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Multitrophic effects of nutrient addition in upland grassland

Published online by Cambridge University Press:  07 February 2008

M.T. Fountain ,
V.K. Brown ,
A.C. Gange ,
W.O.C. Symondson  and
P.J. Murray
M.T. Fountain*
Affiliation:
East Malling Research, Kent ME19 6BJ, UK Centre for Agri-Environmental Research, The University of Reading, Reading RG6 6AR, UK
V.K. Brown
Affiliation:
Centre for Agri-Environmental Research, The University of Reading, Reading RG6 6AR, UK
A.C. Gange
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Surrey TW20 0EX, UK
W.O.C. Symondson
Affiliation:
Cardiff School of Biosciences, Cardiff University, PO Box 915, Cardiff CF10 3TL, UK
P.J. Murray
Affiliation:
Cross Institute Programme for Sustainable Soil Function, Institute of Grassland and Environmental Research, Devon EX20 2SB, UK
*
*Author for correspondence Fax: +44 (0) 1732 849067 E-mail: michelle.fountain@emr.ac.uk
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Abstract

Although the effects of nutrient enhancement on aquatic systems are well documented, the consequences of nutritional supplements on soil food webs are poorly understood, and results of past research examining bottom-up effects are often conflicting. In addition, many studies have failed to separate the effects of nutrient enrichment and the physical effects of adding organic matter. In this field study, we hypothesised that the addition of nitrogen to soil would result in a trophic cascade, through detritivores (Collembola) to predators (spiders), increasing invertebrate numbers and diversity.

Nitrogen and lime were added to plots in an upland grassland in a randomised block design. Populations of Collembola and spiders were sampled by means of pitfall traps and identified to species.

Seventeen species of Collembola were identified from the nitrogen plus lime (N+L) and control plots. Species assemblage, diversity, richness, evenness and total number were not affected by nutrient additions. However, there was an increase in the number of Isotomidae juveniles and Parisotoma anglicana trapped in the N+L plots.

Of the 44 spider species identified, over 80% were Linyphiidae. An effect on species assemblage from the addition of N+L to the plots was observed on two of the four sampling dates (July 2002 and June 2003). The linyphiid, Oedothorax retusus, was the only species significantly affected by the treatments and was more likely to be trapped in the control plots.

The increased number of juvenile Collembola, and change in community composition of spiders, were consequences of the bottom-up effect caused by nutrient inputs. However, despite efforts to eliminate the indirect effects of nutrient inputs, a reduction in soil moisture in the N+L plots cannot be eliminated as a cause of the invertebrate population changes observed. Even so, this experiment was not confounded by the physical effects of habitat structure reported in most previous studies. It provides evidence of moderate bottom-up influences of epigeic soil invertebrate food webs and distinguishes between nutrient addition and plant physical structure effects. It also emphasises the importance of understanding the effects of soil management practices on soil biodiversity, which is under increasing pressure from land development and food production.

Keywords

bottom-upCollembolacommunity structurelimenitrogenspiders
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 98 , Issue 3 , June 2008 , pp. 283 - 292
Copyright
Copyright © 2008 Cambridge University Press

