Advertisement

Journal of Chemical Ecology

, Volume 40, Issue 11–12, pp 1220–1231 | Cite as

Manipulating Feeding Stimulation to Protect Crops Against Insect Pests?

  • Maxime R. HervéEmail author
  • Régine Delourme
  • Antoine Gravot
  • Nathalie Marnet
  • Solenne Berardocco
  • Anne Marie Cortesero
Article

Abstract

Enhancing natural mechanisms of plant defense against herbivores is one of the possible strategies to protect cultivated species against insect pests. Host plant feeding stimulation, which results from phagostimulant and phagodeterrent effects of both primary and secondary metabolites, could play a key role in levels of damage caused to crop plants. We tested this hypothesis by comparing the feeding intensity of the pollen beetle Meligethes aeneus on six oilseed rape (Brassica napus) genotypes in a feeding experiment, and by assessing the content of possible phagostimulant and phagodeterrent compounds in tissues targeted by the insect (flower buds). For this purpose, several dozens of primary and secondary metabolites were quantified by a set of chromatographic techniques. Intergenotypic variability was found both in the feeding experiment and in the metabolic profile of plant tissues. Biochemical composition of the perianth was in particular highly correlated with insect damage. Only a few compounds explained this correlation, among which was sucrose, known to be highly phagostimulating. Further testing is needed to validate the suggested impact of the specific compounds we have identified. Nevertheless, our results open the way for a crop protection strategy based on artificial selection of key determinants of insect feeding stimulation.

Keywords

Brassica napus Meligethes aeneus Feeding stimulation Primary and secondary metabolites Phagostimulant/phagodeterrent compounds Crop protection 

Notes

Acknowledgments

We are grateful to Sam Cook and Maria Manzanares-Dauleux for their very helpful comments on this study, to Mélanie Leclair, Céline Josso, Sonia Dourlot, Christine Lariagon, and Anne Boudier for technical help during the experiments, and to the UMR IGEPP glasshouse team for taking care of the plants used. Metabolic analyses were performed on the P2M2 platform (Le Rheu, France). Maxime Hervé was supported by a CJS grant from the French National Institute of Agronomical Research.

Supplementary material

10886_2014_517_MOESM1_ESM.docx (26 kb)
ESM 1 (DOCX 26 kb)

