, Volume 180, Issue 3, pp 797–807 | Cite as

Intraspecific differences in plant chemotype determine the structure of arthropod food webs

  • János Bálint
  • Sharon E. Zytynska
  • Rozália Veronika Salamon
  • Mohsen Mehrparvar
  • Wolfgang W. Weisser
  • Oswald J. Schmitz
  • Klára BenedekEmail author
  • Adalbert BalogEmail author
Community ecology - Original research


It is becoming increasingly appreciated that the structure and functioning of ecological food webs are controlled by the nature and level of plant chemicals. It is hypothesized that intraspecific variation in plant chemical resistance, in which individuals of a host-plant population exhibit genetic differences in their chemical contents (called ‘plant chemotypes’), may be an important determinant of variation in food web structure and functioning. We evaluated this hypothesis using field assessments and plant chemical assays in the tansy plant Tanacetum vulgare L. (Asteraceae). We examined food webs in which chemotypes of tansy plants are the resource for two specialized aphids, their predators and mutualistic ants. The density of the ant-tended aphid Metopeurum fuscoviride was significantly higher on particular chemotypes (borneol) than others. Clear chemotype preferences between predators were also detected. Aphid specialist seven-spotted ladybird beetles (Coccinella septempunctata) were more often found on camphor plants, while significantly higher numbers of the polyphagous nursery web spider (Pisaura mirabilis) were observed on borneol plants. The analysis of plant chemotype effects on the arthropod community clearly demonstrates a range of possible outcomes between plant-aphid-predator networks. The findings help to offer a deeper insight into how one important factor—plant chemical content—influences which species coexist within a food web on a particular host plant and the nature of their trophic linkages.


Aphids Ants Bottom-up effects Interactions Predation Top-down effects 



This research was founded by the Institute of Research Programs of the Sapientia University, grant no. 1/13/05.01.2012. The authors declare no conflict of interest.

Author contribution statement

W. W. W. and A. B. conceived the experiments. A. B., K. B. and J. B. designed the experiments. A. B., K. B., J. B., R. V. S. and M. M. performed the experiments. S. E. Z., W. W. W., O. J. S. and A. B. analysed the data. A. B., W. W. W. and O. J. S. wrote the manuscript. S. E. Z. provided editorial advice.

Supplementary material

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Supplementary material 1 (JPEG 168 kb)
442_2015_3508_MOESM2_ESM.docx (180 kb)
Supplementary material 2 (DOCX 180 kb)


