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Effects of water stress on emission of volatile organic compounds by Vicia faba, and consequences for attraction of the egg parasitoid Trissolcus basalis

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Abstract

When plants are damaged by herbivorous insects, blends of volatile organic compounds (VOCs) are induced and released and can also be used by parasitoids to locate hosts. The aim was to determine whether VOCs induced by water stress affect the plant–herbivore–parasitoid system represented by broad bean (Vicia faba; Fabales: Fabaceae) stink bug (Nezara viridula; Heteroptera: Pentatomidae) egg parasitoid (Trissolcus basalis; Hymenoptera: Platygastridae). The effects of water stress (expressed as the percentage fraction of transpirable soil water [FTSW] supplied) alone and in combination with N. viridula damage (feeding plus oviposition) were determined according to: (1) the behavioural response of the egg parasitoid in a Y-tube olfactometer and (2) the plant VOCs collected and analysed by thermal desorption–gas chromatography–mass spectrometry. With pot water capacity as FTSW100, water stress was applied as mild (FTSW80), moderate (FTSW50) and severe (FTSW10). Bioassays with plants under abiotic stress alone showed that egg parasitoids are more attracted by FTSW10 plants than by well-watered plants. When plants were under abiotic and biotic stress interactions, the egg parasitoids are more attracted by FTSW10 and FTSW50 plants than by well-watered plants infested with N. viridula. Considering VOCs emissions, projection to latent structures discriminant analysis (PLS-DA) separated treatments according to egg parasitoid responses. Water stress alone and in combination with biotic stress induced changes in VOC emissions of V. faba plants that attract egg parasitoids. These findings contribute to our understanding of how water stress affects the interactions between plants, insect pests and egg parasitoids.

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References

  • Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3543

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp J, Wisthaler A, Hansel A, Kleist E, Miebach M, Niinemets Ü, Schurr U, Wildt J (2005) Ozone induced emissions of biogenic VOC from tobacco: relations between ozone uptake and emission of LOX products. Plant, Cell Environ 28:1334–1343

    Article  CAS  Google Scholar 

  • Brilli F, Barta C, Fortunati A, Lerdau M, Loreto F, Centritto M (2007) Response of isoprene emission and carbon metabolism to drought in white poplar (Populus alba) saplings. New Phytol 175:244–254

    Article  CAS  PubMed  Google Scholar 

  • Brilli F, Tsonev T, Mahmood T, Velikova V, Loreto F, Centritto M (2013) Ultradian variation of isoprene emission, photosynthesis, mesophyll conductance and optimum temperature sensitivity for isoprene emission in water-stressed Eucalyptus citriodora saplings. J Exp Bot 64:519–528

    Article  CAS  PubMed  Google Scholar 

  • Centritto M, Tognetti R, Leitgeb E, Střelcová K, Cohen S (2011a) Above ground processes—anticipating climate change influences. In: Bredemeier M, Cohen S, Godbold DL, Lode E, Pichler V, Schleppi P (eds) Forest management and the water cycle: an ecosystem-based approach. Springer, New York, pp 31–64

    Google Scholar 

  • Centritto M, Brilli F, Fodale R, Loreto F (2011b) Different sensitivity of isoprene emission, respiration, and photosynthesis to high growth temperature coupled with drought stress in black poplar (Populus nigra). Tree Physiol 31:275–286

    Article  CAS  PubMed  Google Scholar 

  • Chaves M, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    Article  CAS  PubMed  Google Scholar 

  • Clarke AR (1990) The control of Nezara viridula (L.) (Hemiptera: Pentatomidae) with introduced egg parasitoids in Australia. A review of a ‘landmark’ example of classical biological control. Aust J Entomol 41:1127–1146

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Colazza S, Bin F (1995) Efficiency of Trissolcus basalis (Hymenoptera: Scelionidae) as an egg parasitoid of Nezara viridula (Heteroptera: Pentatomidae) in central Italy. Environ Entomol 24:1703–1707

    Article  Google Scholar 

  • Colazza S, Salerno G, Wajnberg E (1999a) Volatile and contact chemicals released by Nezara viridula (Heteroptera: Pentatomidae) have a kairomonal effect on the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Biol Control 16:310–317

    Article  Google Scholar 

  • Colazza S, Peri D, Salerno G, Peri E, Lo Pinto M, Liotta G (1999b) Xbug, a video tracking and motion analysis system for LINUX. XII international entomophagous insects workshop. Pacific Grove, pp 26–30

  • Colazza S, Fucarino A, Peri E, Salerno G, Conti E, Bin F (2004a) Insect oviposition induces volatiles emission in herbaceous plant that attracts egg parasitoids. J Exp Biol 207:47–53

