Biology and Fertility of Soils

, Volume 55, Issue 1, pp 1–14 | Cite as

Similar spatial patterns of soil quality indicators in three poplar-based silvo-arable alley cropping systems in Germany

  • René BeuschelEmail author
  • Hans-Peter Piepho
  • Rainer Georg Joergensen
  • Christine Wachendorf
Original Paper


Alley cropping systems (ACS) are regarded as a sustainable land-use alternative that provides ecosystem services, assuming that beneficial tree effects extend towards crop alleys. However, the spatial range of these effects has rarely been considered. The objective of this study was to investigate soil quality indicators at different distances from trees in three German silvo-arable ACS. We analysed soil microbial biomass C and N, ergosterol, microbial activity (enzyme activities, substrate-induced respiration rates) and their functional diversity (MicroResp™ method) in topsoils. Furthermore, fungal abundance and fungal and bacterial contribution to microbial residues (amino sugars) were determined. Tree effects on soil quality indicators were estimated for each depth, for the first time considering both, spatial dependence and abiotic factors (pH, clay content) using mixed effects models with repeated measures. Additionally, differences between soil depths were tested. Analysis combining the three ACS revealed a generalisation of effect sizes and spatial range of tree effects on soil quality indicators. Tree implementation in arable systems increased SOC, microbial biomass and activity in upper topsoils and shifted the composition of main microbial groups towards a higher fungal abundance and functional diversity. Soil quality indices decreased with increasing depth. However, in alleys, no differences between distances from trees were observed. Results demonstrate that ACS are capable to enhance soil quality mediated by microorganisms under trees within 5–8 years. Long-term studies are required to estimate whether beneficial tree effects extend towards crop alleys and deeper soil layers when systems are mature.


Agroforestry Amino sugars Ergosterol Microbial biomass Soil enzyme activities Substrate-induced respiration rates 



This research was funded by the Federal Ministry of Education and Research (BMBF) in the context of the project “SIGNAL—sustainable intensification of agriculture through agroforestry”, which is related to BonaRes. The authors are very grateful to Nicole Gauss and Gabriele Dormann for the induction into the laboratory of Soil Biology and Plant Nutrition at the University of Kassel. We thank Mick Locke for the careful correction of our English.

Supplementary material

374_2018_1324_MOESM1_ESM.pdf (384 kb)
ESM 1 (PDF 384 kb)
374_2018_1324_MOESM2_ESM.pdf (398 kb)
ESM 2 (PDF 397 kb)
374_2018_1324_MOESM3_ESM.pdf (4.6 mb)
ESM 3 (PDF 4.64 mb)


