, Volume 188, Issue 3, pp 777–789 | Cite as

Drought negates growth stimulation due to root herbivory in pasture grasses

  • Kirk L. BarnettEmail author
  • Scott N. Johnson
  • Sally A. Power
Plant-microbe-animal interactions - original research


Predicted increases in extreme weather are likely to alter the interactions between organisms within ecosystems. Whilst many studies have investigated the impacts of climate change on aboveground plant–insect interactions, those belowground remain relatively unexplored. Root herbivores can be the dominant taxa in grasslands, potentially altering plant community dynamics. To better predict the impact of climate change on grasslands, we subjected four Australian pasture grasses (Cynodon dactylon, Paspalum dilatatum, Microlaena stipoides and Lolium perenne) to contrasting rainfall regimes [a press drought (i.e. sustained, moderate water stress), a pulse drought (water stress followed by periodic, infrequent deluge event) and a well-watered control], with and without root herbivores; a manual root cutting treatment was also included for comparison. Plant growth, rooting strategy, phenology and biochemistry were measured to evaluate above and belowground treatment responses. Watering treatments had a larger effect on plant productivity than root damage treatments: press drought and pulse drought treatments reduced biomass by 58% and 47%, respectively. Root herbivore damage effects were species dependent and were not always equivalent to root cutting. The combination of pulse drought and root herbivory resulted in increased root:shoot ratios for both P. dilatatum and L. perenne, as well as decreased biomass and delayed flowering time for P. dilatatum. Plant biomass responses to root damage were greatest under well-watered conditions; however, root damage also delayed or prevented investment in reproduction in at least one species. Our findings highlight the important role of soil-dwelling invertebrates for forecasting growth responses of grassland communities to future rainfall regime changes.


Root damage Grassland Climate change Rainfall regime Phenology Biotic–abiotic interactions 



This research was undertaken by KLB as part of his PhD research program at the Hawkesbury Institute for the Environment at Western Sydney University. We would like to thank Anita Wesoloski, Adam Frew, Sarah Facey, William Balmont and Silvan Dobrick for their help during the course of the experiment.

Author contribution statement

KLB, SAP and SNJ conceived and designed the experiments. KLB performed the experiments, analyzed the data and drafted the manuscript. SAP and SNJ contributed to data interpretation and manuscript revisions.

Supplementary material

442_2018_4244_MOESM1_ESM.docx (435 kb)
Supplementary material 1 (DOCX 434 kb)


