Belowground Experimental Approaches for Exploring Aboveground–Belowground Patterns

  • Scott N. JohnsonEmail author
  • Felicity V. Crotty
  • James M. W. Ryalls
  • Philip J. Murray
Part of the Ecological Studies book series (ECOLSTUD, volume 234)


Experiments in aboveground–belowground community ecology are challenging, usually because manipulation and observation of the belowground component is problematic. Problems arise because the soil is an opaque, tri-phasic medium which restricts access and visualisation. While pot studies are commonly used to investigate aboveground–belowground interactions, they have inherent problems including a tendency to cause hypoxic conditions and elevated temperatures. A range of other techniques has been used by ecologists to manipulate belowground factors, in particular. In the laboratory, controlled manipulation includes simulated root damage experiments, split-root experiments and aboveground–belowground olfactometers. Observing belowground components in the laboratory has been achieved using slant boards, rhizotrons, rhizotubes, X-ray tomography and isotope labelling. Manipulation of belowground communities in field experiments either relies on supplementation (e.g. adding organisms) or exclusion (e.g. insecticides), both of which can have confounding effects of experimental manipulations. Observing belowground communities in the field either relies on chemically based and destructive sampling or non-destructive methods (e.g. metal tagging). Researchers continue to innovate with new techniques such as meta-barcoding showing great potential.



The authors are very grateful to Mattias Erb and Peter Gregory for reviewing this book chapter and providing valuable insights for its improvement. SNJ and JMWR acknowledge financial support from the Australian Research Council (Discovery Grants DP14100363 and DP17102278) and a Future Fellowship (FT170100342) awarded to SNJ.


  1. Alcántara C, Thornton CR, Pérez-de-Luque A et al (2016) The free-living rhizosphere fungus Trichoderma hamatum GD12 enhances clover productivity in clover–ryegrass mixtures. Plant Soil 398:165–180CrossRefGoogle Scholar
  2. Ali JG, Davidson-Lowe E (2015) Plant cues and factors influencing the behaviour of beneficial nematodes as a belowground indirect defense. In: Bais H, Sherrier J (eds) Plant microbe interactions (Advances in Botanical Research vol 75). Academic, New York, pp 191–214CrossRefGoogle Scholar
  3. Ali JG, Alborn HT, Stelinski LL (2010) Subterranean herbivore-induced volatiles released by citrus roots upon feeding by Diaprepes abbreviatus recruit entomopathogenic nematodes. J Chem Ecol 36:361–368PubMedCrossRefPubMedCentralGoogle Scholar
  4. Ali JG, Alborn HT, Stelinski LL (2011) Constitutive and induced subterranean plant volatiles attract both entomopathogenic and plant parasitic nematodes. J Ecol 99:26–35CrossRefGoogle Scholar
  5. Anderson JM (1975) The enigma of soil animal species. In: Vaněk L (ed) Progress in soil zoology: proceedings of the fifth international colloquium on progress in soil zoology. W Junk and Prague Academia, Dordrecht, pp 51–58CrossRefGoogle Scholar
  6. Arribas P, Andújar C, Hopkins K et al (2016) Metabarcoding and mitochondrial metagenomics of endogean arthropods to unveil the mesofauna of the soil. Methods Ecol Evol 7:1071–1081CrossRefGoogle Scholar
  7. Baker PB, Byers RA (1977) A laboratory technique for rearing the clover root curculio. Melsheimer Entomol Ser 23:8–10Google Scholar
  8. Ballhorn DJ, Kautz S (2013) How useful are olfactometer experiments in chemical ecology research? Commun Integr Biol 6:e24787PubMedPubMedCentralCrossRefGoogle Scholar
  9. Barnett K, Johnson SN (2013) Living in the soil matrix: abiotic factors affecting root herbivores. Adv Insect Physiol 45:1–52CrossRefGoogle Scholar
  10. Benefer CM, Blackshaw RP (2013) Molecular approaches for studying root herbivores. Adv Insect Physiol 45:220–255Google Scholar
  11. Bezemer TM, Wagenaar R, van Dam NM et al (2004) Above- and below-ground terpenoid aldehyde induction in cotton, Gossypium herbaceum, following root and leaf injury. J Chem Ecol 30:53–67PubMedCrossRefPubMedCentralGoogle Scholar
