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Journal of Chemical Ecology

, Volume 42, Issue 12, pp 1247–1258 | Cite as

Effects of Arbuscular Mycorrhiza on Plant Chemistry and the Development and Behavior of a Generalist Herbivore

  • Viktoria V. Tomczak
  • Rabea Schweiger
  • Caroline Müller
Article

Abstract

Arbuscular mycorrhiza (AM) formed between plants and AM fungi (AMF) can alter host plant quality and thus influence plant-herbivore interactions. While AM is known to affect the development of generalist chewing-biting herbivores, AM-mediated impacts on insect behavior have been neglected until now. In this study, the effects of Rhizophagus irregularis, a generalist AMF, on phenotypic and leaf metabolic traits of Plantago major plants were investigated. Further, the influence of AM-mediated host plant modifications on the development and on seven behavioral traits of larvae of the generalist Mamestra brassicae were recorded. Tests were carried out in the third (L3) and fourth (L4) larval instar, respectively. While shoot water content, specific leaf area, and foliar concentrations of the secondary metabolite aucubin were higher in AM-treated compared to non-mycorrhized (NM) plants, lower concentrations of the primary metabolites citric acid and isocitric acid were found in leaves of AM plants. Larvae reared on AM plants gained a higher body mass and tended to develop faster than individuals reared on NM plants. However, plant treatment had no significant effect on any of the behavioral traits. Instead, differences between larvae of different ages were detected in several behavioral features, with L4 being less active and less bold than L3 larvae. The results demonstrate that AM-induced modifications of host plant quality influence larval development, whereas the behavioral phenotype seems to be more fixed at least under the tested conditions.

Keywords

Rhizophagus irregularis Plantago major Phenotypic and metabolic plant traits Plant-fungus-herbivore interactions Mamestra brassicae Behavioral traits 

Notes

Acknowledgments

Joop van Loon (Wageningen University) is thanked for providing us with eggs of Mamestra brassicae, Benjamin Wilden for support with rearing M. brassicae, and Franziska Buchholz for help in performing the bioassays. This work was funded by the grant MU1829/14-1 of the Deutsche Forschungsgemeinschaft.

