Oecologia

, Volume 175, Issue 1, pp 187–198 | Cite as

Sequential effects of root and foliar herbivory on aboveground and belowground induced plant defense responses and insect performance

  • Minggang Wang
  • Arjen Biere
  • Wim H. Van der Putten
  • T. Martijn Bezemer
Plant-microbe-animal interactions - Original research

Abstract

Plants are often simultaneously or sequentially attacked by multiple herbivores and changes in host plants induced by one herbivore can influence the performance of other herbivores. We examined how sequential feeding on the plant Plantago lanceolata by the aboveground herbivore Spodoptera exigua and the belowground herbivore Agriotes lineatus influences plant defense and the performance of both insects. Belowground herbivory caused a reduction in the food consumption by the aboveground herbivore independent of whether it was initiated before, at the same time, or after that of the aboveground herbivore. By contrast, aboveground herbivory did not significantly affect belowground herbivore performance, but significantly reduced the performance of later arriving aboveground conspecifics. Interestingly, belowground herbivores negated negative effects of aboveground herbivores on consumption efficiency of their later arriving conspecifics, but only if the belowground herbivores were introduced simultaneously with the early arriving aboveground herbivores. Aboveground–belowground interactions could only partly be explained by induced changes in an important class of defense compounds, iridoid glycosides (IGs). Belowground herbivory caused a reduction in IGs in roots without affecting shoot levels, while aboveground herbivory increased IG levels in roots in the short term (4 days) but only in the shoots in the longer term (17 days). We conclude that the sequence of aboveground and belowground herbivory is important in interactions between aboveground and belowground herbivores and that knowledge on the timing of exposure is essential to predict outcomes of aboveground–belowground interactions.

Keywords

Aboveground–belowground interactions Induced defense Iridoid glycosides Secondary plant compounds Timing 

Notes

Acknowledgments

We thank Ciska Raaijmakers, Roel Wagenaar, Jinghua Huang, Minghui Fei and Jingying Jing for the technical help and two anonymous reviewers for their helpful comments on a previous version of the manuscript. This work was funded by a grant from the China Scholarship Council (no. 2011630083 to M. G. W.). This is publication no. 5567 of the Netherlands Institute of Ecology (NIOO-KNAW).

Conflict of interest

The authors acknowledge that there are no conflicts of interest and that the experiments comply with the current laws of the Netherlands where the experiments were performed.