  12. Blair JM, Bohlen PJ, Edwards CA et al (1995) Manipulations of earthworm populations in field experiments in agroecosystems. Acta Zool Fenn 169:48–51Google Scholar
  13. Blossey B, Hunt-Joshi TR (2003) Belowground herbivory by insects: influence on plants and aboveground herbivores. Annu Rev Entomol 48:521–547PubMedCrossRefPubMedCentralGoogle Scholar
  14. Bohlen PJ, Parmelee RW, Blair JM et al (1995) Efficacy of methods for manipulating earthworm populations in large-scale field experiments in agroecosystems. Soil Biol Biochem 27:993–999CrossRefGoogle Scholar
  15. Böhm W (1979) Methods of studying root systems. Ecological studies, vol 33. Springer, BerlinCrossRefGoogle Scholar
  16. Bont Z, Arce C, Huber M et al (2017) A herbivore tag-and-trace system reveals contact- and density-dependent repellence of a root toxin. J Chem Ecol 43:295–306PubMedCrossRefPubMedCentralGoogle Scholar
  17. Borowicz VA (2010) The impact of arbuscular mycorrhizal fungi on strawberry tolerance to root damage and drought stress. Pedobiologia 53:265–270CrossRefGoogle Scholar
  18. Brown VK, Gange AC (1989) Differential effects of above-ground and below-ground insect herbivory during early plant succession. Oikos 54:67–76CrossRefGoogle Scholar
  19. Brussaard L, Behan-Pelletier VM, Bignell DE et al (1997) Biodiversity and ecosystem functioning in soil. Ambio 26:563–570Google Scholar
  20. Butt KR (1999) Inoculation of earthworms into reclaimed soils: the UK experience. Land Degrad Dev 10:565–575CrossRefGoogle Scholar
  21. Chahartaghi M, Langel R, Scheu S et al (2005) Feeding guilds in Collembola based on nitrogen stable isotope ratios. Soil Biol Biochem 37:1718–1725CrossRefGoogle Scholar
  22. Chung SH, Rosa C, Scully ED et al (2013) Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc Natl Acad Sci USA 110:15728–15733PubMedCrossRefPubMedCentralGoogle Scholar
  23. Clements RO, Murray PJ, Bentley 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 117:349–357CrossRefGoogle Scholar
  24. Coleman DC (2008) From peds to paradoxes: linkages between soil biota and their influences on ecological processes. Soil Biol Biochem 40:271–289CrossRefGoogle Scholar
  25. Coleman DC, MacFadyen A (1966) Recolonization of gamma-irradiated soil by small arthropods – a preliminary study. Oikos 17:62–70CrossRefGoogle Scholar
  26. Coleman DC, McGinnis JT (1970) Quantification of fungus – small arthropod food chains in soil. Oikos 21:134–137CrossRefGoogle Scholar
  27. Coleman DC, Blair JM, Elliott ET et al (1999) Soil invertebrates. In: Robertson GP, Coleman DC, Bledsoe CS et al (eds) Standards soil methods for long-term ecological research. Oxford University Press, Cary, pp 349–377Google Scholar
  28. Coleman D, Fu SL, Hendrix P et al (2002) Soil foodwebs in agroecosystems: impacts of herbivory and tillage management. Eur J Soil Biol 38:21–28CrossRefGoogle Scholar
  29. Cosby AM, Falzon GA, Trotter MG et al (2016) Risk mapping of redheaded cockchafer (Adoryphorus couloni) (Burmeister) infestations using a combination of novel k-means clustering and on-the-go plant and soil sensing technologies. Precis Agric 17:1–17CrossRefGoogle Scholar
  30. Cosme M, Lu J, Erb M et al (2016) A fungal endophyte helps plants to tolerate root herbivory through changes in gibberellin and jasmonate signaling. New Phytol 211:1065–1076PubMedPubMedCentralCrossRefGoogle Scholar
  31. Crossley DA, Blair JM (1991) A high-efficiency, low-technology Tullgren-type extractor for soil microarthropods. Agric Ecosyst Environ 34:187–192CrossRefGoogle Scholar
  32. Crotty FV, Blackshaw RP, Murray PJ (2011) Tracking the flow of bacterially derived 13C and 15N through soil faunal feeding channels. Rapid Commun Mass Spectrom 25:1503–1513PubMedCrossRefGoogle Scholar
  33. Crotty FV, Adl SM, Blackshaw RP et al (2012a) Protozoan pulses unveil their pivotal position within the soil food web. Microb Ecol 63:905–918PubMedCrossRefGoogle Scholar
  34. Crotty FV, Adl SM, Blackshaw RP et al (2012b) Using stable isotopes to differentiate trophic feeding channels within soil food webs. J Eukaryot Microbiol 59:520–526PubMedCrossRefGoogle Scholar
  35. Crotty FV, Stocki M, Knight JD et al (2013) Improving accuracy and sensitivity of isotope ratio mass spectrometry for δ 13C and δ 15N values in very low mass samples for ecological studies. Soil Biol Biochem 65:75–77CrossRefGoogle Scholar
