Skip to main content
SpringerLink
Log in
Book cover

Aboveground–Belowground Community Ecology pp 19–46Cite as

Belowground Experimental Approaches for Exploring Aboveground–Belowground Patterns

  • Chapter
  • First Online:

Part of the book series: Ecological Studies ((ECOLSTUD,volume 234))

Abstract

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.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   99.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • 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 398:165–180

    Article  CAS  Google Scholar 

  • 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 191–214

    Chapter  Google Scholar 

  • 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 36:361–368

    Article  CAS  PubMed  Google Scholar 

  • Ali JG, Alborn HT, Stelinski LL (2011) Constitutive and induced subterranean plant volatiles attract both entomopathogenic and plant parasitic nematodes. J Ecol 99:26–35

    Article  CAS  Google Scholar 

  • 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 51–58

    Chapter  Google Scholar 

  • 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 7:1071–1081

    Article  Google Scholar 

  • Baker PB, Byers RA (1977) A laboratory technique for rearing the clover root curculio. Melsheimer Entomol Ser 23:8–10

    Google Scholar 

  • Ballhorn DJ, Kautz S (2013) How useful are olfactometer experiments in chemical ecology research? Commun Integr Biol 6:e24787

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Barnett K, Johnson SN (2013) Living in the soil matrix: abiotic factors affecting root herbivores. Adv Insect Physiol 45:1–52

    Article  Google Scholar 

  • Benefer CM, Blackshaw RP (2013) Molecular approaches for studying root herbivores. Adv Insect Physiol 45:220–255

    Google Scholar 

  • 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 30:53–67

    Article  CAS  PubMed  Google Scholar 

  • Blair JM, Bohlen PJ, Edwards CA et al (1995) Manipulations of earthworm populations in field experiments in agroecosystems. Acta Zool Fenn 169:48–51

    Google Scholar 

  • Blossey B, Hunt-Joshi TR (2003) Belowground herbivory by insects: influence on plants and aboveground herbivores. Annu Rev Entomol 48:521–547

    Article  CAS  PubMed  Google Scholar 

  • 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 27:993–999

    Article  CAS  Google Scholar 

  • Böhm W (1979) Methods of studying root systems. Ecological studies, vol 33. Springer, Berlin

    Book  Google Scholar 

  • 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 43:295–306

    Article  CAS  PubMed  Google Scholar 

  • Borowicz VA (2010) The impact of arbuscular mycorrhizal fungi on strawberry tolerance to root damage and drought stress. Pedobiologia 53:265–270

    Article  Google Scholar 

  • Brown VK, Gange AC (1989) Differential effects of above-ground and below-ground insect herbivory during early plant succession. Oikos 54:67–76

    Article  Google Scholar 

  • Brussaard L, Behan-Pelletier VM, Bignell DE et al (1997) Biodiversity and ecosystem functioning in soil. Ambio 26:563–570

    Google Scholar 

  • Butt KR (1999) Inoculation of earthworms into reclaimed soils: the UK experience. Land Degrad Dev 10:565–575

    Article  Google Scholar 

  • Chahartaghi M, Langel R, Scheu S et al (2005) Feeding guilds in Collembola based on nitrogen stable isotope ratios. Soil Biol Biochem 37:1718–1725

    Article  CAS  Google Scholar 

  • Chung SH, Rosa C, Scully ED et al (2013) Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc Natl Acad Sci USA 110:15728–15733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 117:349–357

    Article  Google Scholar 

  • Coleman DC (2008) From peds to paradoxes: linkages between soil biota and their influences on ecological processes. Soil Biol Biochem 40:271–289

    Article  CAS  Google Scholar 

  • Coleman DC, MacFadyen A (1966) Recolonization of gamma-irradiated soil by small arthropods – a preliminary study. Oikos 17:62–70

    Article  Google Scholar 

  • Coleman DC, McGinnis JT (1970) Quantification of fungus – small arthropod food chains in soil. Oikos 21:134–137

    Article  Google Scholar 

  • 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 349–377

    Google Scholar 

  • Coleman D, Fu SL, Hendrix P et al (2002) Soil foodwebs in agroecosystems: impacts of herbivory and tillage management. Eur J Soil Biol 38:21–28

    Article  Google Scholar 

  • 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 17:1–17

    Article  Google Scholar 

  • 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 211:1065–1076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crossley DA, Blair JM (1991) A high-efficiency, low-technology Tullgren-type extractor for soil microarthropods. Agric Ecosyst Environ 34:187–192