    Article  PubMed  Google Scholar 

  • Colazza S, McElfresh JS, Millar JG (2004b) Identification of volatile synomones, induced by Nezara viridula feeding and oviposition on bean spp., that attract the egg parasitoid Trissolcus basalis. J Chem Ecol 30:945–964

    Article  CAS  PubMed  Google Scholar 

  • Colazza S, Peri E, Salerno G, Conti E (2010) Host searching by egg parasitoids: exploitation of host chemical cues. In: Parra JRP, Consoli FL, Zucchi RA (eds) Egg parasitoids in agroecosystems with emphasis on trichogramma. Springer, NewYork, pp 97–147

    Google Scholar 

  • Conti E, Colazza S (2012) Chemical ecology of egg parasitoids associated with true bugs. Psyche. doi:10.1155/2012/651015

    Google Scholar 

  • Copolovici L, Kännaste A, Pazouki L, Niinemets Ü (2012) Emissions of green leaf volatiles and terpenoids from Solanum lycopersicum are quantitatively related to the severity of cold and heat shock treatments. J Plant Physiol 169:664–672

    Article  CAS  PubMed  Google Scholar 

  • Copolovici L, Kännaste A, Remmel T, Niinemets Ü (2014) Volatile organic compound emissions from Alnus glutinosa under interacting drought and herbivory stresses. Environ Exp Bot 100:55–63

    Article  CAS  Google Scholar 

  • Cusumano A, Weldegergis BT, Colazza S, Dicke M, Fatouros NE (2015) Attraction of egg-killing parasitoids toward induced plant volatiles in a multi-herbivore context. Oecologia 179:163–174

    Article  PubMed  Google Scholar 

  • de Rijk M, Dicke M, Poelman EH (2013) Foraging behaviour by parasitoids in multiherbivore communities. Anim Behav 85:1517–1528

    Article  Google Scholar 

  • Dicke M (2009) Behavioural and community ecology of plants that cry for help. Plant, Cell Environ 32:654–665

    Article  CAS  Google Scholar 

  • Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175

    Article  CAS  PubMed  Google Scholar 

  • Dicke M, Loreto F (2010) Induced plant volatiles: from genes to climate change. Trends Plant Sci 15:115–117

    Article  CAS  PubMed  Google Scholar 

  • Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198:16–32

    Article  CAS  PubMed  Google Scholar 

  • Fares S, Mahmood T, Liu S, Loreto F, Centritto M (2011) Influence of growth temperature and measuring temperature on isoprene emission, diffusive limitations of photosynthesis and respiration in hybrid poplars. Atmos Environ 45:155–161

    Article  CAS  Google Scholar 

  • Fatouros NE, Barbosa DL, Weldegergis BT, Pashalidou FG, van Loon JJA, Dicke M, Harvey JA, Gols R, Huigens ME (2012) Plant volatiles induced by herbivore egg deposition affect insects of different trophic levels. PLoS One 7(8):e43607. doi:10.1371/journal.pone.0043607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fortunati A, Barta C, Brilli F, Centritto M, Zimmer I, Schnitzler JP, Loreto F (2008) Isoprene emission is not temperature-dependent during and after severe drought-stress: a physiological and biochemical analysis. Plant J 55:687–697

    Article  CAS  PubMed  Google Scholar 

  • Gols R (2014) Direct and indirect chemical defences against insects in a multitrophic framework. Plant, Cell Environ 37:1741–1752

    Article  Google Scholar 

  • Hatanaka A (1993) The biogeneration of green odour by green leaves. Int J Plant Biochem 34:1201–1218

    CAS  Google Scholar 

  • Heffernan O (2013) The dry facts. Nature 501:S2–S3. doi:10.1038/501S2a

    Article  CAS  PubMed  Google Scholar 

  • Heil M (2014) Herbivore-induced plant volatiles: targets, perception and unanswered questions. New Phytol 204:297–306

    Article  CAS  Google Scholar 

  • Hilker M, Fatouros NE (2015) Plant responses to insect egg deposition. Ann Rev Entomol 60:493–515

    Article  CAS  Google Scholar 

  • Hilker M, Meiners T (2002) Induction of plant responses to oviposition and feeding by herbivorous arthropods: a comparison. Entomol Exp Appl 104:181–192

    Article  CAS  Google Scholar 

  • Hilker M, Meiners T (2010) How do plants ‘notice’ attack by herbivorous arthropods? Biol Rev 85:267–280