References

  1. Adams MA, Chen ZL, Landman P, Colmer TD (1999) Simultaneous determination by capillary gas chromatography of organic acids, sugars, and sugar alcohols in plant tissue extracts as their trimethylsilyl derivatives. Anal Biochem 266:77–84PubMedCrossRefGoogle Scholar
  2. Alagar M, Suresh S, Samiyappan R, Saravanakumar D (2007) Reaction of resistant and susceptible rice genotypes against brown planthopper (Nilaparvata lugens). Phytoparasitica 35:346–356CrossRefGoogle Scholar
  3. Ali K, Maltese F, Zyprian E, Rex M, Choi YH, Verpoorte R (2009) NMR metabolic fingerprinting based identification of grapevine metabolites associated with downy mildew resistance. J Agric Food Chem 57:9599–9606PubMedCrossRefGoogle Scholar
  4. Barker M, Rayens W (2003) Partial least squares for discrimination. J Chemometr 17:166–173CrossRefGoogle Scholar
  5. Barrett RD, Agrawal AA (2004) Interactive effects of genotype, environment, and ontogeny on resistance of cucumber (Cucumis sativus) to the generalist herbivore Spodoptera exigua. J Chem Ecol 30:37–54PubMedCrossRefGoogle Scholar
  6. Bartlet E, Williams IH (1991) Factors restricting the feeding of the cabbage stem flea beetle (Psylliodes chrysocephala). Entomol Exp Appl 60:233–238CrossRefGoogle Scholar
  7. Bartlet E, Parsons D, Williams IH, Clark SJ (1994) The influence of glucosinolates and sugars on feeding by the cabbage stem flea beetle, Psylliodes chrysocephala. Entomol Exp Appl 73(1):77–83CrossRefGoogle Scholar
  8. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:289–300Google Scholar
  9. Berenbaum MR (1995) Turnabout is fair play: secondary roles for primary compounds. J Chem Ecol 21:925–940PubMedCrossRefGoogle Scholar
  10. Berenbaum MR, Zangerl AR (2008) Facing the future of plant-insect interaction research: le retour à la “raison d’être”. Plant Physiol 146:804–811PubMedCentralPubMedCrossRefGoogle Scholar
  11. Blight MM, Smart LE (1999) Influence of visual cues and isothiocyanates lures on capture of the pollen beetle, Meligethes aeneus in field traps. J Chem Ecol 25:1501–1516Google Scholar
  12. Carmona D, Lajeunesse MJ, Johnson MTJ (2011) Plant traits that predict resistance to herbivores. Funct Ecol 25:358–367CrossRefGoogle Scholar
  13. Carrié RJ, George DR, Wäckers FL (2012) Selection of floral resources to optimize conservation of agriculturally-functional insect groups. J Insect Conserv 16:635–640CrossRefGoogle Scholar
  14. Chapman RF (2003) Contact chemoreception in feeding by phytophagous insects. Annu Rev Entomol 48:455–484PubMedCrossRefGoogle Scholar
  15. Charpentier R (1985) Host plant selection by the pollen beetle Meligethes aeneus. Entomol Exp Appl 38:277–285CrossRefGoogle Scholar
  16. Clissold FJ, Sanson GD, Read J, Simpson SJ (2009) Gross vs. net income : how plant toughness affects performance of an insect herbivore. Ecology 90(12):3393–3405PubMedCrossRefGoogle Scholar
  17. Cook SM, Awmack CS, Murray DA, Williams IH (2003) Are honey bees’ foraging preferences affected by pollen amino acid composition? Ecol Entomol 28:622–627CrossRefGoogle Scholar
  18. Cook SM, Smart LE, Martin JL, Murray DA, Watts NP, Williams IH (2006) Exploitation of host plant preferences in pest management strategies for oilseed rape (Brassica napus). Entomol Exp Appl 119:221–229CrossRefGoogle Scholar
  19. Cook SM, Rasmussen HB, Birkett MA, Murray DA, Pye BJ, Watts NP, Williams IH (2007) Behavioural and chemical ecology underlying the success of turnip rape (Brassica rapa) trap crops in protecting oilseed rape (Brassica napus) from the pollen beetle (Meligethes aeneus). Arthropod Plant Interact 1:57–67CrossRefGoogle Scholar
  20. Després L, David JP, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22:298–307PubMedCrossRefGoogle Scholar
  21. Diaz Napal GN, Carpinella MC, Palacios SM (2009) Antifeedant activity of ethanolic extract from Flourensia oolepis and isolation of pinocembrin as its active principle compound. Bioresour Technol 100:3669–3673PubMedCrossRefGoogle Scholar