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References

Agustí, N., Shayler, S.P., Harwood, J.D., Vaughan, I.P., Sunderland, K.D. & Symondson, W.O.C. (2003) Collembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers. Molecular Ecology 12, 3467–3475.CrossRefGoogle ScholarPubMed
Axelsen, J.A. & Kristensen, K.T. (2000) Collembola and mites in plots fertilised with different types of green manure. Pedobiologia 44, 556–566.CrossRefGoogle Scholar
Bell, J.R., Bohan, D.A., Shaw, E.M. & Weyman, G.S. (2005) Ballooning dispersal using silk: world fauna, phylogienies, genetics and models. Bulletin of Entomological Research 95, 69–114.CrossRefGoogle ScholarPubMed
Berg, M.P. & Hemerik, L. (2004) Secondary succession of terrestrial isopod, centipede, and millipede communities in grasslands under restoration. Biology and Fertility of Soils 40, 163–170.CrossRefGoogle Scholar
Bird, S., Coulson, R.N. & Crossley, D.A. (2000) Impacts of silvicultural practices on soil and litter arthropod diversity in a Texas pine plantation. Forest Ecology and Management 131, 65–80.CrossRefGoogle Scholar
Bonkowski, M. (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytologist 162, 617–631.CrossRefGoogle ScholarPubMed
Bradford, M.A., Jones, T.H., Bardgett, R.D., Black, H.I.J., Boag, B., Bonkowski, M., Cook, R., Eggers, T., Gange, A.C., Grayston, S.J., Kandeler, E., McCaig, A.E., Newington, J.E., Prosser, J.I., Setala, H., Staddon, P.L., Tordoff, G.M. & Tscherko, D. (2002) Impacts of soil faunal community composition on model grassland ecosystems. Science 298, 615–618.CrossRefGoogle ScholarPubMed
Burt-Smith, G. (2003) Sourhope Field Experiment Report IV (1999–2002) The Macaulay Institute. Aberdeen.Google Scholar
Chapin, F.S., Walker, B.H., Hobbs, R.J., Hopper, D.U., Lawton, J.H., Sala, O.E. & Tilman, D. (1997) Biotic control over the functioning of ecosystem. Science 277, 500–503.CrossRefGoogle Scholar
Chen, B. & Wise, D.H. (1999) Bottom-up limitation of predaceous arthropods in a detritus-based terrestrial food web. Ecology 80, 761–772.CrossRefGoogle Scholar
Cole, L., Buckland, S.M. & Bardgett, R.D. (2005) Relating microarthropod community structure and diversity to soil fertility manipulation in temperate grassland. Soil Biology and Biochemistry 37, 1707–1717.CrossRefGoogle Scholar
Coulson, J.C. & Butterfield, J. (1986) The spider communities on peat and upland grassland in northern England. Holarctic Ecology 9, 229–239.Google Scholar
Davidson, D.A., Bruneau, P.M.C., Grieve, I.C. & Young, I.M. (2002) Impacts of fauna on an upland grassland soil as determined by micromorphological analysis. Applied Soil Ecology 20, 133–143.CrossRefGoogle Scholar
De Deyn, G.B., Raaijmakers, C.E. & Van der Putten, W.H. (2004) Plant community development is affected by nutrients and soil biota. Journal of Ecology 92, 824–834.CrossRefGoogle Scholar
Denno, R.F., Gratton, C., Dobel, H. & Finke, D.L. (2003) Predation risk affects relative strength of top-down and bottom-up impacts on insect herbivores. Ecology 84, 1032–1044.CrossRefGoogle Scholar
Fagan, W.F. & Denno, R.F. (2004) Stoichiometry of actual vs. potential predator-prey interactions: insights into nitrogen limitation for arthropod predators. Ecology Letters 7, 876–883.CrossRefGoogle Scholar
Fjellberg, A. (1998) The Collembola of Fennoscandinavia and Denmark. Part I. Poduromorpha. Fauna Entomologica Scandinavica 35, 183 pp. Leiden, The Netherlands, Brill.Google Scholar
Fountain, M.T. & Hopkin, S.P. (2004) A comparative study of the effects of metal contamination on Collembola in the field and in the laboratory. Ecotoxicology 13, 573–587.CrossRefGoogle ScholarPubMed