    Article  Google Scholar 

  • 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 25:1503–1513

    Article  CAS  PubMed  Google Scholar 

  • Crotty FV, Adl SM, Blackshaw RP et al (2012a) Protozoan pulses unveil their pivotal position within the soil food web. Microb Ecol 63:905–918

    Article  CAS  PubMed  Google Scholar 

  • Crotty FV, Adl SM, Blackshaw RP et al (2012b) Using stable isotopes to differentiate trophic feeding channels within soil food webs. J Eukaryot Microbiol 59:520–526

    Article  PubMed  Google Scholar 

  • 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 65:75–77

    Article  CAS  Google Scholar 

  • Crotty FV, Blackshaw RP, Adl SM et al (2014) Divergence of feeding channels within the soil food web determined by ecosystem type. Ecol Evol 4:1–13

    Article  PubMed  Google Scholar 

  • 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 37:813–826

    Article  PubMed  CAS  Google Scholar 

  • Dawson LA, Byers RA (2008) Methods for studying root herbivory. In: Johnson SN, Murray PJ (eds) Root Feeders – an ecosystem perspective. CABI, Wallingford, pp 3–19

    Chapter  Google Scholar 

  • 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 34:609–615

    Article  CAS  Google Scholar 

  • 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 169:829–840

    Article  PubMed  Google Scholar 

  • 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 106:13213–13218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dicke M, van Loon JJA (2000) Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol Exp Appl 97:237–249

    Article  CAS  Google Scholar 

  • Ehler LE (1998) Invasion biology and biological control. Biol Control 13:127–133

    Article  Google Scholar 

  • 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 44:141–145

    Article  Google Scholar 

  • Elliott JC, Dover SD (1982) X-ray microtomography. J Microsc 126:211–213

    Article  CAS  PubMed  Google Scholar 

  • Ellmore GS, Zanne AE, Orians CM (2006) Comparative sectoriality in temperate hardwoods: hydraulics and xylem anatomy. Bot J Linn Soc 150:61–71

    Article  Google Scholar 

  • Erb M, Lu J (2013) Soil abiotic factors influence interactions between belowground herbivores and plant roots. J Exp Bot 64:1295–1303

    Article  CAS  PubMed  Google Scholar 

  • Erb M, Ton J, Degenhardt J et al (2008) Interactions between arthropod-induced aboveground and belowground defenses in plants. Plant Physiol 146:867–874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 38:629–640

    Article  CAS  PubMed  Google Scholar 

  • 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 41:1–10

    Article  PubMed  Google Scholar 

  • Erwin AC, Geber MA, Agrawal AA (2013) Specific impacts of two root herbivores and soil nutrients on plant performance and insect–insect interactions. Oikos 122:1746–1756

    Article  Google Scholar 

  • Filgueiras CC, Willett DS, Junior AM et al (2016a) Stimulation of the salicylic acid pathway aboveground recruits entomopathogenic nematodes belowground. PLoS One 11:e0154712

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Filgueiras CC, Willett DS, Pereira RV et al (2016b) Eliciting maize defense pathways aboveground attracts belowground biocontrol agents. Sci Rep 6:36484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • France RL, Peters RH (1997) Ecosystem differences in the trophic enrichment of 13C in aquatic food webs. Can J Fish Aquat Sci 54:1255–1258

    Article  Google Scholar 

  • Gange AC (2005) Sampling insects from roots. In: Leather SL (ed) Insect sampling in forest ecosystems. Blackwell Scientific Publishing, Oxford, pp 16–36

    Chapter  Google Scholar 

  • Gerard PJ (2001) Dependence of Sitona lepidus (Coleoptera: Curculionidae) larvae on abundance of white clover Rhizobium nodules. Bull Entomol Res 91:149–152

    CAS  PubMed  Google Scholar 

  • Giller PS (1996) The diversity of soil communities, the ‘poor man’s tropical rainforest’. Biodivers Conserv 5:135–168

    Article  Google Scholar 

  • Gregory PJ, Nortcliff S (2013) Soil conditions and plant growth. Wiley, Chichester

    Book  Google Scholar 

  • 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 65:171–178

    Article  CAS  Google Scholar 

  • Griffiths BS, Donn S, Neilson R et al (2006) Molecular sequencing and morphological analysis of a nematode community. Appl Soil Ecol 32:325–337

