Abstract
We investigate the response of soil microorganisms to atmospheric CO2 and temperature change within model terrestrial ecosystems in the Ecotron. The model communities consisted of four plant species (Cardamine hirsuta, Poa annua, Senecio vulgaris, Spergula arvensis), four herbivorous insect species (two aphids, a leaf-miner, and a whitefly) and their parasitoids, snails, earthworms, woodlice, soil-dwelling Collembola (springtails), nematodes and soil microorganisms (bacteria, fungi, mycorrhizae and Protista). In two successive experiments, the effects of elevated temperature (ambient plus 2 °C) at both ambient and elevated CO2 conditions (ambient plus 200 ppm) were investigated. A 40:60 sand:Surrey loam mixture with relatively low nutrient levels was used. Each experiment ran for 9 months and soil microbial biomass (Cmic and Nmic), soil microbial community (fungal and bacterial phospholipid fatty acids), basal respiration, and enzymes involved in the carbon cycling (xylanase, trehalase) were measured at depths of 0–2, 0–10 and 10–20 cm. In addition, root biomass and tissue C:N ratio were determined to provide information on the amount and quality of substrates for microbial growth.
Elevated temperature under both ambient and elevated CO2 did not show consistent treatment effects. Elevation of air temperature at ambient CO2 induced an increase in Cmic of the 0–10 cm layer, while at elevated CO2 total phospholipid fatty acids (PLFA) increased after the third generation. The metabolic quotient qCO2 decreased at elevated temperature in the ambient CO2 run. Xylanase and trehalase showed no changes in both runs. Root biomass and C:N ratio were not influenced by elevated temperature in ambient CO2. In elevated CO2, however, elevated temperature reduced root biomass in the 0–10 cm and 30–40 cm layers and increased N content of roots in the deeper layers. The different response of root biomass and C:N ratio to elevated temperature may be caused by differences in the dynamics of root decomposition and/or in allocation patterns to coarse or fine roots (i.e. storage vs. resource capture functions). Overall, our data suggests that in soils of low nutrient availability, the effects of climate change on the soil microbial community and processes are likely to be minimal and largely unpredicatable.
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References
Amato M and Ladd J N 1988 Assay for microbial biomass based on ninhydrin-reactive nitrogen in extracts of fumigated soils. Soil Biol. Biochem. 20, 107–114.
Anderson W E and Domsch K H 1978 A physiological method for quantitative measurement of microbial biomass in soils. Soil Biol. Biochem. 10, 215–221.
Bardgett R D, Kandeler E, Tscherko D, Hobbs P J, Jones T H, Thompson U and Bezemer T M 1998 Below-ground microbial community development in a high temperature world. Oikos. (in press).
Bardgett R D, Hobbs P J and Frostegård A 1996 Changes in the structure of soil microbial communities following reductions in the intensity of management of an upland grassland. Biol. Fertil. Soils 22, 261–264.
Bazzaz F A 1990 The response of natural systems to the rising of global CO2. Annu. Rev. Ecol. Syst 21, 167–196.
Bligh E G and Dyer W J 1959 A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917.
Clark H, Newton P C D, Bell C C and Glasgow E M 1995 The influence of elevated CO2 and simulated seasonal changes in temperature on tissue turnover in perennial ryegrass (Lolium perenne) and white clover (Trifolium repens) dominated pasture turves. Appl. Ecol. 32, 128–136.
Coleman D C and Crossley Jr D A 1996 Fundamentals of Soil Ecology. Academic Press, London.
Curtis P S, O'Neill E G, Teen J A, Zak D R and Pregitzer K S 1994 Below-ground responses to rising atmospheric CO2: Implications for plants, soil biota and ecosystem processes. Plant Soil 165, 1–6.
Federle T W 1986 Microbial distribution in soil — new techniques. In Perspectives in Microbial Ecology. Eds. F Megusar and M Gantar. pp. 493–498. Slovene Society for Microbiology, Ljubljana.
Frostegård A, Bååth E and Tumid A 1993a Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis. Soil Biol. Biochem. 25, 723–730.
Frostegaard Å, Tunlid A and Bååth E 1993b Phospholipid fatty acid composition, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Appl. Environ. Microbiol. 59, 3605–3617.
Houghton J T, Meira-Filho L G, Callander B A, Harris N, Kattenberg A and Maskell K 1996 Climate Change 1995: The Science of Climate Change. Cambridge University Press, Cambridge.
Hunt H W, Elliott E T, Detling J K, Monz C A and Reuss D E 1992 Plant size and shoot to root ratio in intact sods of native shortgrass prairie exposed to elevated CO2 for two growing seansons. Bull. Ecol. Soc. Am. 73, 254.
Insam H 1990 Are the soil microbial biomass and basal respiration governed by the climate regime? Soil Biol. Biochem. 22, 525–532.
Jäggi W 1976 Die Bestimmung der CO2-Bildung als Mass der bodenbiologischen Aktivitat. Schweizer Landwirtschaftliche Forschung 15, 371–380.