  1. András CsD, Kapás Á, Bartha Z, Salamon R, Cs Csajági, Székely G, Sz Salamon, György É (2009) Volatile extraction from fennel (Foeniculum vulgare Mill.). J Oil Soap Cosm 58:66–72Google Scholar
  2. Baldwin IT (2006) Volatile signaling in plant–plant interactions: ‘talking trees’ in the genomics era. Science 311:812–815CrossRefPubMedGoogle Scholar
  3. Barabási AL, Albert R (1999) Emergence of scaling in random networks. Science 286:509–512CrossRefPubMedGoogle Scholar
  4. Barbour MA, Rodrigues-Cabal MA, Wu ET, Julkunen-Tiitto R, Ritland CE, Miscampbell AE, Jules ES, Crutsinger GM (2015) Multiple plant traits shape the genetic basis of herbivore community assembly. Funct Ecol. doi: 10.1111/1365-2435.12409 (in press) Google Scholar
  5. Begon M, Townsend CR, Harper JL (2006) Ecology: from individuals to ecosystems, 4th edn. Blackwell, OxfordGoogle Scholar
  6. Benedek K, Bálint J, Salamon VR, Kovács E, Ábrahám B, Cs Fazakas, Loxdale HD, Balog A (2015) Tansy plant (Tanacetum vulgare L.) chemotype determines aphid genotype and its associated predator system. Biol J Linn Soc 114:709–719CrossRefGoogle Scholar
  7. Brink PJV, Braak CJFT (1999) Principal response curves: analysis of time-dependent multivariate responses of biological community to stress. Toxicol Chem 18(2):138–148CrossRefGoogle Scholar
  8. Bruinsma M, Posthumus MA, Mumm R, Mueller MJ, van Loon JJ, Dicke M (2009) Jasmonic acid-induced volatiles of Brassica oleracea attract parasitoids: effects of time and dose, and comparison with induction by herbivores. J Exp Bot 60:2575–2587CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bukovinszky T, van Veen FF, Jongema Y, Dicke M (2008) Direct and indirect effects of resource quality on food web structure. Science 319:804–807CrossRefPubMedGoogle Scholar
  10. Burghardt KT, Schmitz OJ (2015) Influence of plant defenses and nutrients on trophic control of ecosystems. Ch. 9. In: Hanley T, La Pierre K (eds) Trophic ecology: bottom-up and top-down interactions across aquatic and terrestrial systems. Cambridge University Press, CambridgeGoogle Scholar
  11. Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders NJ (2006) Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313:966–968CrossRefPubMedGoogle Scholar
  12. Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15(3):167–175CrossRefPubMedGoogle Scholar
  13. Dunne JA, Williams RJ, Martinez ND (2002) Food-web structure and network theory: the role of connectance and size. Proc Natl Acad Sci USA 99:12917–12922CrossRefPubMedPubMedCentralGoogle Scholar
  14. Flatt T, Weisser WW (2000) The effects of mutualistic ants on aphid life history traits. Ecology 81:3522–3529CrossRefGoogle Scholar
  15. Gols R, Wagenaar R, Bukovinszky T, van Dam NM, Dicke Bullock JM, Harwey JA (2008) Genetic variation in defence chemistry in wild cabbage affects herbivores and their endoparasitoids. Ecology 89(6):1616–1626CrossRefPubMedGoogle Scholar
  16. Hare JD (1992) Effects of plant variation on herbivore-natural enemy interactions. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. University of Chicago Press, Chicago, pp 278–300Google Scholar
  17. Harvey JA, van Dam NM, Gols R (2003) Interactions over four trophic levels: food plant quality affects development of a hyperparasitoid as mediated through a herbivore and its primary parasitoid. J Anim Ecol 72:520–531CrossRefGoogle Scholar
  18. Harvey JA, van Dam NM, Witjes LMA, Soler R, Gols R (2007) Effects of dietary nicotine on the development of an insect herbivore, its parasitoid and secondary hyperparasitoid over four trophic levels. Ecol Entomol 32:15–23CrossRefGoogle Scholar
  19. Holopainen M (1989) A study on the essential oil of tansy (Tanacetum vulgare L.). University of Helsinki, FinlandGoogle Scholar
  20. Holopainen M, Hiltunen R, Lokki J, Forsen K, Schantz MV (1987a) Model for the genetic-control of thujone, sabinene and umbellulone in Tansy (Tanacetum vulgare L). Hereditas 106:205–208CrossRefGoogle Scholar
  21. Holopainen M, Hiltunen R, von Schantz M (1987b) A study on tansy chemotypes. Planta Med 53:284–287CrossRefPubMedGoogle Scholar
  22. Huang M, Abel C, Sohrabi R, Petri J, Haupt I, Cosimano J, Gershenzon J, Tholl D (2010) Variation of herbivore-induced volatile terpenes among Arabidopsis ecotypes depends on allelic differences and sub cellular targeting of two terpene synthases, TPS02 and TPS03. Plant Physiol 153:1293–1310CrossRefPubMedPubMedCentralGoogle Scholar
  23. Johnson MTJ (2008) Bottom-up effects of plant genotype on aphids, ants and predators. Ecology 89:145–154CrossRefPubMedGoogle Scholar
  24. Johnson MTJ, Agrawal AA (2005) Plant genotype and environmental interact to shape a diverse arthropod community on evening primrose (Oenothera biennis). Ecology 86:874–885CrossRefGoogle Scholar
  25. Jordán F, Gjata N, Mei S, Yule CM (2012) Simulating food web dynamics along a gradient: quantifying human influence. PLoS One 7(7):e40280. doi: 10.1371/journal.pone.0040280 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kapás Á, András CsD, Dobre TG, Vass E, Székely G, Stroescu M, Lányi Sz, Ábrahám BÉ (2011) kinetics of essential oil separation from fennel by microwave hydro distillation (MWHD). UPB Sci Bull Series B 73(4):127–130Google Scholar
