization detector relative response factors using the effective carbon number concept. J Chromatogr Sci 23:333–340
Schall P, Ammer C (2013) How to quantify forest management intensity in Central European forests. Eur J Forest Res 132:379–396
Simpson M et al (2011) Insect attraction to synthetic herbivore-induced plant volatile-treated field crops. Agric For Entomol 13:45–57
Sobek S, Scherber C, Steffan-Dewenter I, Tscharntke T (2009) Sapling herbivory, invertebrate herbivores and predators across a natural tree diversity gradient in Germany's largest connected deciduous forest. Oecologia 160:279–288
Springate ND, Basset Y (1996) Diel activity of arboreal arthropods associated with Papua New Guinean trees. J Nat Hist 30:101–112
Tollsten L, Müller PM (1996) Volatile organic compounds emitted from beech leaves. Phytochemistry 43:759–762
Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity—ecosystem service management. Ecol Lett 8:857–874
Turlings TCJ, Tumlinson JH (1992) Systemic release of chemical signals by herbivore-injured corn. Proc Natl Acad Sci USA 89:8399–8402
Tylianakis JM, Romo CM (2010) Natural enemy diversity and biological control: making sense of the context-dependency. Basic Appl Ecol 11:657–668
Tylianakis JM, Tscharntke T, Lewis OT (2007) Habitat modification alters the structure of tropical host–parasitoid food webs. Nature 445:202–205
Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363
Unsicker SB, Kunert G, Gershenzon J (2009) Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol 12:479–485
Wachmann E, Melber A, Deckert J (2004–2012) Wanzen Band 1–5. Goecke & Evers, Keltern
Acknowledgments
We thank Sonja Gockel, Simone Pfeiffer, Markus Fischer, Elisabeth Kalko, Eduard Linsenmair, Dominik Hessenmöller, Jens Nieschulze, Daniel Prati, Ingo Schöning, François Buscot, and Ernst-Detlef Schulze for their role in setting up the Biodiversity Exploratories project. We are grateful to Matthias Gross, Norbert Leber, Maria Lorenz, Britt Farquharson and Rebecca Wagner for field assistance and C. van Achterberg (Leiden, the Netherlands), Wolfgang Adaschkiewitz (Jena), Eric Anton (Jena), Norman F. Johnson (Ohio), Ljubodrag Mihajlovic, Milka Glavendekic (Belgrad), Martin Schwarz (Linz), and Helmut Sebald (Munich) for species identification. We also thank Fanny Maunz and Franziska Unsicker for their help with building the flight-interception traps, and Agnes Fastnacht and the MPI-ICE greenhouse team. The work was funded by the DFG program 1374 Infrastructure-Biodiversity-Exploratories (WE 2618/9-1) and by the Max Planck Society. Fieldwork permits were issued by the responsible state environmental office of Thüringen. All experiments comply with current German law.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Ingolf Steffan-Dewenter.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gossner, M.M., Weisser, W.W., Gershenzon, J. et al. Insect attraction to herbivore-induced beech volatiles under different forest management regimes. Oecologia 176, 569–580 (2014). https://doi.org/10.1007/s00442-014-3025-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-014-3025-4