  36. Crotty FV, Blackshaw RP, Adl SM et al (2014) Divergence of feeding channels within the soil food web determined by ecosystem type. Ecol Evol 4:1–13PubMedCrossRefGoogle Scholar
  37. D’Alessandro M, Erb M, Ton J et al (2014) Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions. Plant Cell Environ 37:813–826PubMedCrossRefGoogle Scholar
  38. Dawson LA, Byers RA (2008) Methods for studying root herbivory. In: Johnson SN, Murray PJ (eds) Root Feeders – an ecosystem perspective. CABI, Wallingford, pp 3–19CrossRefGoogle Scholar
  39. Dawson LA, Grayston SJ, Murray PJ et al (2002) Root feeding behaviour of Tipula paludosa (Meig.) (Diptera : Tipulidae) on Lolium perenne L. and Trifolium repens L. Soil Biol Biochem 34:609–615CrossRefGoogle Scholar
  40. de la Peña E, Echeverria SR, van der Putten WH et al (2006) Mechanism of control of root-feeding nematodes by mycorrhizal fungi in the dune grass Ammophila arenaria. New Phytol 169:829–840PubMedCrossRefPubMedCentralGoogle Scholar
  41. Degenhardt J, Hiltpold I, Köllner TG et al (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc Natl Acad Sci USA 106:13213–13218PubMedCrossRefPubMedCentralGoogle Scholar
  42. Dicke M, van Loon JJA (2000) Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol Exp Appl 97:237–249CrossRefGoogle Scholar
  43. Ehler LE (1998) Invasion biology and biological control. Biol Control 13:127–133CrossRefGoogle Scholar
  44. Eisenhauer N, Straube D, Scheu S (2008) Efficiency of two widespread non-destructive extraction methods under dry soil conditions for different ecological earthworm groups. Eur J Soil Biol 44:141–145CrossRefGoogle Scholar
  45. Elliott JC, Dover SD (1982) X-ray microtomography. J Microsc 126:211–213PubMedCrossRefPubMedCentralGoogle Scholar
  46. Ellmore GS, Zanne AE, Orians CM (2006) Comparative sectoriality in temperate hardwoods: hydraulics and xylem anatomy. Bot J Linn Soc 150:61–71CrossRefGoogle Scholar
  47. Erb M, Lu J (2013) Soil abiotic factors influence interactions between belowground herbivores and plant roots. J Exp Bot 64:1295–1303PubMedCrossRefGoogle Scholar
  48. Erb M, Ton J, Degenhardt J et al (2008) Interactions between arthropod-induced aboveground and belowground defenses in plants. Plant Physiol 146:867–874PubMedPubMedCentralCrossRefGoogle Scholar
  49. Erb M, Glauser G, Robert CAM (2012) Induced immunity against belowground insect herbivores- activation of defenses in the absence of a jasmonate burst. J Chem Ecol 38:629–640PubMedCrossRefGoogle Scholar
  50. Erdmann G, Otte V, Langel R et al (2007) The trophic structure of bark-living oribatid mite communities analysed with stable isotopes (15N, 13C) indicates strong niche differentiation. Exp Appl Acarol 41:1–10PubMedCrossRefPubMedCentralGoogle Scholar
  51. Erwin AC, Geber MA, Agrawal AA (2013) Specific impacts of two root herbivores and soil nutrients on plant performance and insect–insect interactions. Oikos 122:1746–1756CrossRefGoogle Scholar
  52. Filgueiras CC, Willett DS, Junior AM et al (2016a) Stimulation of the salicylic acid pathway aboveground recruits entomopathogenic nematodes belowground. PLoS One 11:e0154712PubMedPubMedCentralCrossRefGoogle Scholar
  53. Filgueiras CC, Willett DS, Pereira RV et al (2016b) Eliciting maize defense pathways aboveground attracts belowground biocontrol agents. Sci Rep 6:36484PubMedPubMedCentralCrossRefGoogle Scholar
  54. France RL, Peters RH (1997) Ecosystem differences in the trophic enrichment of 13C in aquatic food webs. Can J Fish Aquat Sci 54:1255–1258CrossRefGoogle Scholar
  55. Gange AC (2005) Sampling insects from roots. In: Leather SL (ed) Insect sampling in forest ecosystems. Blackwell Scientific Publishing, Oxford, pp 16–36CrossRefGoogle Scholar
  56. Gerard PJ (2001) Dependence of Sitona lepidus (Coleoptera: Curculionidae) larvae on abundance of white clover Rhizobium nodules. Bull Entomol Res 91:149–152PubMedPubMedCentralGoogle Scholar
  57. Giller PS (1996) The diversity of soil communities, the ‘poor man’s tropical rainforest’. Biodivers Conserv 5:135–168CrossRefGoogle Scholar