  1. Ad-hoc-Arbeitsgruppe Boden (2005) Manual of soil mapping, 5th edn. (Bodenkundliche Kartieranleitung, KA5). E. Schweizerbart, HannoverGoogle Scholar
  2. Anderson TH, Domsch KH (1989) Ratios of microbial biomass carbon to total organic carbon in arable soils. Soil Biol Biochem 21:471–479Google Scholar
  3. Anderson TH, Domsch KH (1990) Application of eco-physiological quotients qCO2 and qD on microbial biomasses from soils of different cropping histories. Soil Biol Biochem 22:251–255Google Scholar
  4. Anderson TH, Domsch KH (2010) Soil microbial biomass: the eco-physiological approach. Soil Biol Biochem 42:2039–2043Google Scholar
  5. Appuhn A, Joergensen RG (2006) Microbial colonisation of roots as a function of plant species. Soil Biol Biochem 38:1040–1051Google Scholar
  6. Appuhn A, Joergensen RG, Raubuch M, Scheller E, Wilke B (2004) The automated determination of glucosamine, galactosamine, muramic acid and mannosamine in soil and root hydrolysates by HPLC. J Plant Nutr Soil Sci 167:17–21Google Scholar
  7. Appuhn A, Scheller E, Joergensen RG (2006) Relationships between microbial indices in roots and silt loam soils forming a gradient in soil organic matter. Soil Biol Biochem 38:2557–2564Google Scholar
  8. Bailey VL, Smith JL, Bolton HJ (2002) Fungal-to-bacterial ratios in soils investigated for enhanced C sequestration. Soil Biol Biochem 34:997–1007Google Scholar
  9. Bamminger C, Marschner B, Jüschke E (2014) An incubation study on the stability and biological effects of pyrogenic and hydrothermal biochar in two soils. Europ J Soil Sci 65:72–82Google Scholar
  10. Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20:634–641PubMedGoogle Scholar
  11. Bardhan S, Jose S, Udawatta RP, Fritschi F (2013) Microbial community diversity in a 21-year-old temperate alley cropping system. Agrofor Syst 87:1031–1041Google Scholar
  12. Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method for measuring microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842Google Scholar
  13. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  14. Caldwell BA (2005) Enzyme activities as a component of soil biodiversity: a review. Pedobiologia 49:637–644Google Scholar
  15. Campbell CD, Chapman SJ, Cameron CM, Davidson MS, Potts JM (2003) A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl Environ Microbiol 69:3593–3599PubMedPubMedCentralGoogle Scholar
  16. Campbell CD, Grayston SJ, Hirst DJ (1997) Use of rhizosphere carbon source tests to discriminate soil microbial communities. J Microbiol Methods 30:33–41Google Scholar
  17. Cannell MGR, van Noordwijk M, Ong CK (1996) The central agroforestry hypothesis: the trees must acquire resources that the crop would not otherwise acquire. Agrofor Syst 34:27–31Google Scholar
  18. Cardinael R, Chevallier T, Cambou A, Béral C, Barthès BG, Dupraz C, Durand C, Kouakoua E, Chenu C (2017) Increased soil organic carbon stocks under agroforestry: a survey of six different sites in France. Agric Ecosyst Environ 236:243–255Google Scholar
  19. Chang SX, Shi Z, Thomas BR (2016) Soil respiration and its temperature sensitivity in agricultural and afforested poplar plantation systems in northern Alberta. Biol Fertil Soils 52:629–641Google Scholar
  20. DeForest JL (2009) The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and L-DOPA. Soil Biol Biochem 41:1180–1186Google Scholar
  21. Degens BP, Schipper LA, Sparling GP, Vojvodic-Vukovic M (2000) Decreases in organic C reserves in soils can reduce the catabolic diversity of soil microbial communities. Soil Biol Biochem 32:189–196Google Scholar
  22. Djajakirana G, Joergensen RG, Meyer B (1996) Ergosterol and microbial biomass relationship in soil. Biol Fertil Soils 22:299–304Google Scholar
  23. Ekenler M, Tabatabai MA (2002) β-Glucosaminidase activity of soils: effect of cropping systems and its relationship to nitrogen mineralization. Biol Fertil Soils 36:367–376Google Scholar
  24. Ekenler M, Tabatabai MA (2003) Tillage and residue management effects on β-glucosaminidase activity in soils. Soil Biol Biochem 35:871–874Google Scholar
  25. Engelking B, Flessa H, Joergensen RG (2007) Shifts in amino sugar and ergosterol contents after addition of sucrose and cellulose to soil. Soil Biol Biochem 39:2111–2118Google Scholar
  26. Faust S, Heinze S, Ngosong C, Sradnick A, Oltmanns M, Raupp J, Geisseler D, Joergensen RG (2017) Effect of biodynamic soil amendments on microbial communities in comparison with inorganic fertilization. Appl Soil Ecol 114:82–89Google Scholar
  27. Frey SD, Elliott ET, Paustian K (1999) Bacterial and fungal abundance and biomass in conventional and no-tillage agroecosystems along two climate gradients. Soil Biol Biochem 31:573–585Google Scholar