  1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. CrossRefGoogle Scholar
  2. Australian Bureau of Meteorology (2016) Australian climate variability and change. In: Australian Bureau of Meteorology. Accessed 20 Mar 2016
  3. Bakker JD, Colasurdo LB, Evans JR (2012) Enhancing Garry Oak seedling performance in a semiarid environment. Science 86:300–309. CrossRefGoogle Scholar
  4. Barton CVM, Ellsworth DS, Medlyn BE et al (2010) Whole-tree chambers for elevated atmospheric CO2 experimentation and tree scale flux measurements in south-eastern Australia: the Hawkesbury Forest Experiment. Agric For Meteorol 150:941–951. CrossRefGoogle Scholar
  5. Bebber D, Brown N, Speight M (2002) Drought and root herbivory in understorey Parashorea Kurz (Dipterocarpaceae) seedlings in Borneo. J Trop Ecol 18:795–804. CrossRefGoogle Scholar
  6. Bell NL, Townsend RJ, Popay AJ et al (2011) Black beetle: lessons from the past and options for the future. Pasture Persistence Grassland Res Pract Ser 15:119–124Google Scholar
  7. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 57:289–300. CrossRefGoogle Scholar
  8. Bian S, Jiang Y (2009) Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery. Sci Hortic 120:264–270. CrossRefGoogle Scholar
  9. Blackshaw RP, Kerry BR (2008) Root herbivory in agricultural ecosystems. In: Johnson SN, Murray PJ (eds) Root Feeders—an ecosystem perspective. CABI, Wallingford, pp 35–53CrossRefGoogle Scholar
  10. Bloor JMG, Pichon P, Falcimagne R et al (2010) Effects of warming, summer drought, and CO2 enrichment on aboveground biomass production, flowering phenology, and community structure in an upland grassland ecosystem. Ecosystems 13:888–900. CrossRefGoogle Scholar
  11. Blum A (1996) Crop responses to drought and the interpretation of adaptation. Plant Growth Regul 20:135–148. CrossRefGoogle Scholar
  12. Boschma S, Hill M, Scott J, Rapp G (2003) The response to moisture and defoliation stresses, and traits for resilience of perennial grasses on the Northern Tablelands of New South Wales, Australia. Crop Pasture Sci 54:903–916. CrossRefGoogle Scholar
  13. Bowler C, van Montagu M, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Biol 43:83–116. CrossRefGoogle Scholar
  14. Box GEP, Cox DR (1964) An analysis of transformations. J Roy Stat Soc Ser B (Methodol) 26:211–252Google Scholar
  15. Brown VK, Gange AC (1989) Differential effects of above-and below-ground insect herbivory during early plant succession. Oikos 54:67–76. CrossRefGoogle Scholar
  16. Carlyle CN, Fraser LH, Turkington R (2014) Response of grassland biomass production to simulated climate change and clipping along an elevation gradient. Oecologia 174:1065–1073. CrossRefPubMedGoogle Scholar
  17. Clements RO, Murray PJ, Bently BR et al (1990) The impact of pests and diseases on the herbage yield of permanent grassland at eight sites in England and Wales. Ann Appl Biol 117:349–357. CrossRefGoogle Scholar
  18. Cooke J, Leishman MR (2012) Tradeoffs between foliar silicon and carbon-based defences: evidence from vegetation communities of contrasting soil types. Oikos 121:2052–2060. CrossRefGoogle Scholar
  19. Core Team R (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  20. Crutchfield BA, Potter DA (1995) Tolerance of cool-season turf grasses to feeding by Japanese Beetle and Southern Masked Chafer (Coleoptera: Scarabaeidae) grubs. J Econ Entomol 88:1380–1387. CrossRefGoogle Scholar
  21. DaCosta M, Huang B (2007) Changes in antioxidant enzyme activities and lipid peroxidation for bentgrass species in response to drought stress. J Am Soc Hortic Sci 132:319–326Google Scholar
  22. de Deyn GB, Raaijmakers CE, Zoomer HR et al (2003) Soil invertebrate fauna enhances grassland succession and diversity. Nature 422:711–713. CrossRefPubMedGoogle Scholar
  23. Deshmukh R, Bélanger RR (2016) Molecular evolution of aquaporins and silicon influx in plants. Funct Ecol 30:1277–1285. CrossRefGoogle Scholar