Jenkinson D S, Hart P B S, Rayner J H and Parry L C 1987 Modelling the turnover of organic matter in long-term experiments at Rothamsted. INTECOL Bulletin 15, 1–8.
Jenkinson D S, Adams D E and Wild A 1991 Model estimates of CO2 emissions from soil in response to global wanning. Nature 351, 304–306.
Joergensen R G and Brookes P C 1990 Ninhydrin-reactive nitrogen measurements of microbial biomass in 0.5 M K2SO4 soil extracts. Soil Biol. Biochem. 22, 1023–1027.
Jones T H, Thompson L J, Lawton J H, Bezemer T M, Bardgett R D, Blackburn T M, Bruce K D, Cannon P F, Hall G S, Hartley S E, Howson G, Jones C G, Kampichler C, Kandeler E and Ritchie D A 1998 Impacts of rising atmospheric CO2 on soil biota and processes in model terrestrial ecosystems. Science, vol. 280, 441–443.
Kaiser E A, Mueller T, Joergensen R G, Insam H and Heinemeyer 1992 Evaluation of methods to estimate the soil microbial biomass estimations and the relationship with soil texture and organic matter. Soil Biol. Biochem. 24, 675–683.
Kampichler C, Kandeler E, Bardgett R D, Jones T H and Thompson L J 1998 Impact of elevated atmospheric CO2 concentration on soil microbial biomass and activity in a complex, weedy field model ecosystem. Glob. Change Biol. 4, 335–346.
Kandeler E and Murer E 1993 Aggregate stability and soil microbial processes in a soil with different cultivation. Geoderma 56, 503–513.
Kandeler E and Böhm K 1996 Temporal dynamics of microbial biomass, xylanase activity, N-mineralisation and potential nitrification in different tillage systems. Appl. Soil Ecol. 4, 181–191.
Kemp P R, Waldecker D G, Owensby C E, Reynolds J F and Virginia R A 1994 Effects of elevated CO2 and nitrogen fertilization pretreatments on decomposition on tallgrass prairie leaf litter. Plant Soil 165, 115–127.
Kiem R and Kandeler E 1997 A simple method for the determination of trehalase activity in soils. Microbiol. Res. 152, 19–25.
Killham K 1994 Soil Ecology. Cambridge University Press, Cambridge. 242 pp.
Klironomos J N, Rilling M C and Allen M F 1996 Below-ground microbial and microfaunal responses to Artemisia tridentata under elevated atmospheric CO2. Funct. Ecol. 10, 527–534.
Lal R, Kimble J, Levine E and Stewart B A (Eds.) 1995 Soils and Global Change. CRC Lewis Publishers, Boca Raton, Florida. p 23.
Lawton J H 1996 The Ecotron facility at Silwood park: the value of ‘big bottle’ experiments. Ecology 77, 665–669.
Lawton J H, Naeem S, Woodfin R M, Brown V K, Gamge A, Godfray H C J, Heads P A, Lawler S, Magda D, Thomas C D, Thompson L J and Young S 1993 The Ecotron: a controlled environmental facility for the investigation of population and ecosystem processes. Phil. Trans. Roy. Soc. Lon., Series B 341, 181–194.
Monz C A, Hunt H W, Reeves F B and Elliott E T 1994 The response of mycorrhizal colonization to elevated CO2 and climate change in Pascopyrum smithii and Bouteloua gracilis. Plant Soil 165, 75–80.
Moorhead D L and Linkins A E 1997 Elevated CO2 alters belowground exoenzyme activities in tussock tundra. Plant Soil 189, 321–329.
Naeem S, Thompson L J, Lawler S, Lawton J H and Woodfin R M 1995 Empirical evidence that declining species diversity may alter the performance of terrestrial ecosystems. Phil. Trans. Roy. Soc. Lon., Series B, 347, 249–262.
Naeem S, Thompson L J, Jones T H, Lawler S, Lawton J H and Woodfin R M 1996 Changing community composition and elevated CO2. In Carbon Dioxide, Populations and Communities. Eds. C Körner and F A Bazzaz. pp 93–99. Academic Press, London.
O'Neill E G 1994 Responses of soil biota to elevated atmospheric carbon dioxide. Plant Soil 165, 55–65.
Raich J W and Schlesinger W H 1992 The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus 44B, 81–99.
Rice C W, Garcia F O, Hampton C O and Qwensby C E 1994 Soil microbial response in tallgrass prairie to elevated CO2. Plant Soil 165, 67–74.
Rogers H H, Runion G B and Krupa S V 1994 Plant responses to atmospheric CO2 enrichment with emphasis on roots and rhizosphere. Environ. Poll. 83, 155–189.
Ross D J, Tate K R and Newton P C D 1995 Elevated CO2 and temperature effects on soil carbon and nitrogen cycling in ryegrass/white clover turves of an Endoaquept soil. Plant Soil 176, 37–49.