    Article  Google Scholar 

  • Gunn A, Cherrett JM (1993) The exploitation of food resources by soil meso-invertebrates and macro-invertebrates. Pedobiologia 37:303–320

    Google Scholar 

  • Halley JD, Burd M, Wells P (2005) Excavation and architecture of Argentine ant nests. Insect Soc 52:350–356

    Article  Google Scholar 

  • 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 86:1714–1719

    Article  Google Scholar 

  • Hartley SE, DeGabriel JL (2016) The ecology of herbivore-induced silicon defences in grasses. Funct Ecol 30:1311–1322

    Article  Google Scholar 

  • 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 166:181–185

    Article  CAS  Google Scholar 

  • Hebert PDN, Gregory TR (2005) The promise of DNA barcoding for taxonomy. Syst Biol 54:852–859

    Article  PubMed  Google Scholar 

  • Hiltpold I, Erb M, Robert CAM et al (2011) Systemic root signalling in a belowground, volatile-mediated tritrophic interaction. Plant Cell Environ 34:1267–1275

    Article  CAS  PubMed  Google Scholar 

  • 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 243–255

    Chapter  Google Scholar 

  • 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 101:799–805

    Article  Google Scholar 

  • 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 5:253–260

    Article  CAS  Google Scholar 

  • Hood-Nowotny R, Knols BGJ (2007) Stable isotope methods in biological and ecological studies of arthropods. Entomol Exp Appl 124:3–16

    Article  CAS  Google Scholar 

  • Johansen K, Robson A, Samson P et al (2014) Mapping canegrub damage from high spatial resolution satellite imagery. Proc Aust Soc Sugar Cane Tech 36:62–70

    Google Scholar 

  • 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 2012

    Google Scholar 

  • Johnson SN, Murray PJ (eds) (2008) Root Feeders – an ecosystem perspective, 1st edn. CABI, Wallingford

    Google Scholar 

  • 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 94:433–439

    Article  CAS  PubMed  Google Scholar 

  • Johnson SN, Read DB, Gregory PJ (2004b) Tracking larval insect movement within soil using high resolution X-ray microtomography. Ecol Entomol 29:117–122

    Article  Google Scholar 

  • 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 31:2223–2229

    Article  CAS  PubMed  Google Scholar 

  • 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 31:395–401

    Article  Google Scholar 

  • 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 9:39–46

    Article  Google Scholar 

  • 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 99:57–65

    Article  Google Scholar 

  • 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 82:1021–1030

    Article  PubMed  Google Scholar 

  • Johnson SN, Benefer CM, Frew A et al (2016a) New frontiers in belowground ecology for plant protection from root-feeding insects. Appl Soil Ecol 108:96–107

    Article  Google Scholar 

  • Johnson SN, Erb M, Hartley SE (2016b) Roots under attack: contrasting plant responses to below- and aboveground insect herbivory. New Phytol 210:413–418

    Article  PubMed  Google Scholar 

  • 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 30:894–902

    Article  Google Scholar 

  • Kafle D, Hänel A, Lortzing T et al (2017) Sequential above- and belowground herbivory modifies plant responses depending on herbivore identity. BMC Ecol 17:5

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaplan I, Halitschke R, Kessler A et al (2008a) Constitutive and induced defenses to herbivory in above- and belowground plant tissues. Ecology 89:392–406

    Article  PubMed  Google Scholar 

  • 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 34:1349–1359

    Article  CAS  PubMed  Google Scholar 

  • Kendall WA, Leath KT (1974) Slant-board culture methods for root observations of red clover. Crop Sci 14:317–320

    Article  Google Scholar 

  • King RA, Read DS, Traugott M et al (2008) Molecular analysis of predation: a review of best practice for DNA-based approaches. Mol Ecol 17:947–963

    Article  CAS  PubMed  Google Scholar 

  • 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 55:111–119

    Article  CAS  Google Scholar 

  • 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 257–275

    Chapter  Google Scholar 

  • Lu J, Robert CAM, Riemann M et al (2015) Induced jasmonate signaling leads to contrasting effects on root damage and herbivore performance. Plant Physiol 167:1100–1116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 20–32

    Chapter  Google Scholar 

  • Masters GJ (1995) The impact of root herbivory on aphid performance – field and laboratory evidence. Acta Oecol 16:135–142

    Google Scholar 

  • Masters GJ (2004) Below-ground herbivores and ecosystem processes. In: Weisser WW, Siemann E (eds) Insects and ecosystem function. Springer, Berlin, pp 94–112