  22. Diaz Napal GN, Defagó MT, Valladares GR, Palacios MT (2010) Response of Epilachna paenulata to two flavonoids, pinocembrin and quercetin, in a comparative study. J Chem Ecol 36:898–904PubMedCrossRefGoogle Scholar
  23. Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20Google Scholar
  24. Eickermann M, Ulber B (2010) Screening of oilseed rape and other brassicaceous genotypes for susceptibility to Ceutorhynchus pallidactylus (Mrsh.). J Appl Entomol 134:542–550Google Scholar
  25. Ekbom B, Borg A (1996) Pollen beetle (Meligethes aeneus) oviposition and feeding preference on different host plant species. Entomol Exp Appl 78:291–299CrossRefGoogle Scholar
  26. El Bouhssini M, Ogbonnaya FC, Chen M, Lhaloui S, Rihawi F, Dabbous A (2013) Sources of resistance in primary synthetic hexaploid wheat (Triticum aestivum L.) to insect pests: Hessian fly, Russian wheat aphid and Sunn pest in the fertile crescent. Genet Resour Crop Evol 60:621–627CrossRefGoogle Scholar
  27. Francisco M, Moreno DA, Cartea ME, Ferreres F, Farciá-Viguera C, Velasco P (2009) Simultaneous identification of glucosinolates and phenolics compounds in a representative collection of vegetable Brassica rapa. J Chromatogr A 1216:6611–6619PubMedCrossRefGoogle Scholar
  28. Free JB, Williams IH (1978) The responses of the pollen beetle, Meligethes aeneus, and the seed weevil, Ceutorhynchus assimilis, to oil-seed rape, Brassica napus, and other plants. J Appl Ecol 15:761–774CrossRefGoogle Scholar
  29. Gatehouse JA (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytol 156:145–169CrossRefGoogle Scholar
  30. Giamoustaris A, Mithen R (1995) The effect of modifying the glucosinolate content of leaves of oilseed rape (Brassica napus ssp. oleifera) on its interaction with specialist and generalist pests. Ann Appl Biol 126:347–363CrossRefGoogle Scholar
  31. Glynn C, Rönnberg-Wästljung AC, Julkunen-Tiitto R, Weih M (2004) Willow genotype, but not drought treatment, affects foliar phenolics concentrations and leaf-beetle resistance. Entomol Exp Appl 113:1–14CrossRefGoogle Scholar
  32. González I, Lé Cao KA, Déjean S (2011) mixOmics: omics data integration project. URL: http://www.math.univ-toulouse.fr/~biostat/mixOmics/
  33. Gravot A, Dittami SM, Rousvoal S, Lugan R, Eggert A, Collén J, Boyen C, Bouchereau A, Tonon T (2010) Diurnal oscillations of metabolite abundances and gene analysis provide new insights into central metabolic processes of the brown alga Ectocarpus siliculosus. New Phytol 188:98–110PubMedCrossRefGoogle Scholar
  34. Gruber MY, Wang S, Ethier S, Holowachuk J, Bonham-Smith PC, Soroka J, Lloyd A (2006) “Hairy canola”—Arabidopsis GL3 induces a dense covering of trichomes on Brassica napus seedlings. Plant Mol Biol 60:679–698PubMedCrossRefGoogle Scholar
  35. Henery ML, Henson M, Wallis IR, Stone C, Foley WJ (2008) Predicting crown damage to Eucalyptus grandis by Paropsis atomaria with direct and indirect measures of leaf composition. For Ecol Manag 255:3642–3651CrossRefGoogle Scholar
  36. Hollister B, Mullin CA (1998) Behavioral and electrophysiological dose–response relationships in adult western corn rootworm (Diabrotica virgifera virgifera LeConte) for host pollen amino acids. J Insect Physiol 44:463–470PubMedCrossRefGoogle Scholar
  37. Hopkins RJ, van Dam NM, van Loon JJA (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu Rev Entomol 54:57–83PubMedCrossRefGoogle Scholar
  38. Hori M, Nakamura H, Fujii Y, Suzuki Y, Matsuda K (2010) Chemicals affecting the feeding preference of the Solanaceae-feeding lady beetle Henosepilachna vigintioctomaculata (Coleoptera: Coccinellidae). J Appl Entomol 135:121–161CrossRefGoogle Scholar
  39. Isidoro N, Bartlet E, Ziesmann J, Williams IH (1998) Antennal contact chemosensilla in Psylliodes chrysocephala responding to cruciferous allelochemicals. Physiol Entomol 23:131–138CrossRefGoogle Scholar