References

  1. Augé RM (2001) Water relations, drought vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42CrossRefGoogle Scholar
  2. Baas R, Kuiper D (1989) Effects of vesicular‐arbuscular mycorrhizal infection and phosphate on Plantago major ssp. pleiosperma in relation to internal cytokinin concentrations. Physiol Plant 76:211–215CrossRefGoogle Scholar
  3. Behmer ST (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:165–187CrossRefPubMedGoogle Scholar
  4. Bennett AE, Bever JD, Bowers MD (2009) Arbuscular mycorrhizal fungal species suppress inducible plant responses and alter defensive strategies following herbivory. Oecologia 160:771–779CrossRefPubMedGoogle Scholar
  5. Besson M, Martin JR (2005) Centrophobism/thigmotaxis, a new role for the mushroom bodies in Drosophila. J Neurobiol 62:386–396CrossRefPubMedGoogle Scholar
  6. Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368CrossRefPubMedGoogle Scholar
  7. Clancy KM, Price PW (1987) Rapid herbivore growth enhances enemy attack: sublethal plant defenses remain a paradox. Ecology 68:733–737CrossRefGoogle Scholar
  8. Dahlbom SJ, Lagman D, Lundstedt-Enkel K, Sundström LF, Winberg S (2011) Boldness predicts social status in zebrafish (Danio rerio). PLoS ONE 6:e23565CrossRefPubMedPubMedCentralGoogle Scholar
  9. Denenberg VH (1969) Open-field behavior in the rat: what does it mean? Ann N Y Acad Sci 159:852–859CrossRefPubMedGoogle Scholar
  10. Fester T, Fetzer I, Buchert S, Lucas R, Rillig MC, Härtig C (2011) Towards a systemic metabolic signature of the arbuscular mycorrhizal interaction. Oecologia 167:913–924CrossRefPubMedGoogle Scholar
  11. 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 35:833–843CrossRefPubMedPubMedCentralGoogle Scholar
  12. Gange AC, West HM (1994) Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytol 128:79–87CrossRefGoogle Scholar
  13. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500CrossRefGoogle Scholar
  14. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular, vol 347, pp 1–32Google Scholar
  15. Hummel J, Strehmel N, Selbig J, Walther D, Kopka J (2010) Decision tree supported substructure prediction of metabolites from GC-MS profiles. Metabolomics 6:322–333CrossRefPubMedPubMedCentralGoogle Scholar
  16. Johnson M, Zalucki M (2007) Feeding and foraging behaviour of a generalist caterpillar: are third instars just bigger versions of firsts? Bull Entomol Res 97:81–88CrossRefPubMedGoogle Scholar
  17. Jones R (1977) Search behaviour: a study of three caterpillar species. Behaviour 60:237–259CrossRefGoogle Scholar
  18. Kempel A, Schmidt AK, Brandl R, Schädler M (2010) Support from the underground: induced plant resistance depends on arbuscular mycorrhizal fungi. Funct Ecol 24:293–300CrossRefGoogle Scholar
  19. Khan A, Kuek C, Chaudhry T, Khoo C, Hayes W (2000) Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere 41:197–207CrossRefPubMedGoogle Scholar
  20. Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, Bergmüller E, Dörmann P, Weckwerth W, Gibon Y, Stitt M (2005) GMD@ CSB. DB: the Golm metabolome database. Bioinformatics 21:1635–1638CrossRefPubMedGoogle Scholar
  21. Koricheva J, Gange AC, Jones T (2009) Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90:2088–2097CrossRefPubMedGoogle Scholar
  22. Kováts E (1958) Gas‐chromatographische Charakterisierung organischer Verbindungen. Teil 1: Retentionsindices aliphatischer Halogenide, Alkohole, Aldehyde und Ketone. Helv Chim Acta 41:1915–1932CrossRefGoogle Scholar
  23. Kutyniok M, Müller C (2012) Crosstalk between above-and belowground herbivores is mediated by minute metabolic responses of the host Arabidopsis thaliana. J Exp Bot 63:6199–9210CrossRefPubMedPubMedCentralGoogle Scholar
  24. Mattson WJ (1980) Herbivory in relation to plant nitrogen-content. Annu Rev Ecol Syst 11:119–161CrossRefGoogle Scholar
  25. Müller T, Müller C (2015) Behavioural phenotypes over the lifetime of a holometabolous insect. Front Zool (Suppl 1):S8Google Scholar
  26. Omino T, Yokoi S, Tsuji H (1973) Experimental studies on the daytime behaviour of Noctuid larvae, the cabbage armyworm, Mamestra brassicae, the tobacco cutworm, Spodoptera litura and the black cutworm, Agrotis ipsilon. Jpn J Appl Entomol Zool 17:215–220CrossRefGoogle Scholar
  27. Pankoke H, Buschmann T, Müller C (2013) Role of plant beta-glucosidases in the dual defense system of iridoid glycosides and their hydrolyzing enzymes in Plantago lanceolata and Plantago major. Phytochemistry 94:99–107CrossRefPubMedGoogle Scholar
