Soil biological indicators; bacterial metabolic potential; potentialrespiration; microbial biomass; net nitrogen mineralization; tree species
Abstract :
[en] Biological indicators, measurements based on the presence and activity of soil organisms, are increasingly being considered in assessments of forest soil quality. In addition to chemical indicators, such as soil organic carbon and pH, biological indicators can provide an early diagnosis of changes in soil functions and processes in response to environmental change and forest management actions. We investigated the spatial and temporal variability of selected bio-indicators in the forest floor of two catchments over three years. We further evaluated the sensitivity of these indicators to changes in the dominant tree species following reforestation and natural regeneration. Indicators of microbial abundance and activity (microbial biomass, potential respiration) and carbon maintenance costs (metabolic quotient) were higher under young spruce and mixed deciduous stands than pure stands of oak and beech. Our results indicate a greater microbial activity in the autumn but a wider range of carbon substrate utilisation in the spring. Evaluation of seasonal differences in bio-indicator values is vital for the evaluation and planning of long-term studies and the development of reference values for forest soils in Belgium. Our results highlight the usefulness of these bio-indicators in identifying changes in soil functioning, particularly in response to management activities, at small spatial scales.
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Bibliography
Alderweireld, M., Burnay, F., Pitchugin, M., Lecomte, H., 2015. Inventaire Forestier Wallon. Résultats 1994-2012. SPW, DGO3, DNF, Direction des Ressources Forestières, Jambes.
Allen, D.E., Singh, B.P., Dalal, R.C., Soil health indicators under climate change: a review of current knowledge. Singh, B.P., Cowie, A.L., Chan, K.Y., (eds.) Soil Health and Climate Change, 2011, Springer-Verlag, Berlin Heidelberg, 25–45, 10.1007/978-3-642-20256-8.
Allen, S.E., Chemical Analysis of Ecological Materials. 2nd ed., 1989, Blackwell Scientific Publications, Oxford.
Anderson, T.-H., Domsch, K.H., Application of eco-physiological quotients (qCO2 and qD) on microbial biomasses from soils of diferent cropping histories. Soil Biol. Biochem. 22 (1990), 251–255.
Anderson, T.-H., Domsch, K.H., The metabolic quotient for CO2 (qCO2) as a specific activity parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils. Soil Biol. Biochem. 25 (1993), 393–395, 10.1016/0038-0717(93)90140-7.
Augusto, L., Ranger, J., Binkley, D., Rothe, A., Impact of several common tree species of European temperate forests on soil fertility. Annu. For. Sci. 59 (2002), 233–253, 10.1051/forest.
Bardgett, R.D., Bowman, W.D., Kaufmann, R., Schmidt, S.K., A temporal approach to linking aboveground and belowground ecology. Trends Ecol. Evol. 20 (2005), 634–641, 10.1016/j.tree.2005.08.005.
Bartoń, K., 2016. MuMIn: Multi-Model Inference.
Bates, D., Maechler, M., Bolker, B.M., Walker, S.C., Fitting linear mixed-effects models using lme4. J. Stat. Softw. 76 (2015), 1–48, 10.18637/jss.v067.i01.
Bauhus, J., Khanna, P.K., The significance of microbial biomass and activity in forest soils. Rastin, N., Bauhus, J., (eds.) Going Underground – Ecological Studies in Forest Soils, 1999, Research Signpost, Trivandrum, India, 77–110.
Bauhus, J., Pare, D., Cote, L., Effects of tree species, stand age and soil type on soil microbial biomass and its activity in a southern boreal forest. Soil Biol. Biochem. 30 (1998), 1077–1089.
Bauhus, J., Puettmann, K.J., Kühne, C., 2013. Close-to-nature forest management in Europe. In: Messier, C., Puettmann, K.J., Coates, K.D. (Eds.), Managing Forests as Complex Adaptive Systems: Building Resilience to the Challenge of Global Change. Routledge, pp. 187–213. doi: 10.4324/9780203122808.