  28. Garrett HEG, Buck L (1997) Agroforestry practice and policy in the United States of America. For Ecol Manag 91:5–15Google Scholar
  29. Georgiadis P, Vesterdal L, Stupak I, Raulund-Rasmussen K (2017) Accumulation of soil organic carbon after cropland conversion to short-rotation willow and poplar. Glob Change Biol Bioenergy 9:1390–1401Google Scholar
  30. German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397Google Scholar
  31. Giacometti C, Cavani L, Baldoni G, Ciavatta C, Marzadori C, Kandeler E (2014) Microplate-scale fluorometric soil enzyme assays as tools to asses soil quality in a long-term agricultural field experiment. Appl Soil Ecol 75:80–85Google Scholar
  32. Green VS, Cavigelli MA, Dao TH, Flanagan DC (2005) Soil physical and aggregate-associated C, N, and P distributions in organic and conventional cropping systems. Soil Sci 170(10):822–831Google Scholar
  33. Guggenberger G, Frey SD, Six J, Paustian K, Elliott ET (1999) Bacterial and fungal cell-wall residues in conventional and no-tillage agroecosystems. Soil Sci Soc Am J 63:1188–1198Google Scholar
  34. Hagen-Thorn A, Callesen I, Armolaitis K, Nihlgård B (2004) The impact of six European tree species on the chemistry of mineral topsoil in forest plantations on former agricultural land. For Ecol Manag 195:373–384Google Scholar
  35. Indorf C, Dyckmans J, Khan KS, Joergensen RG (2011) Optimisation of amino sugar quantification by HPLC in soil and plant hydrolysates. Biol Fertil Soils 47:387–396Google Scholar
  36. IUSS Working Group WRB (2015) World Reference Base for soil resources 2014, update 2015. International soil classification system for naming soils and creating legends for soil maps. World soil resources reports 106. FAO, RomeGoogle Scholar
  37. Joergensen RG (1996) The fumigation-extraction method to estimate soil microbial biomass: calibration of the kEC value. Soil Biol Biochem 28:25–31Google Scholar
  38. Joergensen RG (2018) Amino sugars as specific indices for fungal and bacterial residues in soil. Biol Fertil Soils 54:559–568Google Scholar
  39. Joergensen RG, Emmerling C (2006) Methods for evaluating human impact on soil microorganisms based on their activity, biomass, and diversity in agricultural soils. J Plant Nutr Soil Sci 169:295–309Google Scholar
  40. Joergensen RG, Mueller T (1996) The fumigation-extraction method to estimate soil microbial biomass: calibration of the kEN value. Soil Biol Biochem 28:33–37Google Scholar
  41. Joergensen RG, Wichern F (2008) Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biol Biochem 40:2977–2991Google Scholar
  42. Jose S (2009) Agroforestry for ecosystem services and environmental benefits: an overview. Agrofor Syst 76:1–10Google Scholar
  43. Jose S, Bardhan S (2012) Agroforestry for biomass production and carbon sequestration: an overview. Agrofor Syst 86:105–111Google Scholar
  44. Kandeler E, Palli S, Stemmer M, Gerzabek MH (1999a) Tillage changes microbial biomass and enzyme activities in particle-size fractions of a Haplic Chernozem. Soil Biol Biochem 31:1253–1264Google Scholar
  45. Kandeler E, Tscherko D, Spiegel H (1999b) Long-term monitoring of microbial biomass, N mineralization and enzyme activities of a Chernozem under different tillage management. Biol Fertil Soils 28:343–351Google Scholar
  46. Keiblinger KM, Schneider T, Roschitzki B, Schmid E, Eberl L, Hämmerle I, Leitner S, Richter A, Wanek W, Riedel K, Zechmeister-Boltenstern S (2012) Effects of stoichiometry and temperature pertubations on beech leaf litter decomposition, enzyme activities and protein expression. Biogeosciences 9:4537–4551Google Scholar
  47. Kenward MG, Roger JH (2009) An improved approximation to the precision of fixed effects from restricted maximum likelihood. Comput Stat Data Anal 53:2583–2595Google Scholar
  48. Kögel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–162Google Scholar
  49. Kögel-Knabner I (2006) Chemical structure of organic N and organic P in soil. In: Nannipieri P, Smalla K (eds) Soil biology, nucleic acids and proteins in soil, vol 8. Springer, Berlin, pp 23–48Google Scholar
  50. Köhn M (1928) Beiträge zur Theorie und Praxis der mechanischen Bodenanalyse. Landwirtsch Jb 67Google Scholar
  51. Lagomarsino A, Benedetti A, Marinari S, Pompili L, Moscatelli MC, Roggero PP, Lai R, Ledda L (2011) Soil organic C variability and microbial functions in a Mediterranean agro-forest ecosystem. Biol Fertil Soils 47:283–291Google Scholar
  52. Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415Google Scholar
  53. Lavahun MFE, Joergensen RG, Meyer B (1996) Activity and biomass of soil microorganisms at different depths. Biol Fertil Soils 23:38–42Google Scholar