  24. Dreesen FE, Boeck HJD, Janssens IA, Nijs I (2012) Summer heat and drought extremes trigger unexpected changes in productivity of a temperate annual/biannual plant community. Environ Exp Bot 79:21–30. CrossRefGoogle Scholar
  25. Eneji AE, Inanaga S, Muranaka S et al (2008) Growth and nutrient use in four grasses under drought stress as mediated by silicon fertilizers. J Plant Nutr 31:355–365. CrossRefGoogle Scholar
  26. Fay PA, Carlisle JD, Knapp AK et al (2000) Altering rainfall timing and quantity in a mesic grassland ecosystem: design and performance of rainfall manipulation shelters. Ecosystems 3:308–319. CrossRefGoogle Scholar
  27. Fay PA, Carlisle JD, Danner BT et al (2002) Altered rainfall patterns, gas exchange, and growth in grasses and forbs. Int J Plant Sci 163:549–557. CrossRefGoogle Scholar
  28. Fay PA, Carlisle JD, Knapp AK et al (2003) Productivity responses to altered rainfall patterns in a C4-dominated grassland. Oecologia 137:245–251. CrossRefGoogle Scholar
  29. Frew A, Barnett K, Riegler M et al (2016) Belowground ecology of scarabs feeding on grass roots: current knowledge and future directions for management in Australasia. Front Plant Sci 7:321. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Fry EL, Manning P, Allen DGP et al (2013) Plant functional group composition modifies the effects of precipitation change on grassland ecosystem function. PLoS One 8:e57027. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Fry EL, Manning P, Power SA (2014) Ecosystem functions are resistant to extreme changes to rainfall regimes in a mesotrophic grassland. Plant Soil 381:351–365. CrossRefGoogle Scholar
  32. Gavloski J, Whitfield G, Ellis C (1992) Effect of larvae of western corn rootworm (Coleoptera: Chrysomelidae) and of mechanical root pruning on sap flow and growth of corn. J Econ Entomol 85:1434–1441. CrossRefGoogle Scholar
  33. Gibson-Forty EVJ, Barnett KL, Tissue DT, Power SA (2016) Reducing rainfall amount has a greater negative effect on the productivity of grassland plant species than reducing rainfall frequency. Funct Plant Biol 43:380–391. CrossRefGoogle Scholar
  34. Goldson SL, Bourdot GW, Proffitt JR (1987) A study of the effects of Sitona discoideus (Coleoptera: Curculionidae) larval feeding on the growth and development of lucerne (Medicago sativa). J Appl Ecol 24:153–161. CrossRefGoogle Scholar
  35. Gong H, Zhu X, Chen K et al (2005) Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Sci 169:313–321. CrossRefGoogle Scholar
  36. Heckathorn SA, DeLucia EH (1994) Drought-induced nitrogen retranslocation in perennial C4 grasses of tallgrass prairie. Ecology 75:1877–1886. CrossRefGoogle Scholar
  37. Heckathorn SA, Delucia EH (1996) Retranslocation of shoot nitrogen to rhizomes and roots in prairie grasses may limit loss of N to grazing and fire during drought. Funct Ecol 10:396–400. CrossRefGoogle Scholar
  38. Heisler-White JL, Blair JM, Kelly EF et al (2009) Contingent productivity responses to more extreme rainfall regimes across a grassland biome. Glob Change Biol 15:2894–2904. CrossRefGoogle Scholar
  39. Henderson IF, Clements RO (1977) Grass growth in different parts of England in relation to invertebrate numbers and pesticide treatment. Grass Forage Sci 32:89–98. CrossRefGoogle Scholar
  40. Herrera CM (1985) Grass/grazer radiations: an interpretation of silica-body diversity. Oikos 45:446–447. CrossRefGoogle Scholar
  41. Hetrick BAD, Wilson GWT, Leslie JF (1991) Root architecture of warm- and cool-season grasses: relationship to mycorrhizal dependence. Can J Bot 69:112–118. CrossRefGoogle Scholar
  42. Hetrick B, Wilson G, Schwab A (1994) Mycorrhizal activity in warm-and cool-season grasses: variation in nutrient-uptake strategies. Can J Bot 72:1002–1008. CrossRefGoogle Scholar
  43. Hilbert DW (1990) Optimization of plant root: shoot ratios and internal nitrogen concentration. Ann Bot 66:91–99. CrossRefGoogle Scholar