References

  1. Bennett AE, Macrae AM, Moore BD, Caul S, Johnson SN (2013) Early root herbivory impairs arbuscular mycorrhizal fungal colonization and shifts defence allocation in establishing Plantago lanceolata. Plos One 8:e66053PubMedCentralPubMedCrossRefGoogle Scholar
  2. Bezemer TM, Van Dam NM (2005) Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol Evol 20:617–624PubMedCrossRefGoogle Scholar
  3. Bezemer TM, Wagenaar R, Van Dam NM, Wäckers FL (2003) Interactions between above- and belowground insect herbivores as mediated by the plant defense system. Oikos 101:555–562CrossRefGoogle Scholar
  4. Bezemer TM, Wagenaar R, Van Dam NM, Van der Putten WH, Wäckers FL (2004) Above- and below-ground terpenoid aldehyde induction in cotton, Gossypium herbaceum, following root and leaf injury. J Chem Ecol 30:53–67PubMedCrossRefGoogle Scholar
  5. Biere A, Marak HB, Van Damme JMM (2004) Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs? Oecologia 140:430–441PubMedCrossRefGoogle Scholar
  6. Blossey B, Hunt-Joshi TR (2003) Belowground herbivory by insects: influence on plants and aboveground herbivores. Annu Rev Entomol 48:521–547PubMedCrossRefGoogle Scholar
  7. Boldt PE, Biever KD, Ignoffo CM (1975) Lepidopteran pests of soybeans—consumption of soybean foliage and pods and development time. J Econ Entomol 68:480–482Google Scholar
  8. Bowers MD, Puttick GM (1989) Iridoid glycosides and insect feeding preferences—gypsy moths (Lymantria dispar, Lymantriidae) and buckeyes (Junonia coenia, Nymphalidae). Ecol Entomol 14:247–256CrossRefGoogle Scholar
  9. Bowers MD, Stamp NE (1992) Chemical variation within and between individuals of Plantago lanceolata (Plantaginaceae). J Chem Ecol 18:985–995PubMedCrossRefGoogle Scholar
  10. Bowers MD, Stamp NE (1993) Effects of plant-age, genotype, and herbivory on Plantago performance and chemistry. Ecology 74:1778–1791CrossRefGoogle Scholar
  11. Darrow K, Bowers MD (1999) Effects of herbivore damage and nutrient level on induction of iridoid glycosides in Plantago lanceolata. J Chem Ecol 25:1427–1440CrossRefGoogle Scholar
  12. De Deyn GB, Biere A, Van der Putten WH, Wagenaar R, Klironomos JN (2009) Chemical defense, mycorrhizal colonization and growth responses in Plantago lanceolata L. Oecologia 160:433–442PubMedCrossRefGoogle Scholar
  13. Erb M, Flors V, Karlen D, De Lange E, Planchamp C, D’Alessandro M, Turlings TCJ, Ton J (2009) Signal signature of aboveground-induced resistance upon belowground herbivory in maize. Plant J 59:292–302PubMedCrossRefGoogle Scholar
  14. Erb M, Robert CAM, Hibbard BE, Turlings TCJ (2011) Sequence of arrival determines plant-mediated interactions between herbivores. J Ecol 99:7–15CrossRefGoogle Scholar
  15. Fuchs A, Bowers MD (2004) Patterns of iridoid glycoside production and induction in Plantago lanceolata and the importance of plant age. J Chem Ecol 30:1723–1741PubMedCrossRefGoogle Scholar
  16. Gomez S, Orians CM, Preisser EL (2012) Exotic herbivores on a shared native host: tissue quality after individual, simultaneous, and sequential attack. Oecologia 169:1015–1024PubMedCrossRefGoogle Scholar
  17. Harvey JA, Van Nouhuys S, Biere A (2005) Effects of quantitative variation in allelochemicals in Plantago lanceolata on development of a generalist and a specialist herbivore and their endoparasitoids. J Chem Ecol 31:287–302PubMedCrossRefGoogle Scholar
  18. Johnson SN, Clark KE, Hartley SE, Jones TH, McKenzie SW, Koricheva J (2012) Aboveground–belowground herbivore interactions: a meta-analysis. Ecology 93:2208–2215PubMedCrossRefGoogle Scholar
  19. Kaplan I, Denno RF (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10:977–994PubMedCrossRefGoogle Scholar
  20. Kaplan I, Halitschke R, Kessler A, Sardanelli S, Denno RF (2008) Constitutive and induced defenses to herbivory in above- and belowground plant tissues. Ecology 89:392–406PubMedCrossRefGoogle Scholar
  21. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  22. Marak HB, Biere A, Van Damme JMM (2002a) Systemic, genotype-specific induction of two herbivore-deterrent iridoid glycosides in Plantago lanceolata L. in response to fungal infection by Diaporthe adunca (Rob.) Niessel. J Chem Ecol 28:2429–2448PubMedCrossRefGoogle Scholar
  23. Marak HB, Biere A, Van Damme JMM (2002b) Two herbivore-deterrent iridoid glycosides reduce the in vitro growth of a specialist but not of a generalist pathogenic fungus of Plantago lanceolata L. Chemoecology 12:185–192CrossRefGoogle Scholar