Frampton, G.K. (2002) Long-term impacts of an organophosphate-based regime of pesticides on field and field-edge Collembola communities. Pest Management Science 58, 991–1001.CrossRefGoogle ScholarPubMed
Gange, A. (2000) Arbuscular mycorrhizal fungi, Collembola and plant growth. TREE 15, 369–372.Google ScholarPubMed
Gange, A.C. & Brown, V.K. (2002) Soil food web components affect plant community structure during early succession. Ecological Research 17, 217–227.CrossRefGoogle Scholar
Gange, A.C. & Nice, H.E. (1997) Performance of the thistle gall fly, Urophora cardui, in relation to host plant nitrogen and mycorrhizal colonization. New Phytologist 137, 335–343.CrossRefGoogle ScholarPubMed
Gratton, C. & Denno, R.F. (2003) Inter-year carryover effects of a nutrient pulse on Spartina plants, herbivores, and natural enemies. Ecology 84, 2692–2707.CrossRefGoogle Scholar
Hairston, N.G. & Hairston, N.G.J. (1993) Cause-effect relationships in energy-flow, trophic structure, and interspecific interactions. Amateur Naturalist 142, 379–411.CrossRefGoogle Scholar
Halaj, J. & Wise, D.H. (2002) Impact of a detrital subsidy on trophic cascades in a terrestrial grazing food web. Ecology 83, 3141–3151.CrossRefGoogle Scholar
Harvey, P.R., Nellist, D.R. & Telfer, M.G. (2002) Provisional Atlas of British Spiders (Arachnida, Araneae), Volumes 1 & 2. Huntingdon, UK, Biological Records Centre.Google Scholar
Harwood, J.D., Sunderland, K.D. & Symondson, W.O.C. (2003) Web-location by linyphiid spiders: prey-specific aggregation and foraging strategies. Journal of Animal Ecology 72, 745–756.CrossRefGoogle Scholar
Harwood, J.D., Sunderland, K.D. & Symondson, W.O.C. (2004) Prey selection by linyphiid spiders: molecular tracking of the effects of alternative prey on rates of aphid consumption in the field. Molecular Ecology 13, 3549–3560.CrossRefGoogle ScholarPubMed
Hemerik, L. & Brussaard, L. (2002) Diversity of soil macro-invertebrates in grasslands under restoration succession. European Journal of Soil Biology 38, 145–150.CrossRefGoogle Scholar
Hooper, D.U., Chapin, F.S., Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J.H., Lodge, D.M., Loreau, M., Naeem, S., Schmid, B., Setala, H., Symstad, A.J., Vandermeer, J. & Wardle, D.A. (2005) Effects of biodiversity on ecosystem functioning: A consensus of current knowledge. Ecological Monographs 75, 3–35.CrossRefGoogle Scholar
Hopkin, S.P. (2000). A key to the Springtails of Britain and Ireland. AID GAP (Aids to Identification in Difficult Groups of Animals and Plants), test version.Google Scholar
Huhta, V., Karppinen, E., Nurminen, M. & Valpas, A. (1967) Effects of silvicultural practices upon arthropod, annelid and nematode populations in coniferous forest soil. Annales Zoologici Fennici 4, 58–143.Google Scholar
Huhta, V., Nurminen, M. & Valpas, A. (1969) Further notes on the effect of silvicultural practices upon the fauna of coniferous forest soil. Annales Zoologici Fennici 6, 327–334.Google Scholar
Huhta, V., Persson, T. & Setala, H. (1998) Functional implications of soil fauna diversity in boreal forests. Applied Soil Ecology 10, 277–288.CrossRefGoogle Scholar
Jefferies, R.L. (1999) Herbivores, nutrients and trophic cascades in terrestrial environments.Google Scholar
Kajak, A. (1995) The role of soil predators in decomposition processes. European Journal of Entomology 92, 573–580.Google Scholar
Laakso, J. & Setälä, H. (1999) Sensitivity of primary production to changes in the architecture of belowground food webs. Oikos 87, 57–64.CrossRefGoogle Scholar