  40. Jackson DM, Harrison HF (2013) Insect resistance in traditional and heirloom sweetpotato varieties. J Econ Entomol 106:1456–1462PubMedCrossRefGoogle Scholar
  41. Jubault M, Hamon C, Gravot A, Lariagon C, Delourme R, Bouchereau A, Manzanares-Dauleux MJ (2008) Differential regulation of root arginine catabolism and polyamine metabolism in clubroot-susceptible and partially resistant Arabidopsis genotypes. Plant Physiol 146:2008–2019PubMedCentralPubMedCrossRefGoogle Scholar
  42. Kim JH, Mullin CA (1998) Structure-phagostimulatory relationships for amino acids in adult western corn rootworm, Diabrotica virgifera virgifera. J Chem Ecol 24:1499–1511CrossRefGoogle Scholar
  43. Knutson AE, Mekala KD, Smith CW, Campos C (2013) Tolerance to feeding damage by cotton fleahopper (Hemiptera: Miridae) among genotypes representing adapted germplasm pools of United States upland cotton. J Econ Entomol 106:1045–1052PubMedCrossRefGoogle Scholar
  44. Kühnle A, Müller C (2009) Differing acceptance of familiar and unfamiliar plant species by an oligophagous beetle. Entomol Exp Appl 131:189–199CrossRefGoogle Scholar
  45. Lancashire PD, Bleiholder H, Vandenboom T, Langeluddeke P, Strauss R, Weber E, Witzenberger A (1991) A uniform decimal code for growth-stages of crops and weeds. Ann Appl Biol 119:561–601CrossRefGoogle Scholar
  46. Leiss KA, Cristofori G, van Steenis R, Verpoorte R, Klinkhamer PG (2013) An eco-metabolomic study of host plant resistance to western flower thrips in cultivated, biofortified and wild carrots. Phytochemistry 93:63–70PubMedCrossRefGoogle Scholar
  47. Lenth RV (2013) lsmeans: Least-squares means. R package version 1.10–4. http://CRAN.R-project.org/package=lsmeans
  48. Lin S, Mullin CA (1999) Lipid, polyamide, and flavonols phagostimulants for adult western corn rootworm from sunflower (Helianthus annuus L.) pollen. J Agric Food Chem 47:1223–1229PubMedCrossRefGoogle Scholar
  49. Lugan R, Niogret MF, Kervazo L, Larher FR, Kopka J, Bouchereau A (2009) Metabolome and water status phenotyping of Arabidopsis under abiotic stress cues reveals new insight into ESK1 function. Plant Cell Environ 32:95–108PubMedCrossRefGoogle Scholar
  50. Lyytinen A, Lindström L, Mappes J, Julkunen-Tiitto R, Fasulati S, Tiilikkala K (2007) Variability in host plant chemistry: behavioural responses and life-history parameters of the Colorado potato beetle (Leptinotarsa decemlineata). Chemoecology 17:51–56CrossRefGoogle Scholar
  51. Marques I, Draper D (2012) Pollination activity affects selection on floral longevity in the autumnal-flowering plant, Narcissus serotinus L. Botany 90:283–291CrossRefGoogle Scholar
  52. Merivee E, Märtmann H, Must A, Milius M, Williams IH, Mänd M (2008) Electrophysiological responses from neurons of antennal taste sensilla in the polyphagous predatory ground beetle Pterostichus oblongopunctatus (Fabricius 1787) to plant sugars and amino acids. J Insect Physiol 54:1213–1219PubMedCrossRefGoogle Scholar
  53. Merivee E, Must A, Tooming E, Williams IH, Sibul I (2012) Sensitivity of antennal gustatory receptor neurons to aphid honeydew sugars in the carabid Anchomenus dorsalis. Physiol Entomol 37:369–378CrossRefGoogle Scholar
  54. Mitchell BK, Gregory P (1979) Physiology of the maxillary sugar sensitive cell in the red turnip beetle, Entomoscelis Americana. J Comp Physiol A 132:167–178CrossRefGoogle Scholar
  55. Mitchell BK, Schoonhoven LM (1974) Taste receptors in Colorado beetle larvae. J Insect Physiol 20:1787–1793PubMedCrossRefGoogle Scholar
  56. Nielsen JK, Larsen LM, Sørensen H (1979) Host plant selection of the horseradish flea beetle Phyllotreta armoraciae (Coleoptera: Chrysomelidae): identification of two flavonols glycosides stimulating feeding in combination with glucosinolates. Entomol Exp Appl 26:40–48CrossRefGoogle Scholar
  57. Nilsson C (1988) The pollen beetle (M. aeneus F.) in winter and spring rape at Alnarp 1976–1978. II. Oviposition. Vaxtskyddsnotiser 52:139–144Google Scholar