  28. Pankoke H, Höpfner I, Matuszak A, Beyschlag W, Müller C (2015a) The effects of mineral nitrogen limitation, competition, arbuscular mycorrhiza, and their respective interactions, on morphological and chemical plant traits of Plantago lanceolata. Phytochemistry 118:149–161CrossRefPubMedGoogle Scholar
  29. Pankoke H, Gehring R, Müller C (2015b) Impact of the dual defence system of Plantago lanceolata (Plantaginaceae) on performance, nutrient utilisation and feeding choice behaviour of Amata mogadorensis larvae (Lepidoptera, Erebidae). J Insect Physiol 82:99–108CrossRefPubMedGoogle Scholar
  30. Paradi I, Bratek Z, Lang F (2003) Influence of arbuscular mycorrhiza and phosphorus supply on polyamine content, growth and photosynthesis of Plantago lanceolata. Biol Plant 46:563–569CrossRefGoogle Scholar
  31. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775CrossRefPubMedGoogle Scholar
  32. Prut L, Belzung C (2003) The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 463:3–33CrossRefPubMedGoogle Scholar
  33. Puttick GM, Bowers MD (1988) Effect of qualitative and quantitative variation in allelochemicals on a generalist insect - iridoid glycosides and the southern armyworm. J Chem Ecol 14:335–351CrossRefPubMedGoogle Scholar
  34. R Developmental Core Team (2014) R: a language and environment for statistical computing, vol. 3.0.3. R Foundation for Statistical Computing, ViennaGoogle Scholar
  35. Reich P, Ellsworth D, Walters M (1998) Leaf structure (specific leaf area) modulates photosynthesis–nitrogen relations: evidence from within and across species and functional groups. Funct Ecol 12:948–958CrossRefGoogle Scholar
  36. Roger A, Getaz M, Rasmann S, Sanders IR (2013) Identity and combinations of arbuscular mycorrhizal fungal isolates influence plant resistance and insect preference. Ecol Entomol 38:330–338CrossRefGoogle Scholar
  37. Rojas JC, Wyatt TD, Birch MC (2000) Flight and oviposition behavior toward different host plant species by the cabbage moth, Mamestra brassicae (L.) (Lepidoptera : Noctuidae). J Insect Behav 13:247–254CrossRefGoogle Scholar
  38. Rosenthal GA, Berenbaum MR (2012) Herbivores: their interactions with secondary plant metabolites: ecological and evolutionary processes. Academic Press, New YorkGoogle Scholar
  39. Schauer N, Steinhauser D, Strelkow S, Schomburg D, Allison G, Moritz T, Lundgren K, Roessner-Tunali U, Forbes MG, Willmitzer L, Fernie AR (2005) GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Lett 579:1332–1337CrossRefPubMedGoogle Scholar
  40. Schoonhoven LM, van Loon JJ, Dicke M (2005) Insect-plant biology. Oxford University Press, OxfordGoogle Scholar
  41. Schüßler A, Walker C (2010) The Glomeromycota: a species list with new families and new genera. The Royal Botanic Garden Edinburgh, The Royal Botanik Garden Kew, Botanische Staatssammlung Munich, and Oregon State UniversityGoogle Scholar
  42. Schweiger R, Müller C (2015) Leaf metabolome in arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 26:120–126CrossRefPubMedGoogle Scholar
  43. Schweiger R, Baier MC, Persicke M, Müller C (2014a) High specificity in plant leaf metabolic responses to arbuscular mycorrhiza. Nat Commun 5:3886CrossRefPubMedGoogle Scholar
  44. Schweiger R, Baier MC, Müller C (2014b) Arbuscular mycorrhiza-induced shifts in foliar metabolism and photosynthesis mirror the developmental stage of the symbiosis and are only partly driven by improved phosphate uptake. Mol Plant-Microbe Interact 27:1403–1412CrossRefPubMedGoogle Scholar
  45. Simon P, Dupuis R, Costentin J (1994) Thigmotaxis as an index of anxiety in mice. Influence of dopaminergic transmissions. Behav Brain Res 61:59–64CrossRefPubMedGoogle Scholar
  46. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, New YorkGoogle Scholar
  47. Tremmel M, Müller C (2013a) Insect personality depends on environmental conditions. Behav Ecol 24:386–392CrossRefGoogle Scholar
  48. Tremmel M, Müller C (2013b) The consequences of alternating diet on performance and food preferences of a specialist leaf beetle. J Insect Physiol 59:840–847CrossRefPubMedGoogle Scholar
  49. Wu Q-S, Xia R-X (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163:417–425CrossRefPubMedGoogle Scholar
  50. Wurst S, Dugassa‐Gobena D, Langel R, Bonkowski M, Scheu S (2004) Combined effects of earthworms and vesicular–arbuscular mycorrhizas on plant and aphid performance. New Phytol 163:169–176CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Viktoria V. Tomczak
    • 1
  • Rabea Schweiger
    • 1
  • Caroline Müller
    • 1
  1. 1.Department of Chemical EcologyBielefeld UniversityBielefeldGermany

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