Lindberg, N. & Persson, T. (2004) Effects of long-term nutrient fertilisation and irrigation on the microarthropod community in a boreal Norway spruce stand. Forest Ecology and Management 188, 125–135.CrossRefGoogle Scholar
Lohm, U., Lundkvist, H., Persson, T. & Wirén, A. (1977) Effects of nitrogen fertilization on the abundance of enchytraeids and microarthropods in Scots pine forests. Studia Forestalia Suecica 140, 1–23.Google Scholar
Marc, P., Canard, A. & Ysnel, F. (1999) Spiders (Araneae) useful for pest limitation and bioindication. Agriculture Ecosystems and Environment 74, 229–273.CrossRefGoogle Scholar
Marcussen, B.M., Axelsen, J.A. & Toft, S. (1999) The value of two Collembola species as food for a linyphiid spider. Entomologia Experimentalis et Applicata 92, 29–36.CrossRefGoogle Scholar
Masters, G.J., Brown, V.K. & Gange, A.C. (1993) Plant mediated interactions between above and belowground insect herbivores. Oikos 66, 148–151.CrossRefGoogle Scholar
Moore, J.C., McCann, K., Setala, H. & De Ruiter, P.C. (2003) Top-down is bottom-up: Does predation in the rhizosphere regulate aboveground dynamics? Ecology 84, 846–857.CrossRefGoogle Scholar
Moretti, M., Conedera, M., Duelli, P. & Edwards, P.J. (2002) The effects of wildfire on ground-active spiders in deciduous forests on the Swiss southern slope of the Alps. Journal of Applied Ecology 39, 321–336.CrossRefGoogle Scholar
Murray, P.J., Cook, R., Currie, A.F., Dawson, L.A., Gange, A.C., Grayston, S.J. & Treonis, A.M. (2006) Interactions between fertilizer addition, plants and the soil environment: implications for soil faunal structure and diversity. Applied Soil Ecology 33, 199–207.CrossRefGoogle Scholar
Naeem, S., Thompson, L.J., Lawler, S.P., Lawton, J.H. & Woodfin, R.W. (1994) Declining biodiversity can alter the performance of ecosystems. Nature 368, 734–737.CrossRefGoogle Scholar
Niklaus, P.A., Alphei, D., Ebersberger, D., Kampichler, C., Kandeler, E. & Tscherko, D. (2003) Six years of in situ CO2 enrichment evoke changes in soil structure and soil biota of nutrient-poor grassland. Global Change Biology 9, 585–600.CrossRefGoogle Scholar
Ormerod, S.J. & Rundle, S.D. (1998) Effects of experimental acidification and liming on terrestrial invertebrates: implications for calcium availability to vertebrates. Environmental Pollution 103, 183–191.CrossRefGoogle Scholar
Polis, G.A. & Strong, D.R. (1996) Food web complexity and community dynamics. Amateur Naturalist 147, 813–846.CrossRefGoogle Scholar
Roberts, M.J. (1993) The spiders of Great Britain and Ireland. Vols 1–3. pp. 209, 224, 256. Colchester, UK, Harley Books.Google Scholar
Rodwell, J.S. (1992) British Plant Communities Volume 3. Grasslands and montane communities. 550 pp. Cambridger, UK, Cambridge University Press.Google Scholar
Rusek, J. & Marshall, V.G. (2000) Impacts of airborne pollutants on soil fauna. Annual Reviews of Ecology 31, 395–423.CrossRefGoogle Scholar
Rushton, S.P., Topping, C.J. & Eyre, M.D. (1987) The habitat preferences of grassland spiders as identified using Detrended Correspondence Analysis (DECORANA). Bulletin of the British Arachnological Scociety. 7, 165–170.Google Scholar
Rypstra, A.L. & Marshall, S.D. (2005) Augmentation of soil detritus affects the spider community and herbivory in a soybean agroecosystems. Entomologia Experimentalis et Applicata 116, 149–157.CrossRefGoogle Scholar
Salamon, J.A., Alphei, J., Ruf, A., Schaefer, M., Scheu, S., Schneider, K., Suhrig, A. & Maraun, M. (2006) Transitory dynamic effects in the soil invertebrate community in a temperate deciduous forest: Effects of resource quality. Soil Biology and Biochemistry 38, 209–221.CrossRefGoogle Scholar