    Google Scholar 

  • McDougall BM (1970) Movement of 14C-photosynthate into roots of wheat seedlings and exudation of 14C from intact roots. New Phytol 69:37–46

    Article  CAS  Google Scholar 

  • McKenzie SW, Vanbergen AJ, Hails RS et al (2013) Reciprocal feeding facilitation by above- and below-ground herbivores. Biol Lett 9:20130341

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 48:1135–1140

    Article  CAS  Google Scholar 

  • 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 5:601

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 121:233–238

    Article  Google Scholar 

  • 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 71:73–79

    Article  Google Scholar 

  • 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 41:1146–1150

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.1023/A:1020500915728

    Article  CAS  PubMed  Google Scholar 

  • 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 37:1317–1328

    Article  Google Scholar 

  • 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):e11567

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Orgiazzi A, Dunbar MB, Panagos P et al (2015) Soil biodiversity and DNA barcodes: opportunities and challenges. Soil Biol Biochem 80:244–250

    Article  CAS  Google Scholar 

  • 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 94:493–504

    Article  Google Scholar 

  • 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 89:270–278

    Article  PubMed  Google Scholar 

  • Passioura JB (2006) The perils of pot experiments. Funct Plant Biol 33:1075–1079

    Article  PubMed  Google Scholar 

  • 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:e69352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pollierer MM, Langel R, Körner C et al (2007) The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol Lett 10:729–736

    Article  PubMed  Google Scholar 

  • Ponsard S, Arditi R (2000) What can stable isotopes (δ 15N and δ 13C) tell about the food web of soil macro-invertebrates? Ecology 81:852–864

    Google Scholar 

  • 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 39:839–850

    Article  PubMed  Google Scholar 

  • 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 7:1373

    Article  PubMed  PubMed Central  Google Scholar 

  • Price EAC, Hutchings MJ, Marshall C (1996) Causes and consequences of sectoriality in the clonal herb Glechoma hederacea. Vegetatio 127:41–54

    Article  Google Scholar 

  • Quinn MA, Hall MH (1992) Compensatory response of a legume root-nodule system to nodule herbivory by Sitona hispidulus. Entomol Exp Appl 64:167–176

    Article  Google Scholar 

  • Raghu S, Dhileepan K (2005) The value of simulating herbivory in selecting effective weed biological control agents. Biol Control 34:265–273

    Article  Google Scholar 

  • Rasmann S, Turlings TCJ (2007) Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Ecol Lett 10:926–936

    Article  PubMed  Google Scholar 

  • Rasmann S, Köllner TG, Degenhardt J et al (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737

    Article  CAS  PubMed  Google Scholar 

  • 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 47–76

    Google Scholar 

  • 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 1–12

    Chapter  Google Scholar 

  • Robert CAM, Erb M, Duployer M et al (2012a) Herbivore-induced plant volatiles mediate host selection by a root herbivore. New Phytol 194:1061–1069

    Article  CAS  PubMed  Google Scholar 

  • 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 26:1429–1440

    Article  Google Scholar 

  • Rostas M, Cripps MG, Silcock P (2015) Aboveground endophyte affects root volatile emission and host plant selection of a belowground insect. Oecologia 177:487–497

    Article  PubMed  Google Scholar 

  • Rushton SP, Luff ML (1984) A new electrical method for sampling earthworm populations. Pedobiologia 26:15–19

    Google Scholar 

  • Russell EJ (1912) Soil conditions and plant growth. Longmans, Green and Co., London

    Book  Google Scholar 

  • Ryalls JMW (2016) The impacts of climate change and belowground herbivory on aphids via primary metabolites. PhD thesis, Western Sydney University, Sydney

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sapkota R, Nicolaisen M (2015) High-throughput sequencing of nematode communities from total soil DNA extractions. BMC Ecol 15:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Schädler M, Jung G, Brandl R et al (2004) Secondary succession is influenced by belowground insect herbivory on a productive site. Oecologia 138:242–252

    Article  PubMed  Google Scholar 

  • 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 123:285–296

    Article  CAS  PubMed  Google Scholar 

  • 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 29:1301–1308

    Article  CAS  Google Scholar 

  • 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 36:1769–1774

    Article  CAS  Google Scholar 

  • 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 400:381–390

    Article  CAS  Google Scholar 

  • 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 38:29–34

    Article  Google Scholar 

  • Simon C, Daniel R (2011) Metagenomic analyses: past and future trends. Appl Environ Microb 77:1153–1161