Bending, G.D., Turner, M.K., Rayns, F., Marx, M., Wood, M., Microbial and biochemical soil quality indicators and their potential for differentiating areas under contrasting agricultural management regimes. Soil Biol. Biochem. 36 (2004), 1785–1792, 10.1016/j.soilbio.2004.04.035.
Bennett, E.M., Peterson, G.D., Gordon, L.J., Understanding relationships among multiple ecosystem services. Ecol. Lett. 12 (2009), 1394–1404, 10.1111/j.1461-0248.2009.01387.x.
Binkley, D., 1996. The Influence of tree species on forest soils: processes and patterns. In: Mead, D.J., Cornforth, I.S. (Eds.), Trees and Soils Workshop. Agronomy Society of New Zealand Special Publication #10, Canterbury, pp. 1–33.
Binkley, D., Giardina, C., Why do tree species affect soils? The Warp and Woof of tree – soil Interactions. Biogeochemistry 42 (1998), 89–106, 10.1023/A.
Brang, P., Spathelf, P., Larsen, J.B., Bauhus, J., Bončìna, A., Chauvin, C., Drössler, L., García-Güemes, C., Heiri, C., Kerr, G., Lexer, M.J., Mason, B., Mohren, F., Mühlethaler, U., Nocentini, S., Svoboda, M., Suitability of close-to-nature silviculture for adapting temperate European forests to climate change. Forestry 87 (2014), 492–503, 10.1093/forestry/cpu018.
Brant, J.B., Myrold, D.D., Sulzman, E.W., Root controls on soil microbial community structure in forest soils. Oecologia 148 (2006), 650–659, 10.1007/s00442-006-0402-7.
Brookes, P.C., Landman, A., Pruden, G., Jenkinson, D.S., Chloroform funigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol. Biochem. 17 (1985), 837–842.
Burnham, K.P., Anderson, D.R., Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Second. ed., 2002, Springer, New York.
Carnol, M., Bazgir, M., Nutrient return to the forest floor through litter and throughfall under 7 forest species after conversion from Norway spruce. For. Ecol. Manage. 309 (2013), 66–75, 10.1016/j.foreco.2013.04.008.
Chen, F., Zheng, H., Zhang, K., Ouyang, Z., Lan, J., Li, H., Shi, Q., Changes in soil microbial community structure and metabolic activity following conversion from native Pinus massoniana plantations to exotic Eucalyptus plantations. For. Ecol. Manage. 291 (2013), 65–72, 10.1016/j.foreco.2012.11.016.
Clements, W.H., Rohr, J.R., Community responses to contaminants: using basic ecological principals to predict ecotoxicological effects. Environ. Toxicol. Chem. 28 (2009), 1789–1800.
Cluzeau, D., Guernion, M., Chaussod, R., Martin-Laurent, F., Villenave, C., Cortet, J., Ruiz-Camacho, N., Pernin, C., Mateille, T., Philippot, L., Bellido, A., Rougé, L., Arrouays, D., Bispo, A., Pérès, G., Integration of biodiversity in soil quality monitoring: baselines for microbial and soil fauna parameters for different land-use types. Eur. J. Soil Biol. 49 (2012), 63–72, 10.1016/j.ejsobi.2011.11.003.
Cotrufo, M.F., Wallenstein, M.D., Boot, C.M., Denef, K., Paul, E.A., The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter?. Global Change Biol. 19 (2013), 988–995, 10.1111/gcb.12113.
Delgado-Baquerizo, M., Maestre, F.T., Reich, P.B., Jeffries, T.C., Gaitan, J.J., Encinar, D., Berdugo, M., Campbell, C.D., Singh, B.K., Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat. Commun. 7 (2016), 1–8, 10.1038/ncomms10541.
Doran, J.W., Zeiss, M.R., Soil health and sustainability: managing the biotic component of soil quality. Appl. Soil Ecol. 15 (2000), 3–11.
