The legacy of mixed planting and precipitation reduction treatments on soil microbial activity, biomass and community composition in a young tree plantation
Hicks, L. C.; Rahman, Md Masudur; Carnol, Moniqueet al.
2018 • In Soil Biology and Biochemistry, 124, p. 227-235
[en] Drought events are expected to increase as a consequence of climate change, with the potential to influence both plant and soil microbial communities. Mixed planting may be an option to mitigate drought stress to plants, however, the extent to which mixed planting mitigates the indirect effect of drought (reduced plant-derived carbon input) on soil microorganisms remains unknown. Using soils from a young experimental plantation in Central Europe, we investigated whether mixed planting (oak monoculture, and oak admixed with 1–3 other tree species) under simulated drought (50% precipitation reduction for 2 years) influenced soil microbial activity, biomass and community composition. To focus on legacy effects - i.e. indirect effects mediated by plant composition and a history of drought, rather than direct effects of reduced water availability - soils were measured at a standardised moisture content (28±1% water holding capacity). Rates of bacterial growth and respiration were lower in soils with a legacy of drought. In contrast, fungal growth was not affected by a history of drought, suggesting that fungi were less adversely affected by reduced plant-input during drought, compared to bacteria. The effect of drought on the fungal-to-bacterial growth ratio was influenced by mixed planting, leading to a disproportionate decrease in bacterial growth in drought-exposed soils under oak monoculture than when oak was admixed with two or three different tree species. The presence of a particular tree species (with specific functional traits) in the admixture, rather than increased tree richness per se, may explain this response. Microbial biomass parameters, reflecting both the direct and indirect effects of past drought conditions, were consistently lower in drought-exposed soils than controls. While bacteria were more sensitive to the indirect effect of drought than fungi, the biomass concentrations suggested that the direct effect of reduced moisture affected both groups similarly. Overall, our findings demonstrate that drought can have lasting effects on microbial communities, with consequences for microbial function. Results also suggest that admixing oak with other tree species may alleviate the drought-legacy effect on bacteria and increase tolerance to future drought.
Rahman, Md Masudur ✱; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Ecologie végétale et microbienne
Carnol, Monique ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Ecologie végétale et microbienne
Verheyen, Kris
Rousk, J
✱ These authors have contributed equally to this work.
Language :
English
Title :
The legacy of mixed planting and precipitation reduction treatments on soil microbial activity, biomass and community composition in a young tree plantation
FORBIO Climate- Adaptation potential of biodiverse forests in the face of climate change COST Action FP1305 BioLink- Linking belowground biodiversity and ecosystem function in European forests
Funders :
BELSPO - Politique scientifique fédérale [BE] Crafoord Foundation [SE] Swedish Research Council [SE]
Funding number :
Crafoord Foundation (grant no. 20150561); Swedish Research Council Formas (grant no. 941-2015-270); Swedish Research Council Vetenskapsrådet (grant no. 2015-04942)
Andresen, L.C., Dungait, J.A., Bol, R., Selsted, M.B., Ambus, P., Michelsen, A., Bacteria and fungi respond differently to multifactorial climate change in a temperate heathland, traced with 13C-glycine and FACE CO2. PLoS One, 9, 2014, 10.1371/journal.pone.0085070.
Anderson, J.P.E., Domsch, K.H., A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biology and Biochemistry 10 (1978), 215–221.
Bååth, E., Pettersson, M., Söderberg, K.H., Adaptation of a rapid and economical microcentrifugation method to measure thymidine and leucine incorporation by soil bacteria. Soil Biology and Biochemistry 33 (2001), 1571–1574.
Bapiri, A., Bååth, E., Rousk, J., Drying–rewetting cycles affect fungal and bacterial growth differently in an arable soil. Microbial Ecology 60 (2010), 419–428.
Bird, J.A., Herman, D.J., Firestone, M.K., Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil. Soil Biology and Biochemistry 43 (2011), 718–725.