    Article  PubMed  Google Scholar 

  • Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15:176–184

    Article  CAS  PubMed  Google Scholar 

  • Holopainen JK, Himanen SJ, Poppy GM (2013) Climate change and its effects on the chemical ecology of insect parasitoids. In: Wajnberg E, Colazza S (eds) Chemical ecology of insect parasitoids. Wiley, Oxford, pp 168–190

    Chapter  Google Scholar 

  • Johnson SN, Staley JT, McLeod FAL, Hartley SE (2011) Plant-mediated effects of soil invertebrates and summer drought on above-ground multitrophic interactions. J Ecol 99:57–65. doi:10.1111/j.1365-2745.2010.01748.x

    Article  Google Scholar 

  • Jones WA (1988) World review of the parasitoids of the southern green stink bug, Nezara viridula (L.). Ann Entolol Soc Am 81:262–273

    Article  Google Scholar 

  • Jones HG, Stoll M, Santos T, de Sousa C, Chaves MM, Grant OM (2002) Use of infrared thermography for monitoring stomatal closure in the field: application to grapevine. J Exp Bot 53:2249–2260

    Article  CAS  PubMed  Google Scholar 

  • Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144. doi:10.1126/science.291.5511.2141

    Article  CAS  PubMed  Google Scholar 

  • Kessler A, Heil M (2011) Evolutionary ecology of plant defences. The multiple faces of indirect defences and their agents of natural selection. Funct Ecol 25:348–357. doi:10.1111/j.1365-2435.2010.01818.x

    Article  Google Scholar 

  • Loake G, Grant M (2007) Salicylic acid in plant defence—the players and protagonists. Curr Opin Plant Biol 10:466–472

    Article  CAS  PubMed  Google Scholar 

  • Loreto F, Centritto M (2008) Leaf carbon assimilation in a water-limited world. Plant Biosyst 142:154–161

    Article  Google Scholar 

  • Loreto F, Schnitzler JP (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15:154–166

    Article  CAS  PubMed  Google Scholar 

  • Loreto F, Fineschi S (2015) Reconciling functions and evolution of isoprene emission in higher plants. New Phytol 206:578–582. doi:10.1111/nph.13242

    Article  CAS  PubMed  Google Scholar 

  • Loreto F, Ciccioli P, Brancaleoni E, Cecinato A, Frattoni M, Sharkey TD (1996) Different sources of reduced carbon contribute to form three classes of terpenoid emitted by Quercus ilex L. leaves. PNAS 93:9966–9969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loreto F, Barta C, Brilli F, Nogues I (2006) On the induction of volatile organic compound emissions by plants as consequence of wounding or fluctuations of light and temperature. Plant, Cell Environ 29:1820–1828. doi:10.1111/j.1365-3040.2006.01561.x

    Article  CAS  Google Scholar 

  • Loreto F, Dicke M, Schnitzler JP, Turlings TCJ (2014) Plant volatiles and the environment. Plant, Cell Environ 37:1905–1908

    Article  Google Scholar 

  • Mattson WJ, Haack RA (1987) The role of drought in outbreaks of plant-eating insects. Bioscience 37:110–118

    Article  Google Scholar 

  • Meiners T, Peri E (2013) Chemical ecology of insect parasitoids: essential elements for developing effective biological control programmes. In: Wajnberg E, Colazza S (eds) Chemical ecology of insect parasitoids. Wiley, Oxford, pp 193–224

    Google Scholar 

  • Nowak M, Kleinwächter M, Manderscheid R, Weigel HJ, Selmar D (2010) Drought stress increases the accumulation of monoterpenes in sage (Salvia officinalis), an affect that is compensated by elevated carbon dioxide concentration. J Appl Bot Food Qual 83:133–136

    CAS  Google Scholar 

  • Ode PJ (2013) Plant defences and parasitoid chemical ecology. In: Wajnberg E, Colazza S (eds) Chemical ecology of insect parasitoids. Wiley, Oxford, pp 11–28

    Google Scholar 

  • Pallozzi E, Tsonev T, Marino G, Copolovici L, Niinemets Ü, Loreto F, Centritto M (2013) Isoprenoid emissions, photosynthesis and mesophyll conductance in response to blue light in Populus × canadensis, Quercus ilex and Citrus reticulata. Environ Exp Bot 95:50–58

    Article  CAS  Google Scholar 

  • Pineda A, Pangesti N, Soler R, van Dam NM, van Loon JJA, Dicke M (2016) Negative impact of drought stress on a generalist leaf chewer and a phloem feeder is associated with, but not explained by, an increase in herbivore-induced indole glucosinolates. Environ Exp Bot 123:88–97