Fontaine, S., Mariotti, A., Abbadie, L., The priming effect of organic matter: a question of microbial competition?. Soil Biol. Biochem. 35 (2003), 837–843, 10.1016/S0038-0717(03)00123-8.
Ghani, A., Dexter, M., Perrott, K.W., Hot-water extractable carbon in soils: a sensitive measurement for determining impacts of fertilisation, grazing and cultivation. Soil Biol. Biochem. 35 (2003), 1231–1243, 10.1016/S0038-0717(03)00186-X.
Giraudoux, P., 2017. pgirmess: Data Analysis in Ecology. R Package Version 1.6.7.
Grayston, S.J., Vaughan, D., Jones, D., Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl. Soil Ecol. 5 (1996), 29–56.
Haack, S.K., Garchow, H., Klug, M.J., Forney, L.J., Analysis of factors affecting the accuracy, reproducibility, and interpretation of microbial community carbon source utilization patterns†. Appl. Environ. Microbiol. 61 (1995), 1458–1468.
Hart, S.C., Stark, J.M., Davidson, E.A., Firestone, M.K., Nitrogen mineralization, immobilisation and nitrification. Sparks, D.L., (eds.) Methods of Soil Science Analysis, Part II, 1994, Soil Science Society of America, Madison, 985–1018.
Hättenschwiler, S., Tiunov, A., Scheu, S., Biodiversity and litter deomposition in terrestrial ecosystems. Annu. Rev. Ecol. Evol. 36 (2005), 191–218, 10.1146/annurev.ecolsys.36.112904.151932.
Haynes, R.J., Labile organic matter fractions as central components of the quality of agricultural soils: an overview. Adv. Agron. 85 (2005), 221–268.
Haynes, R.J., Francis, G.S., Changes in microbial biomass C, soil carbohydrate composition and aggregate stability induced by growth of selected crop and forage species under field conditions. J. Soil Sci. 44 (1993), 665–675.
Hendershot, W.H., Duquette, M., A simple barium chloride for determining cation exchange capacity and exchangeable cations. J. Soil Soc. Am. 50 (1986), 605–608.
Insam, H., Goberna, M., Use of Biolog for the community level physiological profiling (CLPP) of environmental samples. Kowalchuk, G.A., de Bruijn, F., Head, I.M., Van der Zijpp, A.J., van Elsas, J.D., (eds.) Molecular Microbial Ecology Manual, 2004, Springer, The Netherlands, 853–860.
Jenkinson, D.S., Powlson, D.S., The effects of biocidal treatments on metabolism in soil: V. A method for measuring soil biomass. Soil Biol. Biochem. 8 (1976), 209–213.
Karlen, D.L., Mausbach, M.J., Doran, J.W., Cline, R.G., Harris, R.F., Schuman, G.E., Soil quality: a concept, definition, and framework for evaluation. Soil Sci. Soc. Am. J. 61 (1997), 4–10.
Kennedy, A., Stubbs, T., Soil microbial communities as indicators of soil health. Ann. Arid Zone 45 (2006), 287–308.
Kirschbaum, M.U.F., Will changes in soil organic carbon act as a positive or negative feedback on global warming ?. Biogeochemistry 48 (2000), 21–51.
Konopka, A., Oliver, L., Turco, R.F. Jr., The use of carbon substrate utilization patterns in environmental and ecological microbiology. Microb. Ecol. 35 (1998), 103–115, 10.1007/s002489900065.
Lemanceau, P., Creamer, R.E., Griffiths, B.S., Soil biodiversity and ecosystem functions across Europe: a transect covering variations in bio-geographical zones, land use and soil properties. Appl. Soil Ecol. 97 (2016), 1–2, 10.1016/j.apsoil.2015.07.017.
Malchair, S., Halen, S., Moutier, M., Carnol, M., Appréciation des indicateurs biologiques comme outils d’évaluation de la qualité des sols. 2010, Rapport final de la convention ULg-SPW, Liège.