Salminen, J., Setala, H. & Haimi, J. (1997) Regulation of decomposer community structure and decomposition processes in herbicide stressed humus soil. Applied Soil Ecology 6, 265–274.CrossRefGoogle Scholar
Santos, P.F., Phillips, J. & Whitford, W.G. (1981). The role of mites and nematodes in early stages of buried litter decomposition in a desert. Ecology 62, 664–669.CrossRefGoogle Scholar
Scheu, S. & Schaefer, M. (1998) Bottom-up control of the soil macrofauna community in a beechwood on limestone: Manipulation of food resources. Ecology 79, 1573–1585.CrossRefGoogle Scholar
Schmitz, O.J. (1993) Trophic extrapolation in grassland food chains: simple models and a field experiment. Oecologia 93, 327–335.CrossRefGoogle Scholar
Schmitz, O.J. (1994) Resource edibility and trophic extrapolation in an old-field food web. Proceedings of the National Academy of Science (USA) 91, 5364–5367.CrossRefGoogle Scholar
Siemann, E. (1998) Experimental tests of effects of plant productivity and diversity on grassland arthropod diversity. Ecology 79, 2057–2070.CrossRefGoogle Scholar
Smit, C.E., Schouten, A.J., Van den Brink, P.J., van Esbroek, M.L.P. & Posthuma, L. (2002) Effects of zinc contamination on a natural nematode community in outdoor soil mesocosms. Archives of Environmental Contamination and Toxicology 42, 205–216.Google ScholarPubMed
Strong, D.R., Whipple, A.V., Child, A.L. & Dennis, B. (1999) Model selection for a subterranean trophic cascade: Root-feeding caterpillars and entomopathogenic nematodes. Ecology 80, 2750–2761.CrossRefGoogle Scholar
Symondson, W.O.C., Glen, D.M., Wiltshire, C.W., Langdon, C.J. & Liddell, J.E. (1996) Effects of cultivation techniques and methods of straw disposal on predation by Pterostichus melanarius (Coleoptera: Carabidae) upon slugs (Gastropoda: Pulmonata) in an arable field. Journal of Applied Ecology 33, 741–753.CrossRefGoogle Scholar
Thornhill, W.A. (1983) The distribution and probable importance of linyphiid spiders living on the soil surface of sugar-beet fields. Bulletin of the British Arachnological Society 6, 127–136.Google Scholar
Wardle, D.A. (1999) Biodiversity, ecosystems and interactions that transcend the interface. TREE 14, 125–127.Google Scholar
Wardle, D.A., Yeates, G.W., Watson, R.N. & Nicholson, K.S. (1995) The detritus food-web and the diversity of soil fauna as indicators of disturbance regimes in agroecosystems. Plant and Soil 170, 35–43.CrossRefGoogle Scholar
Wardle, D.A., Verhoef, H.A. & Clarholm, M. (1998) Trophic relationships in the soil microfood-web: predicting the responses to a changing global environment. Global Change Biology 4, 713–727.CrossRefGoogle Scholar
Wardle, D.A., Yeates, G.W., Williamson, W.M., Bonner, K.I. & Barker, G.M. (2004a). Linking aboveground and belowground communities: the indirect influence of aphid species identity and diversity on a three trophic level soil food web. Oikos 107, 283–294.CrossRefGoogle Scholar
Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Setala, H., van der Putten, W.H. & Wall, D.H. (2004b) Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633.CrossRefGoogle ScholarPubMed
Wardle, D.A., Williamson, W.M., Yeates, G.W. & Bonner, K.I. (2005) Trickle-down effects of aboveground trophic cascades on the soil food web. Oikos 111, 348–358.CrossRefGoogle Scholar
Wise, D.H. (2004) Wandering spiders limit densities of a major micro-detritivore in the forest-floor food web. Pedobiologia 48, 181–188.CrossRefGoogle Scholar
Wise, D.H. & Chen, B. (1999) Vertebrate predation does not limit density of a common forest-floor wolf spider: evidence from a field experiment. Oikos 84, 209–214.CrossRefGoogle Scholar