  44. Hladun KR, Adler LS (2009) Influence of leaf herbivory, root herbivory, and pollination on plant performance in Cucurbita moschata. Ecol Entomol 34:144–152. CrossRefGoogle Scholar
  45. Hoover DL, Knapp AK, Smith MD (2014) Resistance and resilience of a grassland ecosystem to climate extremes. Ecology 95:2646–2656. CrossRefGoogle Scholar
  46. Huxman TE, Snyder KA, Tissue D et al (2004) Precipitation pulses and carbon fluxes in semiarid and arid ecosystems. Oecologia 141:254–268. CrossRefPubMedGoogle Scholar
  47. IPCC (2013) Climate change 2013: the physical science basis. Cambridge University Press, New YorkGoogle Scholar
  48. Isbell R (2002) The Australian soil classification. CSIRO, MelbourneGoogle Scholar
  49. Iwasa Y, Roughgarden J (1984) Shoot/root balance of plants: optimal growth of a system with many vegetative organs. Theor Popul Biol 25:78–105. CrossRefGoogle Scholar
  50. Jentsch A, Kreyling J, Boettcher-Treschkow J, Beierkuhnlein C (2009) Beyond gradual warming: extreme weather events alter flower phenology of European grassland and heath species. Glob Change Biol 15:837–849. CrossRefGoogle Scholar
  51. Jiang Y, Huang B (2001) Drought and heat stress injury to two cool-season turfgrasses in relation to antioxidant metabolism and lipid peroxidation contribution. Crop Sci 41:436–442. CrossRefGoogle Scholar
  52. Johnson SN, McNicol JW (2010) Elevated CO2 and aboveground-belowground herbivory by the clover root weevil. Oecologia 162:209–216. CrossRefPubMedGoogle Scholar
  53. Johnson SN, Riegler M (2013) Root damage by insects reverses the effects of elevated atmospheric CO2 on Eucalypt seedlings. PLoS ONE 8:e79479. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Jung V, Albert CH, Violle C et al (2014) Intraspecific trait variability mediates the response of subalpine grassland communities to extreme drought events. J Ecol 102:45–53. CrossRefGoogle Scholar
  55. Kahler AL, Olness AE, Sutter GR et al (1985) Root damage by western corn rootworm and nutrient content in maize. Agron J 77:769–774. CrossRefGoogle Scholar
  56. Kahmen A, Perner J, Buchmann N (2005) Diversity-dependent productivity in semi-natural grasslands following climate perturbations. Funct Ecol 19:594–601. CrossRefGoogle Scholar
  57. Kaufman PB, Dayanandan P, Franklin CI, Takeoka Y (1985) Structure and function of silica bodies in the epidermal system of grass shoots. Ann Bot 55:487–507. CrossRefGoogle Scholar
  58. Kigel J, Konsens I, Rosen N et al (2011) Relationships between flowering time and rainfall gradients across Mediterranean-desert transects. Israel J Ecol Evol 57:91–109. CrossRefGoogle Scholar
  59. Knapp AK, Harper CW, Danner BT, Lett MS (2002) Rainfall variability, carbon cycling, and plant species diversity in a mesic grassland. Science 298:2202–2205. CrossRefGoogle Scholar
  60. Knapp AK, Beier C, Briske DD et al (2008) Consequences of more extreme precipitation regimes for terrestrial ecosystems. Bioscience 58:811–821. CrossRefGoogle Scholar
  61. Knops JMH, Tilman D, Haddad NM et al (1999) Effects of plant species richness on invasion dynamics, disease outbreaks, insect abundances and diversity. Ecol Lett 2:286–293. CrossRefGoogle Scholar
  62. Lee MA, Manning P, Walker CS, Power SA (2014) Plant and arthropod community sensitivity to rainfall manipulation but not nitrogen enrichment in a successional grassland ecosystem. Oecologia 176:1173–1185. CrossRefPubMedGoogle Scholar
  63. Liang Y, Hua H, Zhu YG et al (2006) Importance of plant species and external silicon concentration to active silicon uptake and transport. New Phytol 172:63–72. CrossRefPubMedGoogle Scholar
  64. Loreau M, Naeem S, Inchausti P et al (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808. CrossRefPubMedGoogle Scholar
  65. Matthiessen JN, Ridsdill-Smith TJ (1991) Populations of African black beetle, Heteronychus arator (Coleoptera: Scarabaeidae) in a Mediterranean climate region of Australia. Bull Entomol Res 81:85–91. CrossRefGoogle Scholar