  58. Niveyro SL, Mortensen AG, Fomsgaard IS, Salvo A (2013) Differences among five amaranth varieties (Amaranthus spp.) regarding secondary metabolites and foliar herbivory by chewing insects in the field. Arthropod Plant Interact 7:235–245CrossRefGoogle Scholar
  59. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/
  60. Rapacz M (1998) Physiological effects of winter rape (Brassica napus var. oleifera) prehardening to frost. II. Growth, energy partitioning and water status during cold acclimation. J Agron Crop Sci 181:81–87CrossRefGoogle Scholar
  61. Ruther J, Thiemann K (1997) Response of the pollen beetle Meligethes aeneus to volatiles emitted by intact plants and conspecifics. Entomol Exp Appl 84:183–188CrossRefGoogle Scholar
  62. Sasaki H, Ichimura K, Oda M (1996) Changes in sugar content during cold acclimation and deacclimation of cabbage seedlings. Ann Bot 78:365–369CrossRefGoogle Scholar
  63. Simmonds MS (2001) Importance of Flavonoids in insect-plant interactions: feeding and oviposition. Phytochemistry 56:245–252PubMedCrossRefGoogle Scholar
  64. Simmonds MS (2003) Flavonoid-insect interactions: recent advances in our knowledge. Phytochemistry 64:21–30PubMedCrossRefGoogle Scholar
  65. Smart LE, Blight MM (2000) Response of the pollen beetle, Meligethes aeneus, to traps baited with volatiles from oilseed rape, Brassica napus. J Chem Ecol 26:1051–1064CrossRefGoogle Scholar
  66. Ströcker K, Wendt S, Kirchner WH, Struck C (2013) Feeding preferences of the weevils Sitona gressorius and Sitona griseus on different lupin genotypes and the role of alkaloids. Arthropod Plant Interact 7:579–589CrossRefGoogle Scholar
  67. Tefera T, Demissie G, Mugo S, Beyene Y (2013) Yield and agronomic performance of maize hybrids resistant to the maize weevil Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae). Crop Prot 46:94–99CrossRefGoogle Scholar
  68. Tooming E, Merivee E, Must A, Luik A, Williams IH (2012) Antennal sugar sensitivity in the click beetle Agriotes obscures. Physiol Entomol 37:345–353CrossRefGoogle Scholar
  69. Treutter D (2006) Significance of Flavonoids in plant resistance: a review. Environ Chem Lett 4:147–157CrossRefGoogle Scholar
  70. Velasco P, Francisco M, Moreno DA, Ferreres F, García-Viguera C, Cartea ME (2011) Phytochemical fingerprinting of vegetable Brassica oleracea and Brassica napus by simultaneous identification of glucosinolates and phenolics. Phytochem Anal 22:144–152PubMedCrossRefGoogle Scholar
  71. Venables WN, Ripley BB (2002) Modern applied statistics with S, 4th edn. Springer, New YorkCrossRefGoogle Scholar
  72. Wagner G, Charton S, Lariagon C, Laperche A, Lugan R, Hopkins J, Frendo P, Bouchereau A, Delourme R, Gravot A, Manzanare-Dauleux MJ (2012) Metabotyping: a new approach to investigate rapeseed (Brassica napus L.) genetic diversity in the metabolic response to clubroot infection. Mol Plant Microbe In 25:1478–1491CrossRefGoogle Scholar
  73. Williams IH (2010) The major insect pests of oilseed rape in Europe and their management: an overview. In: Williams IH (ed) Biocontrol-based integrated management of oilseed rape pests. Springer, London, pp 1–43CrossRefGoogle Scholar
  74. Williams IH, Free JB (1978) The feeding and mating behaviour of pollen beetles (Meligethes aeneus Fab.) and seed weevils (Ceuthorhynchus assimilis Payk.) on oil-seed rape (Brassica napus L.). J Agric Sci 91:453–459CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Maxime R. Hervé
    • 1
    • 2
    • 3
    Email author
  • Régine Delourme
    • 1
  • Antoine Gravot
    • 2
    • 3
  • Nathalie Marnet
    • 4
  • Solenne Berardocco
    • 2
    • 3
  • Anne Marie Cortesero
    • 2
    • 3
  1. 1.INRA, UMR1349 IGEPPLe RheuFrance
  2. 2.Université Rennes 1, UMR1349 IGEPPRennesFrance
  3. 3.Université Européenne de BretagneRennesFrance
  4. 4.INRA, UR1268 BIALe RheuFrance

Personalised recommendations