  58. Gregory PJ, Nortcliff S (2013) Soil conditions and plant growth. Wiley, ChichesterCrossRefGoogle Scholar
  59. Griffiths DW, Birch ANE, Macfarlane-Smith WH (1994) Induced changes in the indole glucosinolate content of oilseed and forage rape (Brassica napus) plants in response to either turnip root fly (Delia floralis) larval feeding or artificial root damage. J Sci Food Agric 65:171–178CrossRefGoogle Scholar
  60. Griffiths BS, Donn S, Neilson R et al (2006) Molecular sequencing and morphological analysis of a nematode community. Appl Soil Ecol 32:325–337CrossRefGoogle Scholar
  61. Gunn A, Cherrett JM (1993) The exploitation of food resources by soil meso-invertebrates and macro-invertebrates. Pedobiologia 37:303–320Google Scholar
  62. Halley JD, Burd M, Wells P (2005) Excavation and architecture of Argentine ant nests. Insect Soc 52:350–356CrossRefGoogle Scholar
  63. Harrison RD, Gardner WA, Tollner WE et al (1993) X-ray computed-tomography studies of the burrowing behavior of 4th-instar Pecan weevil (Coleoptera, Curculionidae). J Econ Entomol 86:1714–1719CrossRefGoogle Scholar
  64. Hartley SE, DeGabriel JL (2016) The ecology of herbivore-induced silicon defences in grasses. Funct Ecol 30:1311–1322CrossRefGoogle Scholar
  65. Hatch DJ, Murray PJ (1994) Transfer of nitrogen from damaged roots of white clover (Trifolium repens L.) to closely associated roots of intact perennial ryegrass (Lolium perenne L). Plant Soil 166:181–185CrossRefGoogle Scholar
  66. Hebert PDN, Gregory TR (2005) The promise of DNA barcoding for taxonomy. Syst Biol 54:852–859PubMedCrossRefPubMedCentralGoogle Scholar
  67. Hiltpold I, Erb M, Robert CAM et al (2011) Systemic root signalling in a belowground, volatile-mediated tritrophic interaction. Plant Cell Environ 34:1267–1275PubMedCrossRefPubMedCentralGoogle Scholar
  68. Hjältén J (2004) Simulating herbivory: problems and possibilities. In: Weisser WW, Siemann E (eds) Insects and ecosystem function, Ecological studies, vol 173. Springer, Berlin, pp 243–255CrossRefGoogle Scholar
  69. Hobson KA (1999) Stable-carbon and nitrogen isotope ratios of songbird feathers grown in two terrestrial biomes: implications for evaluating trophic relationships and breeding origins. Condor 101:799–805CrossRefGoogle Scholar
  70. Hol WHG, Macel M, van Veen JA et al (2004) Root damage and aboveground herbivory change concentration and composition of pyrrolizidine alkaloids of Senecio jacobaea. Basic Appl Ecol 5:253–260CrossRefGoogle Scholar
  71. Hood-Nowotny R, Knols BGJ (2007) Stable isotope methods in biological and ecological studies of arthropods. Entomol Exp Appl 124:3–16CrossRefGoogle Scholar
  72. Johansen K, Robson A, Samson P et al (2014) Mapping canegrub damage from high spatial resolution satellite imagery. Proc Aust Soc Sugar Cane Tech 36:62–70Google Scholar
  73. Johnson SN, Gregory PJ (2012) Breaking open the black box – can non-invasive imaging help answer questions in aboveground-belowground ecology? Paper presented at the aboveground-belowground interactions: technologies and new approaches. Joint Symposium of British Ecological Society, the Biochemical Society and the Society for Experimental Biology, Charles Darwin House, London, 8–10 October 2012Google Scholar
  74. Johnson SN, Murray PJ (eds) (2008) Root Feeders – an ecosystem perspective, 1st edn. CABI, WallingfordGoogle Scholar
  75. Johnson SN, Gregory PJ, Murray PJ et al (2004a) Host plant recognition by the root feeding clover weevil, Sitona lepidus (Coleoptera: Curculionidae). Bull Entomol Res 94:433–439CrossRefGoogle Scholar
  76. Johnson SN, Read DB, Gregory PJ (2004b) Tracking larval insect movement within soil using high resolution X-ray microtomography. Ecol Entomol 29:117–122CrossRefGoogle Scholar
  77. Johnson SN, Gregory PJ, Greenham JR et al (2005) Attractive properties of an isoflavonoid found in white clover root nodules on the clover root weevil. J Chem Ecol 31:2223–2229PubMedCrossRefPubMedCentralGoogle Scholar
  78. Johnson SN, Birch ANE, Gregory PJ et al (2006) The ‘mother knows best’ principle: should soil insects be included in the preference–performance debate? Ecol Entomol 31:395–401CrossRefGoogle Scholar
