Drought alters interactions between root and foliar herbivores

Abstract

Drought can alter plant quality and the strength of trophic interactions between herbivore groups, and is likely to increase in occurrence and severity under climate change. We hypothesized that changes in plant chemistry due to root herbivory and drought stress would affect the performance of a generalist and a specialist aphid species feeding on a Brassica plant. High drought stress increased the negative effect of root herbivory on the performance of both aphid species (30 % decrease in fecundity and 15 % reduction in intrinsic rate of increase). Aphid performance was greatest at moderate drought stress, though the two species differed in which treatment combination maximized performance. Nitrogen concentration was greatest in high and moderately drought-stressed plants without root herbivores and moderately drought-stressed plants under low root herbivore density, and correlated positively with aphid fecundity for both species. Glucosinolate concentrations increased 62 % under combined drought stress and root herbivory, and were positively correlated with extended aphid development time. Root herbivory did not influence relative water content and foliar biomass under normal water regimes but they decreased 24 and 63 %, respectively, under high drought stress. This study shows that drought can alter the strength of interactions between foliar and root herbivores, and that plant chemistry is key in mediating such interactions. The two aphid species responded in a broadly similar way to root herbivore and drought-stress treatments, which suggests that generalized predictions of the effects of abiotic factors on interactions between above- and below-ground species may be possible.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Agerbirk N, De Vos M, Kim J, Jander G (2009) Indole glucosinolate breakdown and its biological effects. Phytochem Rev 8:101–120. doi:10.1007/s11101-008-9098-0

    Article  CAS  Google Scholar 

  2. Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87:132–149. doi:10.1890/0012-9658

    Article  Google Scholar 

  3. Ahuja I, Rohloff J, Bones AM (2010) Defence mechanisms of Brassicaceae: implications for plant-insect interactions and potential for integrated pest management. A review. Agron Sustain Dev 30:311–348. doi:10.1051/agro/2009025

    Article  Google Scholar 

  4. Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK, Butterfield J, Buse A, Coulson JC, Farrar J, Good JEG, Harrington R, Hartley S, Jones TH, Lindroth RL, Press MC, Symrnioudis I, Watt AD, Whittaker JB (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Change Biol 8:1–16. doi:10.1046/j.1365-2486.2002.00451.x

    Article  Google Scholar 

  5. Bezemer TM, Jones TH (1998) Plant-insect herbivore interactions in elevated atmospheric CO2: quantitative analyses and guild effects. Oikos 82:212–222

    Article  Google Scholar 

  6. 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 101:555–562. doi:10.1034/j.1600-0706.2003.12424.x

    Article  Google Scholar 

  7. Blande JD, Pickett JA, Poppy GM (2007) A comparison of semiochemically mediated interactions involving specialist and generalist Brassica-feeding aphids and the braconid parasitoid Diaeretiella rapae. J Chem Ecol 33:767–779. doi:10.1007/s10886-007-9264-7

    PubMed  Article  CAS  Google Scholar 

  8. Cole RA (1997) The relative importance of glucosinolates and amino acids to the development of two aphid pests Brevicoryne brassicae and Myzus persicae on wild and cultivated Brassica species. Entomol Exp Appl 85:121–133. doi:10.1046/j.1570-7458.1997.00242.x

    Article  CAS  Google Scholar 

  9. Crawley MJ (2007) The R book. Wiley, West Sussex

    Google Scholar 

  10. Douglas AE (2006) Phloem-sap feeding by animals: problems and solutions. J Exp Bot 57:747–754. doi:10.1093/jxb/erj067

    PubMed  Article  CAS  Google Scholar 

  11. Finch S, Coaker TH (1969) A method for the continuous rearing of the cabbage root fly Erioischia brassicae (Bch.) and some observations on its biology. Bull Entomol Res 58:619–627. doi:10.1017/S0007485300057345

    Article  Google Scholar 

  12. Finch S, Jones TH (1989) An analysis of the deterrent effect of aphids on cabbage root fly (Delia radicum) egg-laying. Ecol Entomol 14:387–391. doi:10.1111/j.1365-2311.1989.tb00940.x

    Article  Google Scholar 

  13. Gange AC, Brown VK (1989) Effects of root herbivory by an insect on a foliar-feeding species, mediated through changes in the host plant. Oecologia 81:38–42

    Article  Google Scholar 

  14. Gols R, Bukovinszky T, van Dam N, Dicke M, Bullock J, Harvey J (2008) Performance of generalist and specialist herbivores and their endoparasitoids differs on cultivated and wild brassica populations. J Chem Ecol 34:132–143