  66. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297. CrossRefGoogle Scholar
  67. McKenzie SW, Vanbergen AJ, Hails RS et al (2013) Reciprocal feeding facilitation between above- and below-ground herbivores. Biol Let 9:20130341. CrossRefGoogle Scholar
  68. McLarnon E, McQueen-Mason S, Lenk I, Hartley SE (2017) Evidence for active uptake and deposition of Si-based defenses in tall fescue. Front Plant Sci 8:1199. CrossRefPubMedPubMedCentralGoogle Scholar
  69. McNaughton SJ (1991) Dryland herbaceous perennials. In: Mooney HA, Winner WE, Pell EJ (eds) Response of plants to multiple stresses. Academic San Diego, San Diego, pp 307–321CrossRefGoogle Scholar
  70. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467. CrossRefGoogle Scholar
  71. Mitani N, Ma JF (2005) Uptake system of silicon in different plant species. J Exp Bot 56:1255–1261. CrossRefPubMedGoogle Scholar
  72. Molyneux DE, Davies WJ (1983) Rooting pattern and water relations of three pasture grasses growing in drying soil. Oecologia 58:220–224. CrossRefPubMedGoogle Scholar
  73. Nagy L, Kreyling J, Gellesch E et al (2013) Recurring weather extremes alter the flowering phenology of two common temperate shrubs. Int J Biometeorol 57:579–588. CrossRefPubMedGoogle Scholar
  74. Newman GS, Arthur MA, Muller RN (2006) Above-and belowground net primary production in a temperate mixed deciduous forest. Ecosystems 9:317–329. CrossRefGoogle Scholar
  75. Niu S, Luo Y, Li D et al (2014) Plant growth and mortality under climatic extremes: an overview. Environ Exp Bot 98:13–19. CrossRefGoogle Scholar
  76. Oksanen J, Blanchet FG, Kindt R, et al (2016) vegan: community ecology package. Accessed 6 June 2016
  77. Pearcy RW, Ehleringer J (1984) Comparative ecophysiology of C3 and C4 plants. Plant Cell Environ 7:1–13. CrossRefGoogle Scholar
  78. Power SA, Barnett KL, Ochoa Hueso R et al (2016) DRI-Grass: a new experimental platform for addressing grassland ecosystem responses to future precipitation scenarios in south-east Australia. Front Plant Sci 7:1373. CrossRefPubMedPubMedCentralGoogle Scholar
  79. Purushothaman R, Zaman-Allah M, Mallikarjuna N et al (2013) Root anatomical traits and their possible contribution to drought tolerance in grain legumes. Plant Prod Sci 16:1–8. CrossRefGoogle Scholar
  80. Radcliffe JE (1971) Effects of grass grub (Costelytra zealandica White) larvae on pasture plants. N Z J Agric Res 14:597–606. CrossRefGoogle Scholar
  81. Ratnadass A, Randriamanantsoa R, Rajaonera T et al (2013) Interaction between cropping systems and white grub (Coleoptera: Scarabeoidea) status (pest or beneficial) on upland rice. Cah Agric 22:432–441. CrossRefGoogle Scholar
  82. Reidinger S, Ramsey MH, Hartley SE (2012) Rapid and accurate analyses of silicon and phosphorus in plants using a portable X-ray fluorescence spectrometer. New Phytol 195:699–706. CrossRefPubMedGoogle Scholar
  83. Ridsdill-Smith TJ (1975) Selection of living grass roots in the soil by larvae of Sericesthis nigrolineata (Coleoptera: Scarabaeidae). Entomol Exp Appl 18:75–86. CrossRefGoogle Scholar
  84. Ridsdill-Smith TJ (1977) Effects of root-feeding by scarabaeid larvae on growth of perennial ryegrass plants. J Appl Ecol 14:73–80. CrossRefGoogle Scholar
  85. Riedell WE (1990) Rootworm and mechanical damage effects on root morphology and water relations in maize. Crop Sci 30:628–631. CrossRefGoogle Scholar
  86. Romero C, Bellés JM, Vayá JL et al (1997) Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: pleiotropic phenotypes include drought tolerance. Planta 201:293–297. CrossRefPubMedGoogle Scholar
  87. Rosario-Martinez HD (2015) phia: post-hoc interaction analysis. Accessed 28 Sep 2015
  88. Ryalls JMW, Moore BD, Riegler M et al (2015) Amino acid-mediated impacts of elevated carbon dioxide and simulated root herbivory on aphids are neutralized by increased air temperatures. J Exp Bot 66:613–623. CrossRefPubMedGoogle Scholar