  79. Johnson SN, Crawford JW, Gregory PJ et al (2007) Non-invasive techniques for investigating and modelling root-feeding insects in managed and natural systems. Agric For Entomol 9:39–46CrossRefGoogle Scholar
  80. Johnson SN, Staley JT, McLeod FAL et al (2011) Plant-mediated effects of soil invertebrates and summer drought on above-ground multitrophic interactions. J Ecol 99:57–65CrossRefGoogle Scholar
  81. Johnson SN, Mitchell C, McNicol JW et al (2013) Downstairs drivers – root herbivores shape communities of above-ground herbivores and natural enemies via changes in plant nutrients. J Anim Ecol 82:1021–1030CrossRefGoogle Scholar
  82. Johnson SN, Benefer CM, Frew A et al (2016a) New frontiers in belowground ecology for plant protection from root-feeding insects. Appl Soil Ecol 108:96–107CrossRefGoogle Scholar
  83. Johnson SN, Erb M, Hartley SE (2016b) Roots under attack: contrasting plant responses to below- and aboveground insect herbivory. New Phytol 210:413–418PubMedCrossRefPubMedCentralGoogle Scholar
  84. Johnson SN, Lopaticki G, Barnett K et al (2016c) An insect ecosystem engineer alleviates drought stress in plants without increasing plant susceptibility to an above-ground herbivore. Funct Ecol 30:894–902CrossRefGoogle Scholar
  85. Kafle D, Hänel A, Lortzing T et al (2017) Sequential above- and belowground herbivory modifies plant responses depending on herbivore identity. BMC Ecol 17:5PubMedPubMedCentralCrossRefGoogle Scholar
  86. Kaplan I, Halitschke R, Kessler A et al (2008a) Constitutive and induced defenses to herbivory in above- and belowground plant tissues. Ecology 89:392–406CrossRefGoogle Scholar
  87. Kaplan I, Halitschke R, Kessler A et al (2008b) Effects of plant vascular architecture on aboveground–belowground-induced responses to foliar and root herbivores on Nicotiana tabacum. J Chem Ecol 34:1349–1359PubMedCrossRefPubMedCentralGoogle Scholar
  88. Kendall WA, Leath KT (1974) Slant-board culture methods for root observations of red clover. Crop Sci 14:317–320CrossRefGoogle Scholar
  89. King RA, Read DS, Traugott M et al (2008) Molecular analysis of predation: a review of best practice for DNA-based approaches. Mol Ecol 17:947–963PubMedCrossRefPubMedCentralGoogle Scholar
  90. Kramer S, Marhan S, Ruess L et al (2012) Carbon flow into microbial and fungal biomass as a basis for the belowground food web of agroecosystems. Pedobiologia 55:111–119CrossRefGoogle Scholar
  91. Lehtilä K, Boalt E (2008) The use and usefulness of artificial herbivory in plant-herbivore studies. In: Weisser WW, Siemann E (eds) Insects and ecosystem function. Springer, Berlin, pp 257–275CrossRefGoogle Scholar
  92. Lu J, Robert CAM, Riemann M et al (2015) Induced jasmonate signaling leads to contrasting effects on root damage and herbivore performance. Plant Physiol 167:1100–1116PubMedPubMedCentralCrossRefGoogle Scholar
  93. Mankin RW, Johnson SN, Grinev DV et al (2008) New experimental techniques for studying root herbivory. In: Johnson SN, Murray PJ (eds) Root feeders – an ecosystem perspective. CABI, Wallingford, pp 20–32CrossRefGoogle Scholar
  94. Masters GJ (1995) The impact of root herbivory on aphid performance – field and laboratory evidence. Acta Oecol 16:135–142Google Scholar
  95. Masters GJ (2004) Below-ground herbivores and ecosystem processes. In: Weisser WW, Siemann E (eds) Insects and ecosystem function. Springer, Berlin, pp 94–112Google Scholar
  96. McDougall BM (1970) Movement of 14C-photosynthate into roots of wheat seedlings and exudation of 14C from intact roots. New Phytol 69:37–46CrossRefGoogle Scholar
  97. McKenzie SW, Vanbergen AJ, Hails RS et al (2013) Reciprocal feeding facilitation by above- and below-ground herbivores. Biol Lett 9:20130341PubMedPubMedCentralCrossRefGoogle Scholar
  98. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food-chains – further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140CrossRefGoogle Scholar
  99. Moujahed R, Frati F, Cusumano A et al (2014) Egg parasitoid attraction toward induced plant volatiles is disrupted by a non-host herbivore attacking above or belowground plant organs. Front Plant Sci 5:601PubMedPubMedCentralCrossRefGoogle Scholar
  100. Murray PJ, Clements RO (1992) Studies on the feeding of Sitona lineatus L. (Coleoptera, Curculionidae) on white clover (Trifolium repens L.) seedlings. Ann Appl Biol 121:233–238CrossRefGoogle Scholar