    PubMed  Article  CAS  Google Scholar 

  15. Grace J (1997) Plant water relations. In: Crawley MJ (ed) Plant ecology. Blackwell, Oxford, pp 28–50

    Google Scholar 

  16. Hartley SE, Jones TH (2003) Plant diversity and insect herbivores: effects of environmental change in contrasting model systems. Oikos 101:6–17. doi:10.1034/j.1600-0706.2003.12566.x

    Article  Google Scholar 

  17. Heaney RK, Spinks EA, Hanley AB, Fenwick GR (1986) Technical bulletin: analysis of glucosinolates in rapeseed. AFRC, Food Research Institute, Norwich, pp 1–25

    Google Scholar 

  18. Hopkins RJ, van Dam NM, van Loon JJA (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu Rev Entomol 54:57–83. doi:10.1146/annurev.ento.54.110807.090623

    PubMed  Article  CAS  Google Scholar 

  19. Jander G, Howe G (2008) Plant interactions with arthropod herbivores: state of the field. Plant Physiol 146:801–803. doi:10.1104/pp.104.900247

    PubMed  Article  CAS  Google Scholar 

  20. 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 

  21. Jones CG, Hartley SE (1999) A protein competition model of phenolic allocation. Oikos 86:27–44. doi:10.2307/3546567

    Article  CAS  Google Scholar 

  22. Kallis G (2008) Droughts. Annu Rev Environ Resour 33:85–118. doi:10.1146/annurev.environ.33.081307.123117

    Article  Google Scholar 

  23. Kaplan I, Halitschke R, Kessler A, Rehill BJ, Sardanelli S, Denno RF (2008) Physiological integration of roots and shoots in plant defense strategies links above- and belowground herbivory. Ecol Lett 11:841–851. doi:10.1111/j.1461-0248.2008.01200.x

    PubMed  Article  Google Scholar 

  24. Kazana E, Pope TW, Tibbles L, Bridges M, Pickett JA, Bones AM, Powell G, Rossiter JT (2007) The cabbage aphid: a walking mustard oil bomb. Proc R Soc B 274:2271–2277. doi:10.1098/rspb.2007.0237

    PubMed  Article  CAS  Google Scholar 

  25. Kim JH, Jander G (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant J 49:1008–1019. doi:10.1111/j.1365-313X.2006.03019.x

    PubMed  Article  CAS  Google Scholar 

  26. King C, Jacob HS, Berlandier F (2006) The influence of water deficiency on the relationship between canola (Brassica napus L.), and two aphid species (Hemiptera: Aphididae), Lipaphis erysimi (Kaltenbach) and Brevicoryne brassicae (L.). Aust J Agric Res 57:439–445. doi:10.1071/ar05137

    Article  Google Scholar 

  27. Kuśnierczyk A, Winge P, Jørstad TS, Troczyńska J, Rossiter JT, Bones AM (2008) Towards global understanding of plant defence against aphids—timing and dynamics of early Arabidopsis defence responses to cabbage aphid (Brevicoryne brassicae) attack. Plant Cell Environ 31:1097–1115. doi:10.1111/j.1365-3040.2008.01823.x

    PubMed  Article  Google Scholar 

  28. Larsson S (1989) Stressful times for the plant stress—insect performance hypothesis. Oikos 56:277–283

    Article  Google Scholar 

  29. Leather S (1989) Do alate aphids produce fitter offspring—the influence of maternal rearing history and morph on life-history parameters of Rhopalosiphum padi (L). Funct Ecol 3:237–244

    Article  Google Scholar 

  30. Masters GJ, Brown VK, Gange AC (1993) Plant mediated interactions between aboveground and belowground insect herbivores. Oikos 66:148–151

    Article  Google Scholar 

  31. Newton E, Bullock J, Hodgson D (2009) Glucosinolate polymorphism in wild cabbage (Brassica oleracea) influences the structure of herbivore communities. Oecologia 160:63–76. doi:10.1007/s00442-009-1281-5

    PubMed  Article  Google Scholar 

  32. Newton E, Bullock J, Hodgson D (2010) Temporal consistency in herbivore responses to glucosinolate polymorphism in populations of wild cabbage (Brassica oleracea). Oecologia 164:689–699. doi:10.1007/s00442-010-1702-5

    PubMed  Article  Google Scholar 

  33. Radovich TJK, Kleinhenz MD, Streeter JG (2005) Irrigation timing relative to head development influences yield components, sugar levels, and glucosinolate concentrations in cabbage. J Am Soc Hort Sci 130:943–949

    CAS  Google Scholar 

  34. Schreiner M, Beyene B, Krumbein A, Stutzel H (2009) Ontogenetic changes of 2-Propenyl and 3-Indolylmethyl glucosinolates in Brassica carinata leaves as affected by water supply. J Agric Food Chem 57:7259–7263. doi:10.1021/jf901076h