  54. Lee KH, Jose S (2003) Soil respiration and microbial biomass in a pecan-cotton alley cropping system in southern USA. Agrofor Syst 58:45–54Google Scholar
  55. Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for mixed models, 2nd edn. SAS Institute Inc., Cary, NC, USAGoogle Scholar
  56. Littell RC, Pendergast J, Natarajan R (2000) Modelling covariance structure in the analysis of repeated measures data. Statist Med 19:1793–1819Google Scholar
  57. Marx MC, Wood M, Jarvis SC (2001) A microplate fluorimetric assay for the study of enzyme diversity in soils. Soil Biol Biochem 33:1633–1640Google Scholar
  58. Medeiros EV, Duda GP, Santos LAR, Sousa Lima JR, Almeida-Cortêz JS, Hammecker C, Lardy L, Cournac L (2017) Soil organic carbon, microbial biomass and enzyme activities responses to natural regeneration in a tropical dry region in Northeast Brazil. Catena 151:137–146Google Scholar
  59. Meyer A, Fischer H, Kuzyakov Y, Fischer K (2008) Improved RP-HPLC and anion-exchange chromatography methods for the determination of amino acids and carbohydrates in soil solutions. J Plant Nutr Soil Sci 171:917–926Google Scholar
  60. Myers RT, Zak DR, White DC, Peacock A (2001) Landscape-level patterns of microbial community composition and substrate use in upland forest ecosystems. Soil Sci Soc Am J 65:359–367Google Scholar
  61. Miltner A, Bombach P, Schmidt-Brücken B, Kästner M (2012) SOM genesis: microbial biomass as a significant source. Biogeochemistry 111:41–55Google Scholar
  62. Mungai NW, Motavalli PP, Kremer RJ, Nelson KA (2005) Spatial variation of soil enzyme activities and microbial functional diversity in temperate alley cropping systems. Biol Fertil Soils 42:129–136Google Scholar
  63. Murugan R, Loges R, Taube F, Sradnick A, Joergensen RG (2014) Changes in soil microbial biomass and residual indices as ecological indicators of land use change in temperate permanent grassland. Microb Ecol 67:907–918PubMedGoogle Scholar
  64. Nannipieri P, Acher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Europ J Soil Sci 54:655–670Google Scholar
  65. Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762Google Scholar
  66. Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fertil Soils 54:11–19Google Scholar
  67. Nehls U, Mikolajewski S, Magel E, Hampp R (2001) Carbohydrate metabolism in ectomycorrhizas: gene expression, monosaccharide transport and metabolic control. New Phytol 150:533–541Google Scholar
  68. Nii-Annang S, Grünewald H, Freese D, Hüttl RF, Dilly O (2009) Microbial activity, organic C accumulation and 13C abundance in soils under alley cropping systems after 9 years of recultivation of quaternary deposits. Biol Fertil Soils 45:531–538Google Scholar
  69. North PF (1976) Towards an absolute measurement of soil structural stability using ultrasound. J Soil Sci 27:421–459Google Scholar
  70. Olsson PA, Larsson L, Bago B, Wallander H, van Aarle IM (2003) Ergosterol and fatty acids for biomass estimation of mycorrhizal fungi. New Phytol 159:1–10Google Scholar
  71. Paudel BR, Udawatta RP, Anderson SH (2011) Agroforestry and grass buffer effects on soil quality parameters for grazed pasture and row-crop systems. Appl Soil Ecol 48:125–132Google Scholar
  72. Paudel BR, Udawatta RP, Kremer RJ, Anderson SH (2012) Soil quality indicator responses to row crop, grazed pasture, and agroforestry buffer management. Agrofor Syst 84:311–323Google Scholar
  73. Piepho HP (2009) Data transformation in statistical analysis of field trials with changing treatment variance. Agron J 101:865–869Google Scholar
  74. Piepho HP, Büchse A, Richter C (2004) A mixed modelling approach for randomized experiments with repeated measures. J Agron Crop Sci 190:230–247Google Scholar
  75. Piepho HP, Edmondson R (2018) A tutorial on the statistical analysis of factorial experiments with qualitative and quantitative treatment factor levels. J Agron Crop Sci 204:429–455Google Scholar
  76. Potthoff M, Dyckmans J, Flessa H, Muhs A, Beese F, Joergensen RG (2005) Dynamics of maize (Zea mays L.) leaf straw mineralization as affected of soil and the availability of nitrogen. Soil Biol Biochem 37:1259–1266Google Scholar
  77. Quinkenstein A, Wöllecke J, Böhm C, Grünewald H, Freese D, Schneider BU, Hüttl RF (2009) Ecological benefits of the alley cropping agroforestry system in sensitive regions of Europe. Environ Sci Pol 12:1112–1121Google Scholar
  78. SAS Institute Inc (2013) SAS/STAT user’s guide, version 9. SAS Institute Inc., Cary, NC, USA, p 4Google Scholar