Borken, W., Savage, K., Davidson, E.A., Trumbore, S.E., Effects of experimental drought on soil respiration and radiocarbon efflux from a temperate forest soil. Global Change Biology 12 (2006), 177–193.
Canarini, A., Kiær, L.P., Dijkstra, F.A., Soil carbon loss regulated by drought intensity and available substrate: a meta-analysis. Soil Biology and Biochemistry 112 (2017), 90–99.
Carnol, M., Bazgir, M., Nutrient return to the forest floor through litter and throughfall under 7 forest species after conversion from Norway spruce. Forest Ecology and Management 309 (2013), 66–75.
Ciais, P., Reichstein, M., Viovy, N., Granier, A., Ogée, J., Allard, V., Aubinet, M., Buchmann, N., Bernhofer, C., Carrara, A., Chevallier, F., Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437 (2005), 529–533.
Conant, R.T., Ryan, M.G., Ågren, G.I., Birge, H.E., Davidson, E.A., Eliasson, P.E., Evans, S.E., Frey, S.D., Giardina, C.P., Hopkins, F.M., Hyvönen, R., Temperature and soil organic matter decomposition rates–synthesis of current knowledge and a way forward. Global Change Biology 17 (2011), 3392–3404.
Evans, S.E., Wallenstein, M.D., Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter?. Biogeochemistry 109 (2012), 101–116.
Fierer, N., Colman, B.P., Schimel, J.P., Jackson, R.B., Predicting the temperature dependence of microbial respiration in soil: a continental-scale analysis. Global Biogeochemical Cycles, 20, 2006, 10.1029/2005GB002644.
Forrester, D.I., Bauhus, J., A review of processes behind diversity-productivity relationships in forests. Current Forestry Reports 2 (2016), 45–61.
Frostegård, Å., Tunlid, A., Bååth, E., Phospholipid fatty acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Applied and Environmental Microbiology 59 (1993), 3605–3617.
Frostegård, Å., Bååth, E., The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biology and Fertility of Soils 22 (1996), 59–65.
Fuchslueger, L., Bahn, M., Fritz, K., Hasibeder, R., Richter, A., Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow. New Phytologist 201 (2014), 916–927.
Gelman, A., Shor, B., Bafumi, J., Park, D., Rich state, poor state, red state, blue state: what's the matter with Connecticut?. Quarterly Journal of Political Science 2 (2007), 345–367.
Göransson, H., Godbold, D.L., Jones, D.L., Rousk, J., Bacterial growth and respiration responses upon rewetting dry forest soils: impact of drought-legacy. Soil Biology and Biochemistry 57 (2013), 477–486.
Guhr, A., Borken, W., Spohn, M., Matzner, E., Redistribution of soil water by a saprotrophic fungus enhances carbon mineralization. Proceedings of the National Academy of Sciences 112 (2015), 14647–14651.
Gunina, A., Smith, A.R., Godbold, D.L., Jones, D.L., Kuzyakov, Y., Response of soil microbial community to afforestation with pure and mixed species. Plant and Soil 412 (2017), 357–368.
Harris, R.F., Effect of water potential on microbial growth and activity. Water Potential Relations in Soil Microbiology, 1981, 23–95.
Hasibeder, R., Fuchslueger, L., Richter, A., Bahn, M., Summer drought alters carbon allocation to roots and root respiration in mountain grassland. New Phytologist 205 (2015), 1117–1127.
Hawkes, C.V., Waring, B.G., Rocca, J.D., Kivlin, S.N., Historical climate controls soil respiration responses to current soil moisture. Proceedings of the National Academy of Sciences 114 (2017), 6322–6327.
Homyak, P.M., Allison, S.D., Huxman, T.E., Goulden, M.L., Treseder, K.K., Effects of drought manipulation on soil nitrogen cycling: a meta-analysis. Journal of Geophysical Research: Biogeosciences, 2017, 10.1002/2017JG004146.