    PubMed  Article  CAS  Google Scholar 

  35. Scriber JM, Slansky F (1981) The nutritional ecology of immature insects. Annu Rev Entomol 26:183–211. doi:10.1146/annurev.en.26.010181.001151

    Article  Google Scholar 

  36. Slansky F, Wheeler GS (1992) Caterpillars compensatory feeding response to diluted nutrients leads to toxic allelochemical dose. Entomol Exp Appl 65:171–186. doi:10.1111/j.1570-7458.1992.tb01641.x

    Article  Google Scholar 

  37. Soler R, Bezemer TM, van Der Putten WH, Vet LE, Harvey JA (2005) Root herbivore effects on above-ground herbivore, parasitoid and hyperparasitoid performance via changes in plant quality. J Anim Ecol 74:1121–1130. doi:10.1111/j.1365-2656.2005.01006.x

    Article  Google Scholar 

  38. Staley JT, Mortimer SR, Morecroft MD, Brown VK, Masters GJ (2007) Summer drought alters plant-mediated competition between foliar- and root-feeding insects. Glob Change Biol 13:866–877. doi:10.1111/j.1365-2486.2007.01338.x

    Google Scholar 

  39. Staley JT, Mortimer SR, Morecroft MD (2008) Drought impacts on above-belowground interactions: do effects differ between annual and perennial host species? Basic Appl Ecol 9:673–681. doi:10.1016/j.baac.2007.10.006

    Article  Google Scholar 

  40. Tariq M, Staley JT, Wright DJ (2010) Maternal host plant effects on aphid performance: contrasts between a generalist and a specialist species on Brussels sprout cultivars. Agric For Entomol 12:107–112. doi:10.1111/j.1461-9563.2009.00458.x

    Article  Google Scholar 

  41. Tariq M, Wright DJ, Rossiter JT, Staley JT (2012) Aphids in a changing world: testing the plant stress, plant vigour and pulsed stress hypotheses. Agric For Entomol 14:177–185. doi:10.1111/j.1461-9563.2011.00557.x

    Article  Google Scholar 

  42. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  43. van Dam NM, Raaijmakers CE (2006) Local and systemic induced responses to cabbage root fly larvae (Delia radicum) in Brassica nigra and Brassica oleracea. Chemoecology 16:17–24. doi:10.1007/s00049-005-0323-7

    Article  Google Scholar 

  44. van Dam NM, Raaijmakers CE, van der Putten WH (2005) Root herbivory reduces growth and survival of the shoot feeding specialist Pieris rapae on Brassica nigra. Entomol Exp Appl 115:161–170. doi:10.1111/j.1570-7458.2005.00241.x

    Article  Google Scholar 

  45. van der Putten WH, Macel M, Visser ME (2010) Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Philos Trans R Soc Lond B Biol Sci 365:2025–2034. doi:10.1098/rstb.2010.0037

    PubMed  Article  Google Scholar 

  46. van Emden HF (1991) The role of host plant resistance in insect pest mis-management. Bull Entomol Res 81:123–126

    Article  Google Scholar 

  47. van Leur H, Raaijmakers CE, van Dam NM (2008) Reciprocal interactions between the cabbage root fly (Delia radicum) and two glucosinolate phenotypes of Barbarea vulgaris. Entomol Exp Appl 128:312–322. doi:10.1111/j.1570-7458.2008.00722.x

    Article  Google Scholar 

  48. White TCR (1984) The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia 63:90–105

    Article  Google Scholar 

  49. White TCR (2009) Plant vigour versus plant stress: a false dichotomy. Oikos 118:807–808. doi:10.1111/j.1600-0706.2009.17495.x

    Article  Google Scholar 

  50. Wilson PR (1990) A new instrument concept for nitrogen/protein analysis—a challenge to the Kjeldahl method. Aspects Appl Biol 25:443–446

    Google Scholar 

  51. Wyatt IJ, White PF (1977) Simple estimation of intrinsic increase rates for aphids and tetranychid mites. J Appl Ecol 14:757–766

    Article  Google Scholar 

Download references

Acknowledgments

We thank Rosemary Collier (University of Warwick) for supplying D. radicum. M. T. was financially supported by the Higher Education Commission of Pakistan. Four anonymous referees helped us to improve the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Muhammad Tariq.

Additional information

Communicated by Stefan Scheu.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Tariq, M., Rossiter, J.T., Wright, D.J. et al. Drought alters interactions between root and foliar herbivores. Oecologia 172, 1095–1104 (2013). https://doi.org/10.1007/s00442-012-2572-9

Download citation

Keywords

  • Delia radicum
  • Brevicoryne brassicae
  • Glucosinolates
  • Myzus persicae
  • Nitrogen