Menzel, A., Sparks, T.H., Estrella, N., Koch, E.W., Aasa, A., Ahas, R., Alm-Kübler, K., Bissolli, P., Braslavská, O., Briede, A., Chmielewski, F.M., Crepinsek, Z., Curnel, Y., Dahl, Å., Defila, C., Donnelly, A., Filella, Y., Jatczak, K., Måge, F., Mestre, A., Nordli, Ø., Peñuelas, J., Pirinen, P., Remišová, V., Scheifinger, H., Striz, M., Susnik, A., van Vliet, A.J.H., Wielgolaski, F.-E., Zach, S., Zust, A., European phenological response to climate change matches the warming pattern. Global Change Biol. 12 (2006), 1969–1976, 10.1111/j.1365-2486.2006.01193.x.
Ministry for Social Affairs, H. and E., 2009. Climate Change Belgium. Belgium's Fifth Natl. Commun. under United Nations Framew. Conv. Clim. Chang. Available from: < https://www.climatechangepost.com/belgium/climate-change/> (accessed 08.03.17).
Moscatelli, M.C., Lagomarsino, A., Marinari, S., de Angelis, P., Grego, S., Soil microbial indices as bioindicators of environmental changes in a poplar plantation. Ecol. Indic. 5 (2005), 171–179, 10.1016/j.ecolind.2005.03.002.
Nohrstedt, H.Ö., Nitrogen fixation (C2H2-reduction) in birch litter. Scand. J. For. Res. 3 (1988), 17–23, 10.1080/02827588809382491.
Parkin, T.B., Spatial variability of microbial processes in soil – a review. J. Environ. Qual., 22, 1993, 409, 10.2134/jeq1993.00472425002200030004x.
Pérès, G., Vandenbulcke, F., Guernion, M., Hedde, M., Beguiristain, T., Douay, F., Houot, S., Piron, D., Richard, A., Bispo, A., Grand, C., Galsomies, L., Cluzeau, D., Earthworm indicators as tools for soil monitoring, characterization and risk assessment. An example from the national Bioindicator programme (France). Pedobiologia (Jena) 54 (2011), S77–S87, 10.1016/j.pedobi.2011.09.015.
Prescott, C.E., Does nitrogen availability control rates of litter decomposition in forests?. Plant Soil 168–169 (1995), 83–88.
Preston-Mafham, J., Boddy, L., Randerson, P.F., Analysis of microbial community functional diversity using sole-carbon-source utilisation profiles – a critique. FEMS Microbiol. Ecol. 42 (2002), 1–14.
Pulleman, M., Creamer, R.E., Hamer, U., Helder, J., Pelosi, C., Pérès, G., Rutgers, M., Soil biodiversity, biological indicators and soil ecosystem services – an overview of European approaches. Curr. Opin. Environ. Sustain. 4 (2012), 529–538, 10.1016/j.cosust.2012.10.009.
Raiesi, F., Beheshti, A., Microbiological indicators of soil quality and degradation following conversion of native forests to continuous croplands. Ecol. Indic. 50 (2015), 173–185 doi: 10.1016/j.ecolind.2014.11.008.
Raulund-Rasmussen, K., Vejre, H., Effect of tree species and soil properties on nutrient immobilization in the forest floor. Plant Soil 168–169 (1995), 345–352.
Ritz, K., Black, H.I.J., Campbell, C.D., Harris, J.A., Wood, C., Selecting biological indicators for monitoring soils: a framework for balancing scientific and technical opinion to assist policy development. Ecol. Indic. 9 (2009), 1212–1221, 10.1016/j.ecolind.2009.02.009.
Rousk, J., Biomass or growth? How to measure soil food webs to understand structure and function. Soil Biol. Biochem. 102 (2016), 1–3, 10.1016/j.soilbio.2016.07.001.