  79. Scheller E, Joergensen RG (2008) Decomposition of wheat straw differing in nitrogen content in soils under conventional and organic farming management. J Plant Nutr Soil Sci 171:886–892Google Scholar
  80. Schmidt MWI, Rumpel C, Kögel-Knabner I (1999) Evaluation of an ultrasonic dispersion procedure to isolate primary organomineral complexes from soils. Eur J Soil Sci 50:87–94Google Scholar
  81. Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmenn J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56PubMedGoogle Scholar
  82. Schüßler A (2009) Struktur, Funktion und Ökologie der arbuskulären Mykorrhiza. In: Bayerische Akademie der Wissenschaften (Ed) Rundgespräche der Kommission für Ökologie: Ökologische Rolle von Pilzen, vol 37. Dr. Friedrich Pfeil, München, pp 97–108Google Scholar
  83. Shihan A, Haettenschwiler S, Milcu A, Joly FX, Santonja M, Fromin N (2017) Changes in soil microbial substrate utilization in response to altered litter diversity and precipitation in a Mediterranean shrubland. Biol Fertil Soils 53:171–185Google Scholar
  84. Stevenson FJ (1994) Humus chemistry. Genesis, composition, reactions, 2nd edn. Wiley, New YorkGoogle Scholar
  85. Swieter A, Langhof M, Lamerre J, Greef JM (2018) Long-term yields of oilseed rape and winter wheat in a short rotation alley cropping agroforestry system. Agrofor Syst.
  86. Talbot JM, Treseder KK (2012) Interactions among lignin, cellulose, and nitrogen drive litter chemistry-decay relationships. Ecology 93:345–354PubMedGoogle Scholar
  87. Taylor CR, Hardiman EM, Ahmad M, Sainsbury PD, Norris PR, Bugg TDH (2012) Isolation of bacterial strains able to metabolize lignin from screening of environmental samples. J Appl Microbiol 113:521–530PubMedGoogle Scholar
  88. Torralba M, Fagerholm N, Burgess PJ, Gerardo M, Plieninger T (2016) Do European agroforestry systems enhance biodiversity and ecosystem services? A meta-analysis. Agric Ecosyst Environ 230:150–161Google Scholar
  89. Tsonkova P, Böhm C, Quinkenstein A, Freese D (2012) Ecological benefits provided by alley cropping systems for production of woody biomass in the temperate region: a review. Agrofor Syst 85:133–152Google Scholar
  90. Udawatta RP, Gantzer CJ, Anderson SH, Garrett HE (2008a) Agroforestry and grass buffer effects on pore characteristics measured by high-resolution X-ray computed tomography. Soil Sci Soc Am J 72:295–304Google Scholar
  91. Udawatta RP, Kremer RJ, Adamson BW, Anderson SH (2008b) Variations in soil aggregate stability and enzyme activities in a temperate agroforestry practice. Appl Soil Ecol 39:153–160Google Scholar
  92. Udawatta RP, Kremer RJ, Garrett HE, Anderson SH (2009) Soil enzyme activities and physical properties in a watershed managed under agroforestry and row-crop systems. Agric Ecosyst Environ 131:98–104Google Scholar
  93. Udawatta RP, Kremer RJ, Nelson KA, Jose S, Bardhan S (2014) Soil quality of a mature alley cropping agroforestry system in temperate North America. Commun Soil Sci Plant Anal 45:2539–2551Google Scholar
  94. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707Google Scholar
  95. Wardle DA (1995) Impacts of disturbance on detritus food webs in agro-ecosystems of contrasting tillage and weed management practices. Adv Ecol Res 26:107–185Google Scholar
  96. Weerasekara C, Udawatta RP, Jose S, Kremer RJ, Weerasekara C (2016) Soil quality differences in a row-crop watershed with agroforestry and grass buffers. Agrofor Syst 90:829–838Google Scholar
  97. Wu J, Joergensen RG, Pommerening B, Chaussod R, Brookes PC (1990) Measurement of microbial biomass C by fumigation extraction – an automated procedure. Soil Biol Biochem 22:1167–1169Google Scholar
  98. Wu YT, Gutknecht J, Nadrowski K, Geißler C, Kühn P, Scholten T, Both S, Erfmeier A, Böhnke M, Bruelheide H, Wubet T, Buscot F (2012) Relationships between soil microorganisms plant communities, and soil characteristics in Chinese subtropical forests. Ecosystems 15:624–636Google Scholar
  99. Xue C, Penton CR, Zhu C, Chen H, Duan Y, Peng C, Guo S, Ling N, Shen Q (2018) Alterations in soil fungal community composition and network assemblage structure by different long-term fertilization regimes are correlated to the soil ionome. Biol Fertil Soils 54:95–106Google Scholar
  100. Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84:2042–2050Google Scholar
  101. Zak JC, Willig MR, Moorhead DL, Wildman HG (1994) Functional diversity of microbial communities: a quantitative approach. Soil Biol Biochem 26:1101–1108Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Soil Biology and Plant NutritionUniversity of KasselWitzenhausenGermany
  2. 2.Biostatistics Unit, Institute of Crop ScienceUniversity of HohenheimStuttgartGermany

Personalised recommendations