    Article  CAS  Google Scholar 

  • Ponzio C, Gols R, Weldegergis BT, Dicke M (2014) Caterpillar-induced plant volatiles remain a reliable signal for foraging wasps during dual attack with a plant pathogen or non-host insect herbivore. Plant, Cell Environ 37:1924–1935. doi:10.1111/pce.12301

    Article  Google Scholar 

  • Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251

    Article  Google Scholar 

  • Romo CM, Tylianakis JM (2013) Elevated temperature and drought interact to reduce parasitoid effectiveness in suppressing hosts. PLoS One 8:e58136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Safavi M (1968) Etude biologique et ecologique des hymenopteres parasites des oeuefs des punaises des cereales. Entomophaga 13:381–495

    Google Scholar 

  • Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect-plant biology. Oxford University Press, Oxford

    Google Scholar 

  • Sharkey TD, Loreto F (1993) Water stress, temperature, and light effects on the capacity for isoprene emission and photosynthesis of kudzu leaves. Oecologia 95:328–333

    Article  Google Scholar 

  • Sinclair TR, Ludlow MM (1986) Influence of soil water supply on the plant water balance of four tropical grain legumes. Aust J Plant Physiol 13:329–341

    Article  Google Scholar 

  • Sokal R, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freeman, New York, 887 pp

    Google Scholar 

  • StatSoft Statistica (2001) Data analysis software system, version 7.1. StatSoft, Tulsa

    Google Scholar 

  • Steindel F, Beauchamp J, Hansel A, Kesselmeier J, Kleist E, Kuhn U, Wisthaler A, Wildt J (2005) Stress induced VOC emissions from mildew infested oak. Geophys Res Abstr 7:EGU05-A-03010

    Google Scholar 

  • Takabayashi J, Dicke M, Posthumus MA (1994) Volatile herbivore-induced terpenoids in plant-mite interactions: variation caused by biotic and abiotic factors. J Chem Ecol 20:1329–1354

    Article  CAS  PubMed  Google Scholar 

  • Tariq M, Wright DJ, Bruce TJA, Staley JT (2013a) Drought and root herbivory interact to alter the response of above-ground parasitoids to aphid infested plants and associated plant volatile signals. PLoS One 8:e69013. doi:10.1371/journal.pone.0069013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tariq M, Rossiter JT, Wright DJ, Staley JT (2013b) Drought alters interactions between root and foliar herbivores. Oecologia 172:1095–1104

    Article  PubMed  Google Scholar 

  • Toome M, Randjärv P, Copolovici L, Niinemets Ü, Heinsoo K, Luik A, Noe SM (2010) Leaf rust induced volatile organic compounds signalling in willow during infection. Planta 232:235–243

    Article  CAS  PubMed  Google Scholar 

  • Weldegergis BT, Zhu F, Poelman EH, Dicke M (2015) Drought stress affects plant metabolites and herbivore preference but not host location by its parasitoids. Oecologia 177:701–713

    Article  PubMed  Google Scholar 

  • White TCR (1974) A hypothesis to explain outbreaks of looper caterpillars, with special reference to populations of Selidosema suavis in a plantation of Pinus radiata in New Zealand. Oecologia 16:279–301

    Article  Google Scholar 

  • Yuan JS, Himanen SJ, Holopainen JK, Chen F, Stewart CN Jr (2009) Smelling global climate change: mitigation of function for plant volatile organic compounds. Trends Ecol Evol 24:323–331

    Article  PubMed  Google Scholar 

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Acknowledgements

We are grateful to Andrea Lucchetti for rearing the insects. This study was supported by the project MIUR-PRIN 2010–2011 ‘Going to the root of plant productivity: how the rhizosphere interacts with the aboveground armament for indirect and direct defence against abiotic and biotic stressors (PRO-ROOT)’ and by Fondazione Cassa di Risparmio Perugia (2015.0337.021 Ricerca Scientifica e Tecnologica). The authors thank Dr Chris Berrie for scientific language appraisal.

Funding

This study was funded by MIUR-PRIN 2010–2011 ‘Going to the root of plant productivity: how the rhizosphere interacts with the aboveground armament for indirect and direct defence against abiotic and biotic stressors (PRO-ROOT)’ and by Fondazione Cassa di Risparmio Perugia (2015.0337.021 Ricerca Scientifica e Tecnologica).

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Correspondence to Francesca Frati.

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Communicated by P.G. Becher.

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Salerno, G., Frati, F., Marino, G. et al. Effects of water stress on emission of volatile organic compounds by Vicia faba, and consequences for attraction of the egg parasitoid Trissolcus basalis . J Pest Sci 90, 635–647 (2017). https://doi.org/10.1007/s10340-016-0830-z

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