Rutgers, M., Wouterse, M., Drost, S.M., Breure, A.M., Mulder, C., Stone, D., Creamer, R.E., Winding, A., Bloem, J., Monitoring soil bacteria with community-level physiological profiles using Biolog™ ECO-plates in the Netherlands and Europe. Appl. Soil Ecol. 97 (2016), 23–35, 10.1016/j.apsoil.2015.06.007.
Scheibe, A., Steffens, C., Seven, J., Jacob, A., Hertel, D., Leuschner, C., Gleixner, G., Effects of tree identity dominate over tree diversity on the soil microbial community structure. Soil Biol. Biochem. 81 (2015), 219–227, 10.1016/j.soilbio.2014.11.020.
Schloter, M., Dilly, O., Munch, J.C., Indicators for evaluating soil quality. Agric. Ecosyst. Environ. 98 (2003), 255–262, 10.1016/S0167-8809(03)00085-9.
Schoenholtz, S., Miegroet, H.V., Burger, J., A review of chemical and physical properties as indicators of forest soil quality: challenges and opportunities. For. Ecol. Manage. 138 (2000), 335–356, 10.1016/S0378-1127(00)00423-0.
Schua, K., Wende, S., Wagner, S., Feger, K.-H., Soil chemical and microbial properties in a mixed stand of spruce and birch in the Ore Mountains (Germany) – a case study. Forests 6 (2015), 1949–1965, 10.3390/f6061949.
Serna-Chavez, H.M., Fierer, N., van Bodegom, P.M., Global drivers and patterns of microbial abundance in soil. Glob. Ecol. Biogeogr. 22 (2013), 1162–1172, 10.1111/geb.12070.
Shade, A., Peter, H., Allison, S.D., Baho, D.L., Berga, M., Bürgmann, H., Huber, D.H., Langenheder, S., Lennon, J.T., Martiny, J.B.H., Matulich, K.L., Schmidt, T.M., Handelsman, J., Fundamentals of microbial community resistance and resilience. Front. Microbiol. 3 (2012), 1–19, 10.3389/fmicb.2012.00417.
Smolders, E., Oorts, K., Van Sprang, P., Schoeters, I., Janssen, C.R., McGrath, S.P., McLaughlin, M.J., Toxicity of trace metals in soil as affected by soil type and aging after contamination: using calibrated bioavailability models to set ecological soil standards. Environ. Toxicol. Chem. 28 (2009), 1633–1642.
Sparling, G.P., Vojvodic-Vukovic, M., Schipper, L.A., Hot-water-soluble C as a simple measure of labile soil organic matter: the relationship with microbial biomass C. Soil Biol. Biochem. 30 (1998), 1469–1472.
Sparling, G.P., West, A.W., A direct extraction method to estimate soil microbial C: calibration in situ using microbial respiration and 14C labellled cells. Soil Biol. Biochem. 20 (1988), 337–343.
Stone, D., Ritz, K., Grif, B.G., Orgiazzi, A., Creamer, R.E., Selection of biological indicators appropriate for European soil monitoring. Appl. Soil Ecol. 97 (2016), 12–22, 10.1016/j.apsoil.2015.08.005.
Thoms, C., Gleixner, G., Seasonal differences in tree species’ influence on soil microbial communities. Soil Biol. Biochem. 66 (2013), 239–248, 10.1016/j.soilbio.2013.05.018.
Vallet, P., Dhôte, J.-F., Le Moguédec, G., Ravart, M., Pignard, G., Development of total aboveground volume equations for seven important forest tree species in France. For. Ecol. Manage. 229 (2006), 98–110, 10.1016/j.foreco.2006.03.013.
van der Heijden, M.G.A., Bardgett, R.D., van Straalen, N.M., The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 11 (2008), 296–310, 10.1111/j.1461-0248.2007.01139.x.