  101. Murray PJ, Clements RO (1994) Investigations of the host feeding preferences of Sitona weevils found commonly on white clover (Trifolium repens) in the UK. Entomol Exp Appl 71:73–79CrossRefGoogle Scholar
  102. Murray PJ, Clegg CD, Crotty FV et al (2009) Dissipation of bacterially derived C and N through the meso- and macrofauna of a grassland soil. Soil Biol Biochem 41:1146–1150CrossRefGoogle Scholar
  103. Neveu N, Grandgirard J, Nenon JP et al (2002) Systemic release of herbivore-induced plant volatiles by turnips infested by concealed root-feeding larvae Delia radicum L. J Chem Ecol 28:1717–1732. Scholar
  104. Nielsen UN, Osler GHR, Campbell CD et al (2010a) The influence of vegetation type, soil properties and precipitation on the composition of soil mite and microbial communities at the landscape scale. J Biogeogr 37:1317–1328CrossRefGoogle Scholar
  105. Nielsen UN, Osler GHR, Campbell CD et al (2010b) The enigma of soil animal species diversity revisited: the role of small-scale heterogeneity. PLoS One 5(7):e11567PubMedPubMedCentralCrossRefGoogle Scholar
  106. Orgiazzi A, Dunbar MB, Panagos P et al (2015) Soil biodiversity and DNA barcodes: opportunities and challenges. Soil Biol Biochem 80:244–250CrossRefGoogle Scholar
  107. Orians CM, Jones CG (2001) Plants as resource mosaics: a functional model for predicting patterns of within-plant resource heterogeneity to consumers based on vascular architecture and local environmental variability. Oikos 94:493–504CrossRefGoogle Scholar
  108. Orians CM, Ardón M, Mohammad BA (2002) Vascular architecture and patchy nutrient availability generate within-plant heterogeneity in plant traits important to herbivores. Am J Bot 89:270–278PubMedCrossRefPubMedCentralGoogle Scholar
  109. Passioura JB (2006) The perils of pot experiments. Funct Plant Biol 33:1075–1079CrossRefGoogle Scholar
  110. Pedrotti L, Mueller MJ, Waller F (2013) Piriformospora indica root colonization triggers local and systemic root responses and inhibits secondary colonization of distal roots. PLoS One 8:e69352PubMedPubMedCentralCrossRefGoogle Scholar
  111. Pollierer MM, Langel R, Körner C et al (2007) The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol Lett 10:729–736CrossRefPubMedPubMedCentralGoogle Scholar
  112. Ponsard S, Arditi R (2000) What can stable isotopes (δ 15N and δ 13C) tell about the food web of soil macro-invertebrates? Ecology 81:852–864Google Scholar
  113. Poorter H, Bühler J, van Dusschoten D et al (2012) Pot size matters: a meta-analysis of the effects of rooting volume on plant growth. Funct Plant Biol 39:839–850CrossRefGoogle Scholar
  114. Power SA, Barnett KL, Ochoa-Huesco 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 7:1373PubMedPubMedCentralCrossRefGoogle Scholar
  115. Price EAC, Hutchings MJ, Marshall C (1996) Causes and consequences of sectoriality in the clonal herb Glechoma hederacea. Vegetatio 127:41–54CrossRefGoogle Scholar
  116. Quinn MA, Hall MH (1992) Compensatory response of a legume root-nodule system to nodule herbivory by Sitona hispidulus. Entomol Exp Appl 64:167–176CrossRefGoogle Scholar
  117. Raghu S, Dhileepan K (2005) The value of simulating herbivory in selecting effective weed biological control agents. Biol Control 34:265–273CrossRefGoogle Scholar
  118. Rasmann S, Turlings TCJ (2007) Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Ecol Lett 10:926–936CrossRefGoogle Scholar
  119. Rasmann S, Köllner TG, Degenhardt J et al (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737PubMedPubMedCentralCrossRefGoogle Scholar
  120. Rhea-Fournier D, González G (2017) Methodological considerations in the study of earthworms in forest ecosystems. In: Chakravarty S, Shukla G (eds) Forest ecology and conservation. InTech, Rijeka, pp 47–76Google Scholar
  121. Ritz K (2011) Views of the underworld: in situ visualization of soil biota. In: Ritz K, Young IM (eds) Architecture and biology of soils: life in inner space. CABI, Wallingford, pp 1–12CrossRefGoogle Scholar
  122. Robert CAM, Erb M, Duployer M et al (2012a) Herbivore-induced plant volatiles mediate host selection by a root herbivore. New Phytol 194:1061–1069CrossRefGoogle Scholar