  89. Schindelin J, Arganda-Carreras I, Frise E et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Meth 9:676–682. CrossRefGoogle Scholar
  90. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. CrossRefPubMedPubMedCentralGoogle Scholar
  91. Shimoyama S (1958) Effect of calcium silicate application to rice plants on the alleviation of lodging and damage from strong gales. Studies in the improvement of ultimate yields of crops by the application of silicate materials. Jpn Assoc Adv Sci 57–99Google Scholar
  92. Simberloff D, Brown BJ, Lowrie S (1978) Isopod and insect root borers may benefit Florida mangroves. Science 201:630–632. CrossRefPubMedGoogle Scholar
  93. Staley JT, Mortimer SR, Morecroft MD et al (2007) Summer drought alters plant-mediated competition between foliar- and root-feeding insects. Glob Change Biol 13:866–877. CrossRefGoogle Scholar
  94. Steinger T, Müller-Schärer H (1992) Physiological and growth responses of Centaurea maculosa (Asteraceae) to root herbivory under varying levels of interspecific plant competition and soil nitrogen availability. Oecologia 91:141–149. CrossRefPubMedGoogle Scholar
  95. Taschetto AS, England MH (2009) An analysis of late twentieth century trends in Australian rainfall. Int J Climatol 29:791–807. CrossRefGoogle Scholar
  96. Troughton A (1974) Growth and function of the root in relation to the shoot. In: Kolek J (ed) Structure and function of primary root tissues proceedings of a symposium. The Slovak Academy of Sciences, Bratislava, pp 153–164Google Scholar
  97. Turner NC, Begg JE (1981) Plant-water relations and adaptation to stress. Plant Soil 58:97–131. CrossRefGoogle Scholar
  98. van Ruijven J, De Deyn GB, Raaijmakers CE et al (2005) Interactions between spatially separated herbivores indirectly alter plant diversity. Ecol Lett 8:30–37. CrossRefGoogle Scholar
  99. Vasellati V, Oesterheld M, Medan D, Loreti J (2001) Effects of flooding and drought on the anatomy of Paspalum dilatatum. Ann Bot 88:355–360. CrossRefGoogle Scholar
  100. Violle C, Navas M-L, Vile D et al (2007) Let the concept of trait be functional! Oikos 116:882–892. CrossRefGoogle Scholar
  101. Wade RN, Karley AJ, Johnson SN, Hartley SE (2017) Impact of predicted precipitation scenarios on multitrophic interactions. Funct Ecol 31:1647–1658. CrossRefGoogle Scholar
  102. Walter J, Nagy L, Hein R et al (2011) Do plants remember drought? Hints towards a drought-memory in grasses. Environ Exp Bot 71:34–40. CrossRefGoogle Scholar
  103. Walter J, Grant K, Beierkuhnlein C et al (2012) Agriculture, ecosystems and environment increased rainfall variability reduces biomass and forage quality of temperate grassland largely independent of mowing frequency. Agric Ecosyst Environ 148:1–10. CrossRefGoogle Scholar
  104. Walter J, Jentsch A, Beierkuhnlein C, Kreyling J (2013) Ecological stress memory and cross stress tolerance in plants in the face of climate extremes. Environ Exp Bot 94:3–8. CrossRefGoogle Scholar
  105. Wilcox KR, von Fischer JC, Muscha JM et al (2015) Contrasting above- and belowground sensitivity of three great plains grasslands to altered rainfall regimes. Glob Change Biol 21:335–344. CrossRefGoogle Scholar
  106. Zhu Y, Gong H (2014) Beneficial effects of silicon on salt and drought tolerance in plants. Agron Sustain Dev 34:455–472. CrossRefGoogle Scholar
  107. Zuur AF, Ieno EN, Walker NJ et al (2009) Mixed effects models and extensions in ecology with R. Springer Science & Business Media, New YorkCrossRefGoogle Scholar
  108. Zvereva EL, Kozlov MV (2012) Sources of variation in plant responses to belowground insect herbivory: a meta-analysis. Oecologia 169:441–452. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Kirk L. Barnett
    • 1
    Email author
  • Scott N. Johnson
    • 1
  • Sally A. Power
    • 1
  1. 1.Hawkesbury Institute for the EnvironmentWestern Sydney UniversityPenrithAustralia

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