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., Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75 (2005), 3–35.
IPCC, Summary for policymakers. Stocker, T.F., Qin, D., Plattner, G.K., Tignor, M., Allen, S.K., Boschung, J., Nauels, A., Xia, Y., Bex, V., Midgley, P.M., (eds.) Climate Change 2013: the Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, 2013, Cambridge University Press, Cambridge, United Kingdom and New York, USA.
IUSS Working Group WRB, World Reference Base for Soil Resources 2006. World Soil Resources Reports 103, 2006.
Jones, D.L., Nguyen, C., Finlay, R.D., Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant and Soil 321 (2009), 5–33.
Lebourgeois, F., Gomez, N., Pinto, P., Mérian, P., Mixed stands reduce Abies alba tree-ring sensitivity to summer drought in the Vosges mountains, western Europe. Forest Ecology and Management 303 (2013), 61–71.
Lenton, T.M., Early warning of climate tipping points. Nature Climate Change 1 (2011), 201–209.
Manzoni, S., Schimel, J.P., Porporato, A., Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93 (2012), 930–938.
Martiny, J.B., Martiny, A.C., Weihe, C., Lu, Y., Berlemont, R., Brodie, E.L., Goulden, M.L., Treseder, K.K., Allison, S.D., Microbial legacies alter decomposition in response to simulated global change. The ISME Journal 11 (2017), 490–499.
Meisner, A., Leizeaga, A., Rousk, J., Bååth, E., Partial drying accelerates bacterial growth recovery to rewetting. Soil Biology and Biochemistry 112 (2017), 269–276.
Mina, M., Huber, M.O., Forrester, D.I., Thürig, E., Rohner, B., Multiple factors modulate tree growth complementarity in central European mixed forests. Journal of Ecology, 2017, 10.1111/1365-2745.12846.
Newell, S.Y., Fallon, R.D., Toward a method for measuring instantaneous fungal growth rates in field samples. Ecology 72 (1991), 1547–1559.
Nilsson, L.O., Bååth, E., Falkengren-Grerup, U., Wallander, H., Growth of ectomycorrhizal mycelia and composition of soil microbial communities in oak forest soils along a nitrogen deposition gradient. Oecologia 153 (2007), 375–384.
Peñuelas, J., Prieto, P., Beier, C., Cesaraccio, C., De Angelis, P., De Dato, G., Emmett, B.A., Estiarte, M., Garadnai, J., Gorissen, A., Láng, E.K., Response of plant species richness and primary productivity in shrublands along a north–south gradient in Europe to seven years of experimental warming and drought: reductions in primary productivity in the heat and drought year of 2003. Global Change Biology 13 (2007), 2563–2581.
Pretzsch, H., Schütze, G., Uhl, E., Resistance of European tree species to drought stress in mixed versus pure forests: evidence of stress release by inter-specific facilitation. Plant Biology 15 (2013), 483–495.
Rahman, M.M., Castagneyrol, B., Verheyen, K., Jactel., H and Carnol., M., In Review. Can tree species richness attenuate the effect of drought on organic matter decomposition and stabilization in young plantation forests?.
R Core Team, R: a Language and Environment For Statistical Computing. 2015, R Foundation for Statistical Computing, Vienna, Austria.
Ren, C., Chen, J., Lu, X., Doughty, R., Zhao, F., Zhong, Z., Han, X., Yang, G., Feng, Y., Ren, G., Responses of soil total microbial biomass and community compositions to rainfall reductions. Soil Biology and Biochemistry 116 (2018), 4–10.
Rousk, J., Bååth, E., Fungal biomass production and turnover in soil estimated using the acetate-in-ergosterol technique. Soil Biology and Biochemistry 39 (2007), 2173–2177.
Rousk, J., Brookes, P.C., Bååth, E., Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Applied and Environmental Microbiology 75 (2009), 1589–1596.