van der Plas, F., Manning, P., Soliveres, S., Allan, E., Scherer-Lorenzen, M., Verheyen, K., Wirth, C., Zavala, M.A., Ampoorter, E., Baeten, L., Barbaro, L., Bauhus, J., Benavides, R., Benneter, A., Bonal, D., Bouriaud, O., Bruelheide, H., Bussotti, F., Carnol, M., Castagneyrol, B., Charbonnier, Y., Coomes, D.A., Coppi, A., Bestias, C.C., Dawud, S.M., De Wandeler, H., Domisch, T., Finér, L., Gessler, A., Granier, A., Grossiord, C., Guyot, V., Hättenschwiler, S., Jactel, H., Jaroszewicz, B., Joly, F.-X., Jucker, T., Koricheva, J., Milligan, H., Mueller, S., Muys, B., Nguyen, D., Pollastrini, M., Ratcliffe, S., Raulund-Rasmussen, K., Selvi, F., Stenlid, J., Valladares, F., Vesterdal, L., Zielínski, D., Fischer, M., Biotic homogenization can decrease landscape-scale forest multifunctionality. Proc. Natl. Acad. Sci. U.S.A. 113 (2016), 3557–3562.
Vance, E.D., Brookes, P.C., Jenkinson, D., An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19 (1987), 703–707, 10.1016/0038-0717(87)90052-6.
Vesterdal, L., Schmidt, I.K., Callesen, I., Nilsson, L.O., Gundersen, P., Carbon and nitrogen in forest floor and mineral soil under six common European tree species. For. Ecol. Manage. 255 (2008), 35–48, 10.1016/j.foreco.2007.08.015.
Wang, W.J., Dalal, R.C., Moody, P.W., Smith, C.J., Relationships of soil respiration to microbial biomass, substrate availability and clay content. Soil Biol. Biochem. 35 (2003), 273–284.
Wardle, D.A., Controls of temporal variability of the soil microbial biomass: a global-scale synthesis. Soil Biol. Biochem. 30 (1998), 1627–1637.
Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Setälä, H., van der Putten, W.H., Wall, D.H., Ecological linkages between aboveground and belowground biota. Science 80:304 (2004), 1629–1633, 10.1126/science.1094875.
Wardle, D.A., Ghani, A., A critique of the microbial metabolic quotient (qCO2) as a bioindicator of disturbance and ecosystem development. Soil Biol. Biochem. 27 (1995), 1601–1610, 10.1016/0038-0717(95)00093-T.
Welke, S.E., Hope, G.D., Influences of stand composition and age on forest floor processes and chemistry in pure and mixed stands of Douglas-fir and paper birch in interior British Columbia. For. Ecol. Manage. 219 (2005), 29–42, 10.1016/j.foreco.2005.08.040.
Winding, A., Hund-Rinke, K., Rutgers, M., The use of microorganisms in ecological soil classification and assessment concepts. Ecotoxicol. Environ. Saf. 62 (2005), 230–248, 10.1016/j.ecoenv.2005.03.026.
Xu, X., Schimel, J.P., Thornton, P.E., Song, X., Yuan, F., Goswami, S., Substrate and environmental controls on microbial assimilation of soil organic carbon: a framework for Earth system models. Ecol. Lett. 17 (2014), 547–555, 10.1111/ele.12254.
Yin, H., Li, Y., Xiao, J., Xu, Z., Cheng, X., Liu, Q., Enhanced root exudation stimulates soil nitrogen transformations in a subalpine coniferous forest under experimental warming. Global Change Biol. 19 (2013), 2158–2167, 10.1111/gcb.12161.
Zak, D.R., Holmes, W.E., White, D.C., Peacock, A.D., Tilman, D., Plant diversity, soil microbial communities, and ecosystem function: are there any links?. Ecology 84 (2003), 2042–2050, 10.1890/02-0433.
Zornoza, R., Acosta, J.A., Bastida, F., Domínguez, S.G., Toledo, D.M., Faz, A., Identification of sensitive indicators to assess the interrelationship between soil quality, management practices and human health. Soil 1 (2015), 173–185, 10.5194/soil-1-173-2015.
Similar publications
Sorry the service is unavailable at the moment. Please try again later.
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.