  24. Maron JL (1998) Insect herbivory above- and belowground: individual and joint effects on plant fitness. Ecology 79:1281–1293CrossRefGoogle Scholar
  25. Masters GJ, Brown VK, Gange AC (1993) Plant mediated interactions between aboveground and belowground insect herbivores. Oikos 66:148–151CrossRefGoogle Scholar
  26. Merkx-Jacques M, Despland E, Bede JC (2008) Nutrient utilization by caterpillars of the generalist beet armyworm, Spodoptera exigua. Physiol Entomol 33:51–61CrossRefGoogle Scholar
  27. Nieminen MJ, Suomi J, Van Nouhuys S, Sauri P, Riekkola ML (2003) Effect of iridoid glycoside content on oviposition host plant choice and parasitism in a specialist herbivore. J Chem Ecol 29:823–844PubMedCrossRefGoogle Scholar
  28. Parker WE, Howard JJ (2001) The biology and management of wireworms (Agriotes spp.) on potato with particular reference to the UK. Agric For Entomol 3:85–98CrossRefGoogle Scholar
  29. Poelman EH, Broekgaarden C, Van Loon JJA, Dicke M (2008) Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Mol Ecol 17:3352–3365PubMedCrossRefGoogle Scholar
  30. Quintero C, Bowers MD (2011) Plant induced defenses depend more on plant age than previous history of damage: implications for plant-herbivore interactions. J Chem Ecol 37:992–1001PubMedCrossRefGoogle Scholar
  31. Rasmann S, Agrawal AA, Cook SC, Erwin AC (2009) Cardenolides, induced responses, and interactions between above- and belowground herbivores of milkweed (Asclepias spp.). Ecology 90:2393–2404PubMedCrossRefGoogle Scholar
  32. Reudler Talsma JH, Biere A, Harvey JA, Van Nouhuys S (2008) Oviposition cues for a specialist butterfly—plant chemistry and size. J Chem Ecol 34:1202–1212PubMedCentralPubMedCrossRefGoogle Scholar
  33. Reudler Talsma JH, Biere A, Harvey JA, Van Nouhuys S (2011) Differential performance of a specialist and two generalist herbivores and their parasitoids on Plantago lanceolata. J Chem Ecol 37:765–778CrossRefGoogle Scholar
  34. Singh P, Unnithan GC, Delobel AGL (1983) An artificial diet for sorghum shootfly larvae. Entomol Exp Appl 33:122–124CrossRefGoogle Scholar
  35. Soler R, Bezemer TM, Cortesero AM, Van der Putten WH, Vet LEM, Harvey JA (2007) Impact of foliar herbivory on the development of a root-feeding insect and its parasitoid. Oecologia 152:257–264PubMedCentralPubMedCrossRefGoogle Scholar
  36. Sutter R, Müller C (2011) Mining for treatment-specific and general changes in target compounds and metabolic fingerprints in response to herbivory and phytohormones in Plantago lanceolata. New Phytol 191:1069–1082PubMedCrossRefGoogle Scholar
  37. Van Dam NM, Raaijmakers CE (2006) Local and systemic induced responses to cabbage root fly larvae (Delia radicum) in Brassica nigra and B. oleracea. Chemoecology 16:17–24CrossRefGoogle Scholar
  38. Van Dam NM, Witjes L, Svatos A (2004) Interactions between aboveground and belowground induction of glucosinolates in two wild Brassica species. New Phytol 161:801–810CrossRefGoogle Scholar
  39. Van der Putten WH, Vet LEM, Harvey JA, Wäckers FL (2001) Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol Evol 16:547–554CrossRefGoogle Scholar
  40. Viswanathan DV, Lifchits OA, Thaler JS (2007) Consequences of sequential attack for resistance to herbivores when plants have specific induced responses. Oikos 116:1389–1399CrossRefGoogle Scholar
  41. Voelckel C, Baldwin IT (2004) Herbivore-induced plant vaccination. Part II. Array-studies reveal the transience of herbivore-specific transcriptional imprints and a distinct imprint from stress combinations. Plant J 38:650–663PubMedCrossRefGoogle Scholar
  42. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633PubMedCrossRefGoogle Scholar
  43. Wurst S, Van der Putten WH (2007) Root herbivore identity matters in plant-mediated interactions between root and shoot herbivores. Basic Appl Ecol 8:491–499CrossRefGoogle Scholar
  44. Wurst S, Van Dam NM, Monroy F, Biere A, Van der Putten WH (2008) Intraspecific variation in plant defense alters effects of root herbivores on leaf chemistry and aboveground herbivore damage. J Chem Ecol 34:1360–1367PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Minggang Wang
    • 1
  • Arjen Biere
    • 1
  • Wim H. Van der Putten
    • 1
    • 2
  • T. Martijn Bezemer
    • 1
  1. 1.Department of Terrestrial EcologyNetherlands Institute of Ecology (NIOO-KNAW)WageningenThe Netherlands
  2. 2.Laboratory of NematologyWageningen UniversityWageningenThe Netherlands

Personalised recommendations