Ross D J, Saggar S, Tate K R, Feltham C W and Newton P C D 1996 Elevated CO2 effects on carbon and nitrogen cycling in grass/clover turves of a Psammaquent soil. Plant Soil 182, 185–198.
Sadowsky M J and Schortemeyer M 1997 Soil microbial responses to increased concentration of atmospheric CO2. Glob. Change Biol. 3, 217–224.
Scharpenseel H W, Schomaker M and Ayoub A, Eds 1990 Soils on a Warmer Earth. Elsevier, Amsterdam.
Schinner F, Öhlinger R, Kandeler E and Margesin R 1996 Methods in Soil Biology. Springer, Berlin.
Schlesinger W H 1995 Soil respiration and changes in soil carbon stocks. In Biotic Feedbacks in the Global Climatic Systems. Eds G M Woodwell and F T Mackenze. pp 160–168. Oxford University Press, New York, Oxford.
Schortemeyer M, Hartwig U A, Hendrey G R and Sadowsky M J 1996 Microbial community changes in the rhizospheres of white clover and perennial ryegrass exposed to free air carbon dioxide enrichment (FACE). Soil Biol. Biochem. 28, 1717–1724.
Singleton P and Sainsbury D 1987 Dictionary of Microbiology and Molecular Biology. John Wiley & Sons, Chichester, New York.
Smuckner A J M, McBurney S L and Srivastava A K 1982 Quantitative separation of roots from compacted soil profiles by the Hydropneumatik Elutriation Systems. Agron. J. 74, 500–503.
Soussana J F, Casella E and Loiseau P 1996 Long-term effects of CO2 enrichment and temperature increase on temperate grass sward. II. Plant nitrogen budgets and root fraction. Plant Soil 182, 101–114.
Stemmer M, Gerzabek M H and Kandeler E 1998 Organic matter and enzyme activity in particle-size fractions of soils obtained after low-energy sonication. Soil Biol. Biochem, 30, 9–17.
Tate K R and Ross D J 1997 Elevated CO2 and moisture effects on soil carbon storage and cycling in temperate grassland. Glob. Change Biol. 3, 225–235.
Trumbore S E, Chadwick O A, Amundson R 1996 Rapid exchange beween soil carbon and atmospheric carbon dioxide driven by temperature change. Science 272, 393–396.
Tunlid A, Hoitink H A J, Low C and White D C 1989 Characterization of bacteria that suppress Rhizoctonia damping-off in bark compost media by analysis of fatty acid biomarkers. Appl. Environ. Microbiol. 55, 1368–1374.
Tunlid A and White D C 1992 Biochemical analysis of biomass, community structure, nutritional status, and metabolic activity of microbial communities in soil. In Soil Biochemistry, vol 7. Eds. G Stotzky, J M Bollag. pp 229–262. Marcel Dekker, New York.
van de Geijn S C and van Veen J A 1993 Implications of increased carbon dioxide levels for carbon input and turnover in soils. Vegetatio 104/105, 283–292.
van de Werf H. and Verstraete W. 1987 Estimation of active soil microbial biomass by mathematical analysis of respiration curves: calibration of the test procedure. Soil Biol. Biochem. 19, 261–265.
van Veen J A, Liljeroth E, Lekkerkerk L J A and van de Geijn S C 1991 Carbon fluxes in plantsoil systems at elevated atmospheric CO2 levels. Ecol. Applic. 1, 175–181.
von Mersi W and Schinner F 1996 Xylanase acticitiy. In Methods in Soil Biology. Eds. F Schinner, R Öhlinger, E Kandeler and R Margesin. pp 193–196. Springer, Berlin.
Wellbank P J, Gibbs M J, Taylor P J and Williams E D 1974 Root growth of cereal crops. Reports of Rothamsted Experimental Station for 1973, Part 2, pp. 26–66.
White D C, Davis W M, Nickels J S, King J C and Bobbie R J 1979 Determination of the sedimentary microbial biomass by extractable lipid phosphate. Oecologia 40, 51–62.
Yeates G W, Bardgett R D, Cook R, Hobbs P J, Bowling P J and Potter J F 1997 Faunal and microbial diversity in three Welsh grassland soils under conventional and organic management regimes. J Appl. Ecol. 34, 453–470.
Zak D R, Pregitzer K S, Curtis P S, Teeri J A, Fogel R and Randlett D L 1993 Elevated atmospheric CO2 and feedbacks between carbon and nitrogen cycles. Plant Soil 151, 105–117.
Zogg G P, Zak D R, Ringelberg D B, MacDonald N W, Pregitzer K S and White D C 1997 Compositional and functional shifts in microbial communities due to soil warming. Soil Sci. Soc. Am. J. 61, 475–481.
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Kandeler, E., Tscherko, D., Bardgett, R. et al. The response of soil microorganisms and roots to elevated CO2 and temperature in a terrestrial model ecosystem. Plant and Soil 202, 251–262 (1998). https://doi.org/10.1023/A:1004309623256
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DOI: https://doi.org/10.1023/A:1004309623256