Rousk, J., Smith, A.R., Jones, D.L., Investigating the long-term legacy of drought and warming on the soil microbial community across five European shrubland ecosystems. Global Change Biology 19 (2013), 3872–3884.
Ruess, L., Chamberlain, P.M., The fat that matters: soil food web analysis using fatty acids and their carbon stable isotope signature. Soil Biology and Biochemistry 42 (2010), 1898–1910.
Ruehr, N.K., Offermann, C.A., Gessler, A., Winkler, J.B., Ferrio, J.P., Buchmann, N., Barnard, R.L., Drought effects on allocation of recent carbon: from beech leaves to soil CO2 efflux. New Phytologist 184 (2009), 950–961.
Sanaullah, M., Blagodatskaya, E., Chabbi, A., Rumpel, C., Kuzyakov, Y., Drought effects on microbial biomass and enzyme activities in the rhizosphere of grasses depend on plant community composition. Applied Soil Ecology 48 (2011), 38–44.
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 Biology and Biochemistry 81 (2015), 219–227.
Setiawan, N.N., Vanhellemont, M., De Schrijver, A., Schelfhout, S., Baeten, L., Verheyen, K., Mixing effects on litter decomposition rates in a young tree diversity experiment. Acta Oecologica 70 (2016), 79–86.
Sheik, C.S., Krumholz, L.R., Elshahed, M.S., Beasley, W.H., Zhou, X., Luo, Y., Effect of warming and drought on grassland microbial communities. The ISME Journal 5 (2011), 1692–1700.
Singh, B.K., Munro, S., Reid, E., Ord, B., Potts, J.M., Paterson, E., Millard, P., Investigating microbial community structure in soils by physiological, biochemical and molecular fingerprinting methods. European Journal of Soil Science 57 (2006), 72–82.
Thoms, C., Gattinger, A., Jacob, M., Thomas, F.M., Gleixner, G., Direct and indirect effects of tree diversity drive soil microbial diversity in temperate deciduous forest. Soil Biology and Biochemistry 42 (2010), 1558–1565.
Tilman, D., The ecological consequences of changes in biodiversity: a search for general principles. Ecology 80 (1999), 1455–1474.
Verheyen, K., Ceunen, K., Ampoorter, E., Baeten, L., Bosman, B., Branquart, E., Carnol, M., De Wandeler, H., Grégoire, J.C., Lhoir, P., Muys, B., Assessment of the functional role of tree diversity: the multi-site FORBIO experiment. Plant Ecology and Evolution 146 (2013), 26–35.
Verheyen, K., Vanhellemont, M., Auge, H., Baeten, L., Baraloto, C., Barsoum, N., Bilodeau-Gauthier, S., Bruelheide, H., Castagneyrol, B., Godbold, D., Haase, J., Contributions of a global network of tree diversity experiments to sustainable forest plantations. Ambio 45 (2016), 29–41.
Vogel, A., Eisenhauer, N., Weigelt, A., Scherer-Lorenzen, M., Plant diversity does not buffer drought effects on early-stage litter mass loss rates and microbial properties. Global Change Biology 19 (2013), 2795–2803.
de Vries, F.T., Liiri, M.E., Bjørnlund, L., Bowker, M.A., Christensen, S., Setälä, H.M., Bardgett, R.D., Land use alters the resistance and resilience of soil food webs to drought. Nature Climate Change 2 (2012), 276–280.
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 304 (2004), 1629–1633.
Wu, Z., Dijkstra, P., Koch, G.W., Penuelas, J., Hungate, B.A., Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation. Global Change Biology 17 (2011), 927–942.
Yuste, J.C., Penuelas, J., Estiarte, M., Garcia-Mas, J., Mattana, S., Ogaya, R., Pujol, M., Sardans, J., Drought-resistant fungi control soil organic matter decomposition and its response to temperature. Global Change Biology 17 (2011), 1475–1486.