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Subler S, Baranski CM, Edwards CA (1997) Earthworm additions increased short-term nitrogen availability and leaching in two grain-crop agroecosystems. Soil Biol Biochem 29:413–421

    Article  CAS  Google Scholar 

  • Taberlet P, Coissac E, Pompanon F et al (2012) Towards next-generation biodiversity assessment using DNA metabarcoding. Mol Ecol 21:2045–2050

    Article  CAS  PubMed  Google Scholar 

  • Taina IA, Heck RJ, Elliot TR (2008) Application of X-ray computed tomography to soil science: a literature review. Can J Soil Sci 88:1–20

    Article  Google Scholar 

  • 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):e69013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 64:775–789

    Article  CAS  PubMed  Google Scholar 

  • 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 38:879–887

    Article  CAS  PubMed  Google Scholar 

  • Tiunov AV (2007) Stable isotopes of carbon and nitrogen in soil ecological studies. Biol Bull 34:395–407

    Article  CAS  Google Scholar 

  • 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 7:1468

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 39:1023–1030

    Article  CAS  Google Scholar 

  • 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 208

    Google Scholar 

  • 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:pls021

    PubMed  PubMed Central  Google Scholar 

  • 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 119:1011–1019

    Article  Google Scholar 

  • Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182

    Article  PubMed  Google Scholar 

  • Vanholme B, De Meutter J, Tytgat T et al (2004) Secretions of plant-parasitic nematodes: a molecular update. Gene 332:13–27

    Article  CAS  PubMed  Google Scholar 

  • Wäckers FL, Bezemer TM (2003) Root herbivory induces an above-ground indirect defence. Ecol Lett 6:9–12

    Article  Google Scholar 

  • Wade RN, Karley AJ, Johnson SN et al (2017) Impact of predicted precipitation scenarios on multitrophic interactions. Funct Ecol 31:1647–1658

    Article  Google Scholar 

  • Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216

    CAS  PubMed  Google Scholar 

  • 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):e29473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 13:75–83

    Article  CAS  PubMed  Google Scholar 

  • 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 30:221–232

    Google Scholar 

  • War AR, Sharma HC, Paulraj MG et al (2011) Herbivore induced plant volatiles: their role in plant defense for pest management. Plant Signal Behav 6:1973–1978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilkinson DM (2008) Testate amoebae and nutrient cycling: peering into the black box of soil ecology. Trends Ecol Evol 23:596–599

    Article  PubMed  Google Scholar 

  • Wilson K, Gunn A, Cherrett JM (1995) The application of a rhizotron to study the subterranean effects of pesticides. Pedobiologia 39:132–143

    Google Scholar 

  • 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):e67250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang M, Crocker RL, Mankin RW et al (2003) Acoustic identification and measurement of activity patterns of white grubs in soil. J Econ Entomol 96:1704–1710

    Article  PubMed  Google Scholar 

  • Zvereva EL, Kozlov MV (2012) Sources of variation in plant responses to belowground insect herbivory: a meta-analysis. Oecologia 169:441–452

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Hawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW, Australia

    Scott N. Johnson & James M. W. Ryalls

  2. Game and Wildlife Conservation Trust, Leicester, UK

    Felicity V. Crotty

  3. Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of Reading, Reading, UK

    James M. W. Ryalls

  4. Rothamsted Research, North Wyke, Okehampton, UK

    Philip J. Murray

Authors
  1. Scott N. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Felicity V. Crotty
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. James M. W. Ryalls
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Philip J. Murray
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Scott N. Johnson .

Editor information

Editors and Affiliations

  1. Center for Ecological Research, Kyoto University, Shiga, Japan

    Takayuki Ohgushi

  2. Functional Biodiversity, Institute of Biology, Freie Universität, Berlin, Germany

    Susanne Wurst

  3. Hawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW, Australia

    Scott N. Johnson

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Johnson, S.N., Crotty, F.V., Ryalls, J.M.W., Murray, P.J. (2018). Belowground Experimental Approaches for Exploring Aboveground–Belowground Patterns. In: Ohgushi, T., Wurst, S., Johnson, S. (eds) Aboveground–Belowground Community Ecology. Ecological Studies, vol 234. Springer, Cham. https://doi.org/10.1007/978-3-319-91614-9_2

Download citation

Publish with us

Policies and ethics

Search

Navigation