  27. Keskitalo M, Linden A, Valkonen J (1998) Genetic and morphological diversity of Finnish tansy (Tanacetum vulgare L., Asteraceae). Theor Appl Genet 96:1141–1150CrossRefGoogle Scholar
  28. Linhart YB, Keefover-Ring K, Mooney KA, Breland B, Thompson JD (2005) A chemical polymorphism in a multitrophic setting: thyme monoterpene composition and food web structure. Am Nat 166:517–529CrossRefPubMedGoogle Scholar
  29. Mantyla E, Tero K, Erkki H (2004) Attraction of willow warblers to sawfly damaged mountain birches: novel function of inducible plant defences? Ecol Lett 7:915–918CrossRefGoogle Scholar
  30. Mehrparvar M, Mahdavi Arab N, Weisser WW (2013) Diet-mediated effects of specialized tansy aphids on survival and development of their predators: is there any benefit of dietary mixing? Biol Control 65:142–146CrossRefGoogle Scholar
  31. Mestre L, Bucher R, Entling MH (2014) Trait-mediated effects between predators: ant chemical cues induce spider dispersal. J Zool 293(2):119–125CrossRefGoogle Scholar
  32. Mooney KA, Halitschke R, Kessler A, Agrawal AA (2010) Evolutionary trade-offs in plants mediate strength of trophic cascades. Science 327:1642–1644CrossRefPubMedGoogle Scholar
  33. Mumm R, Dick M (2010) Variation in natural plant products and the attraction of bodyguards for indirect plant defence. Can J Zool 88(7):628–667CrossRefGoogle Scholar
  34. Pierre PS, Jansen JJ, Hordijk CA, van Dam NM, Cortesero AM, Dugravot S (2011) Differences in volatile profiles of turnip plants subjected to single and dual herbivory above- and belowground. J Chem Ecol 37:1–10CrossRefGoogle Scholar
  35. Poelman EH, van Loon JJA, Dicke M (2008) Consequences of variation in plant defense for biodiversity at higher trophic levels. Trends Plant Sci 13:534–541CrossRefPubMedGoogle Scholar
  36. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. Accessed 7 June 2014
  37. Rasmann S, Tobias G, Köllner J, Degenhardt IH, Stefan T, Ulrich K, Jonathan G, Ted CJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737CrossRefPubMedGoogle Scholar
  38. Rohloff J, Mordal R, Dragland S (2004) Chemotypical variation of tansy (Tanacetum vulgare L.) from 40 different locations in Norway. J Agric Food Chem 52:1742–1748CrossRefPubMedGoogle Scholar
  39. Roth S, Knorr C, Lindroth RL (1997) Dietary phenolics affects performance of the gypsy moth (Lepidoptera: Lymantriidae) and its parasitoid Cotesia melanoscela (Hymenoptera: Braconidae). Environ Entomol 26:668–671CrossRefGoogle Scholar
  40. Runyon JB, Mescher MC, De Moraes CM (2006) Volatile chemical cues guide host location and host selection by parasitic plants. Science 313:1964–1967CrossRefPubMedGoogle Scholar
  41. Schmitz OJ (2008) Herbivory from individuals to ecosystems. Annu Rev Ecol Evol Syst 39:133–152CrossRefGoogle Scholar
  42. Schmitz OJ (2010) Resolving ecosystem complexity. Monographs in population biology. Princeton University Press, PrincetonGoogle Scholar
  43. Snoeren TAL, Kappers IF, Broekgaarden C, Mumm R, Dicke M, Bouwmeester HJ (2010) Natural variation in herbivore-induced volatiles in Arabidopsis thaliana. J Exp Bot 61:3041–3056CrossRefPubMedPubMedCentralGoogle Scholar
  44. Soler R, Harvey JA, Kamp AFD, Vet LEM, Van der Putten WH, Van Dam NM, Stuefer JF, Gols R, Hordijk CA, Bezemeret TM (2007) Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals. Oikos 116:367–376CrossRefGoogle Scholar
  45. Stadler B, Dixon AFG (2008) Mutualism: ants and their insect partners. Cambridge University Press, New YorkCrossRefGoogle Scholar
  46. Van der Putten WH, Vet LEM, Harvey JA, Wäckers FL (2001) Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trees 16:547–554Google Scholar
  47. Whitham TG, Gehring CA, Lamit LJ, Wojtowicz T, Evans LM, Keith AR, Smith DS (2012) Community specificity: life and afterlife effects of genes. Trends Plant Sci 17:271–281CrossRefPubMedGoogle Scholar
  48. Wolf VC, Gassmann A, Clasen BM, Smith AG, Muller C (2012) Genetic and chemical variation of Tanacetum vulgare in plants of native and invasive origin. Biol Control 61:240–245CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • János Bálint
    • 1
  • Sharon E. Zytynska
    • 2
  • Rozália Veronika Salamon
    • 3
  • Mohsen Mehrparvar
    • 4
  • Wolfgang W. Weisser
    • 2
  • Oswald J. Schmitz
    • 5
  • Klára Benedek
    • 1
    Email author
  • Adalbert Balog
    • 1
    Email author
  1. 1.Department of Horticulture, Faculty of Technical and Human ScienceSapientia UniversityTirgu-MuresRomania
  2. 2.Terrestrial Ecology Research Group, Department of Ecology and Ecosystem Management, Centre for Food and Life Sciences WeihenstephanTechnische Universität MünchenFreising-WeihenstephanGermany
  3. 3.Department of Food Science, Faculty of Technical ScienceSapientia UniversityMiercurea CiucRomania
  4. 4.Department of Biodiversity, Institute of Science and High Technology and Environmental SciencesGraduate University of Advanced TechnologyKermanIran
  5. 5.School of Forestry and Environmental StudiesYale University New HavenUSA

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