  123. Robert CAM, Erb M, Hibbard BE et al (2012b) A specialist root herbivore reduces plant resistance and uses an induced plant volatile to aggregate in a density-dependent manner. Funct Ecol 26:1429–1440CrossRefGoogle Scholar
  124. Rostas M, Cripps MG, Silcock P (2015) Aboveground endophyte affects root volatile emission and host plant selection of a belowground insect. Oecologia 177:487–497PubMedCrossRefPubMedCentralGoogle Scholar
  125. Rushton SP, Luff ML (1984) A new electrical method for sampling earthworm populations. Pedobiologia 26:15–19Google Scholar
  126. Russell EJ (1912) Soil conditions and plant growth. Longmans, Green and Co., LondonCrossRefGoogle Scholar
  127. Ryalls JMW (2016) The impacts of climate change and belowground herbivory on aphids via primary metabolites. PhD thesis, Western Sydney University, SydneyGoogle Scholar
  128. 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 66:613–623PubMedCrossRefPubMedCentralGoogle Scholar
  129. Sapkota R, Nicolaisen M (2015) High-throughput sequencing of nematode communities from total soil DNA extractions. BMC Ecol 15:3PubMedPubMedCentralCrossRefGoogle Scholar
  130. Schädler M, Jung G, Brandl R et al (2004) Secondary succession is influenced by belowground insect herbivory on a productive site. Oecologia 138:242–252PubMedCrossRefPubMedCentralGoogle Scholar
  131. Scheu S, Falca M (2000) The soil food web of two beech forests (Fagus sylvatica) of contrasting humus type: stable isotope analysis of a macro- and a mesofauna-dominated community. Oecologia 123:285–296PubMedCrossRefPubMedCentralGoogle Scholar
  132. Schmidt O, Scrimgeour CM, Handley LL (1997) Natural abundance of 15N and 13C in earthworms from a wheat and a wheat-clover field. Soil Biol Biochem 29:1301–1308CrossRefGoogle Scholar
  133. Schneider K, Migge S, Norton RA et al (2004) Trophic niche differentiation in soil microarthropods (Oribatida, Acari): evidence from stable isotope ratios (15N/14N). Soil Biol Biochem 36:1769–1774CrossRefGoogle Scholar
  134. Schöning C, Wurst S (2016) Positive effects of root-knot nematodes (Meloidogyne incognita) on nitrogen availability do not outweigh their negative effects on fitness in Nicotiana attenuata. Plant Soil 400:381–390CrossRefGoogle Scholar
  135. Setälä H, Aarnio T (2002) Vertical stratification and trophic interactions among organisms of a soil decomposer food web – a field experiment using 15N as a tool. Eur J Soil Biol 38:29–34CrossRefGoogle Scholar
  136. Simon C, Daniel R (2011) Metagenomic analyses: past and future trends. Appl Environ Microb 77:1153–1161CrossRefGoogle Scholar
  137. 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 91:141–149PubMedCrossRefPubMedCentralGoogle Scholar
  138. Subler S, Baranski CM, Edwards CA (1997) Earthworm additions increased short-term nitrogen availability and leaching in two grain-crop agroecosystems. Soil Biol Biochem 29:413–421CrossRefGoogle Scholar
  139. Taberlet P, Coissac E, Pompanon F et al (2012) Towards next-generation biodiversity assessment using DNA metabarcoding. Mol Ecol 21:2045–2050PubMedCrossRefPubMedCentralGoogle Scholar
  140. Taina IA, Heck RJ, Elliot TR (2008) Application of X-ray computed tomography to soil science: a literature review. Can J Soil Sci 88:1–20CrossRefGoogle Scholar
  141. Tariq M, Wright DJ, Bruce TJA et al (2013) Drought and root herbivory interact to alter the response of above-ground parasitoids to aphid infested plants and associated plant volatile signals. PLoS One 8(7):e69013PubMedPubMedCentralCrossRefGoogle Scholar
  142. Thibaud M-C, Arrighi J-F, Bayle V et al (2010) Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J 64:775–789PubMedCrossRefPubMedCentralGoogle Scholar
  143. Thorn AM, Orians CM (2011) Patchy nitrate promotes inter-sector flow and 15N allocation in Ocimum basilicum: a model and an experiment. Funct Plant Biol 38:879–887CrossRefGoogle Scholar
  144. Tiunov AV (2007) Stable isotopes of carbon and nitrogen in soil ecological studies. Biol Bull 34:395–407CrossRefGoogle Scholar
  145. Torode MD, Barnett KL, Facey SL et al (2016) Altered precipitation impacts on above- and belowground grassland invertebrates: summer drought leads to outbreaks in spring. Front Plant Sci 7:1468PubMedPubMedCentralCrossRefGoogle Scholar
  146. Traugott M, Pázmándi C, Kaufmann R et al (2007) Evaluating 15N/14N and C13/C12 isotope ratio analysis to investigate trophic relationships of elaterid larvae (Coleoptera : Elateridae). Soil Biol Biochem 39:1023–1030CrossRefGoogle Scholar
  147. Turlings T, Davison A, Ricard I et al (2005) Above-and belowground olfactometers for high throughput bioassays. In: Noldus LPJJ, Grieco F, Loijens LWS, Zimmerman PH (eds) Proceedings of Measuring Behavior 2005, 5th international conference on methods and techniques in behavioral research. Wageningen, 30 August–2 September 2005. Noldus Information Technology, Wageningen, p 208Google Scholar
  148. van Dam NM, Samudrala D, Harren FJM et al (2012) Real-time analysis of sulfur-containing volatiles in Brassica plants infested with root-feeding Delia radicum larvae using proton-transfer reaction mass spectrometry. AoB Plants 2012:pls021PubMedPubMedCentralGoogle Scholar
  149. Vandegehuchte ML, de la Peña E, Bonte D (2010) Interactions between root and shoot herbivores of Ammophila arenaria in the laboratory do not translate into correlated abundances in the field. Oikos 119:1011–1019CrossRefGoogle Scholar
  150. Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182PubMedCrossRefPubMedCentralGoogle Scholar
  151. Vanholme B, De Meutter J, Tytgat T et al (2004) Secretions of plant-parasitic nematodes: a molecular update. Gene 332:13–27PubMedCrossRefPubMedCentralGoogle Scholar
  152. Wäckers FL, Bezemer TM (2003) Root herbivory induces an above-ground indirect defence. Ecol Lett 6:9–12CrossRefGoogle Scholar
  153. Wade RN, Karley AJ, Johnson SN et al (2017) Impact of predicted precipitation scenarios on multitrophic interactions. Funct Ecol 31:1647–1658CrossRefGoogle Scholar
  154. Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216PubMedGoogle Scholar
  155. Wallinger C, Juen A, Staudacher K et al (2012) Rapid plant identification using species- and group-specific primers targeting chloroplast DNA. PLoS One 7(1):e29473PubMedPubMedCentralCrossRefGoogle Scholar
  156. Wallinger C, Staudacher K, Schallhart N et al (2013) The effect of plant identity and the level of plant decay on molecular gut content analysis in a herbivorous soil insect. Mol Ecol Resour 13:75–83PubMedCrossRefGoogle Scholar
  157. Walter DE, Kethley J, Moore JC (1987) A heptane flotation method for recovering microarthropods from semiarid soils, with comparison to the Merchant-Crossley high gradient extraction method and estimates of microarthropod biomass. Pedobiologia 30:221–232Google Scholar
  158. War AR, Sharma HC, Paulraj MG et al (2011) Herbivore induced plant volatiles: their role in plant defense for pest management. Plant Signal Behav 6:1973–1978PubMedPubMedCentralCrossRefGoogle Scholar
  159. Wilkinson DM (2008) Testate amoebae and nutrient cycling: peering into the black box of soil ecology. Trends Ecol Evol 23:596–599PubMedCrossRefGoogle Scholar
  160. Wilson K, Gunn A, Cherrett JM (1995) The application of a rhizotron to study the subterranean effects of pesticides. Pedobiologia 39:132–143Google Scholar
  161. Zappala S, Helliwell JR, Tracy SR et al (2013) Effects of X-ray dose on rhizosphere studies using x-ray computed tomography. PLoS One 8(6):e67250PubMedPubMedCentralCrossRefGoogle Scholar
  162. Zhang M, Crocker RL, Mankin RW et al (2003) Acoustic identification and measurement of activity patterns of white grubs in soil. J Econ Entomol 96:1704–1710PubMedCrossRefGoogle Scholar
  163. Zvereva EL, Kozlov MV (2012) Sources of variation in plant responses to belowground insect herbivory: a meta-analysis. Oecologia 169:441–452PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Scott N. Johnson
    • 1
    Email author
  • Felicity V. Crotty
    • 2
  • James M. W. Ryalls
    • 1
    • 3
  • Philip J. Murray
    • 4
  1. 1.Hawkesbury Institute for the Environment, Western Sydney UniversityPenrithAustralia
  2. 2.Game and Wildlife Conservation TrustLeicesterUK
  3. 3.Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of ReadingReadingUK
  4. 4.Rothamsted ResearchNorth Wyke, OkehamptonUK

Personalised recommendations