Convergence of soil microbial properties after plant colonization of an experimental plant diversity gradient
© Steinauer et al. 2016
Received: 7 November 2015
Accepted: 22 March 2016
Published: 7 April 2016
Several studies have examined the effects of plant colonization on aboveground communities and processes. However, the effects of plant colonization on soil microbial communities are less known. We addressed this gap by studying effects of plant colonization within an experimental plant diversity gradient in subplots that had not been weeded for 2 and 5 years. This study was part of a long-term grassland biodiversity experiment (Jena Experiment) with a gradient in plant species richness (1, 2, 4, 8, 16, and 60 sown species per plot). We measured plant species richness and productivity (aboveground cover and biomass) as well as soil microbial basal respiration and biomass in non-weeded subplots and compared the results with those of weeded subplots of the same plots.
After 2 and 5 years of plant colonization, the number of colonizing plant species decreased with increasing plant diversity, i.e., low-diversity plant communities were most vulnerable to colonization. Plant colonization offset the significant relationship between sown plant diversity and plant biomass production. In line with plant community responses, soil basal respiration and microbial biomass increased with increasing sown plant diversity in weeded subplots, but soil microbial properties converged in non-weeded subplots and were not significantly affected by the initial plant species richness gradient.
Colonizing plant species change the quantity and quality of inputs to the soil, thereby altering soil microbial properties. Thus, plant community convergence is likely to be rapidly followed by the convergence of microbial properties in the soil.
Human-induced global change is leading to worldwide changes in plant community assembly resulting in profound impacts on ecosystem functions [1, 2]. Gaining more knowledge about the mechanisms that influence biodiversity, compositional stability of plant communities, and resistance against plant colonization provide essential information to evaluate the consequences of biodiversity loss and the subsequent changes in ecosystem functions.
Generally, plant diversity increases the stability of community biomass in biodiversity experiments [3–5]. Presumably, this is due to more complete exploitation of resources with increasing plant diversity . Therefore, more diverse plant communities are more resistant to the colonization of species than less diverse plant communities [7–9] and/or are more likely to contain better competitors for available resources . Newly colonizing plant species must survive and grow on resources not consumed by resident plant species . The prerequisite for successful plant colonization thus might be complementary resource requirements compared to the resident plant species . Therefore, colonization success of a plant species is higher when its functional traits are most different from the functional traits of the resident species [12–14]. Consistent with this expectation, higher species richness and functional complementarity were shown to increase plant biomass production in experimental studies [15, 16] due to a more complete use of available resources  leaving fewer vacant niches for colonizers [7, 13]. The composition and functioning of plant communities are closely linked to belowground communities and processes . Colonizing plant species entering a resident community affect the biogeochemistry of ecosystems , alter the rate of nutrient cycling , and induce a shift in the structure of rhizosphere microbial communities , e.g., by accumulating specific pathogens in their rhizosphere .
Previous studies showed that the biomass and the activity of soil microorganisms increase significantly with increasing plant diversity [23–25]. The underlying mechanisms are enhanced net primary productivity, soil carbon inputs via rhizodeposition, and decomposition of plant biomass at high plant diversity [26, 27]. Different plant species, including colonizer species, release different organic compounds that change the rhizosphere conditions affecting the microbial community structure, abundance, and activity . Some newly colonizing plant species might produce chemical compounds that are novel to the resident plant species, thereby having unique effects on soil microbial properties. Therefore, shifts in plant community composition and diversity due to the colonization of plant species may affect soil microbial community composition, biomass, and functions .
The study was conducted as part of the Jena Experiment, a long-term grassland biodiversity experiment in Jena, Germany . A plant diversity gradient (1, 2, 4, 8, 16, and 60 species) was established in 2002 on 82 plots (two monoculture plots had to be given up over the course of the experiment due to very low coverage of the target species, which resulted in 80 plots for the present study). The species pool of the experiment consists of 60 plant species categorized into four functional groups (grasses, legumes, tall and small herbs; see Additional file 1: Table S1 for complete species list of plant species pool). Monocultures, two-, four-, and eight-species mixtures were replicated 16 times, 16-species-mixtures were replicated 14 times and the complete species pool of 60 species was replicated four times. Sowing density amounted to 1000 viable seeds per m2 divided equally among species. Plant community composition was maintained by weeding all experimental plots three times per year (May, July, and September) to remove all non-target species. Here, we use the terms “resident” for plant species initially sown in experimental plots (i.e., target plant species) and “colonizing” for plant species not sown originally in the plots (i.e., non-target plant species).
We established two independent experiments (A and B) differing in length of plant colonization (experiment A: 2 years, experiment B: 5 years) within 80 main plots resulting in 160 subplots for each experiment in a split-plot design. Therefore, the sown plant species combination and planting density was the same in both experiments. In experiment A, two subplots of 1 × 1 m were established in autumn 2009. In one subplot, regular weeding was continued during the entire study, whereas in the other subplot, weeding was stopped for approximately 2 years allowing for plant colonization. Using a metal corer, five soil samples (diameter 2 cm, 10 cm deep) per subplot were randomly taken in June 2011. Additionally, plant cover (%) of resident and colonizing plant species were estimated using a modified decimal Londo scale  and used as a proxy for plant productivity. Numerical values for species cover were coded as 1 (<1 %), 2 (1–5 %), 10 (6–15 %), 20 (16–25 %), 30 (26–35 %), 40 (36–45 %), 50 (46–55 %), 60 (56–65 %), 70 (66–75 %), 80 (76–85 %), and 90 (>85 %). Subplots of experiment A subplots were given up after this sampling campaign and therefore they were no more available for further measurements.
In experiment B, new subplots (5 × 3 m) were established in 2009, following the same format as in experiment A: in one subplot, regular weeding was continued, and in the other subplot, weeding was stopped. Like experiment A, five soil samples per subplot were randomly taken within 1 × 1 m in May 2014, i.e., after 5 years of plant colonization in the non-weeded subplots. Here, plant productivity was measured in two 0.1 m2 plots as aboveground plant biomass (g m−2).
In both experiments, soil samples were pooled, homogenized, sieved (2 mm), and approximately 5 g (fresh weight) of each soil sample was used for the measurement of soil microbial biomass and respiration. Microbial respiration (µL O2 h−1 g−1 soil dry mass) was measured as mean of the O2 consumption rates of 14–24 h after the start of the measurements using an O2-microcompensation apparatus . Soil microbial biomass C (µg C g−1 soil dry mass) was measured by substrate-induced respiration (SIR) after the addition of d-glucose . Due to soil sieving fungal hyphae are broken up and therefore, this method mainly measures the respiration and biomass of soil bacteria. Gravimetric soil water content (%) was determined as the difference in percentages of fresh vs. dry soil (dried at 70 °C for 24 h).
First, we used General Linear Models (GLM) for a split-plot design (t-values with Satterthwaite approximation) to test effects of plant diversity (PD; manipulated at the plot level), plant colonization (COL; weeded vs. non-weeded subplots), and the interaction of plant diversity and plant colonization (PD × COL) on microbial respiration, microbial biomass (both experiments), plant cover (experiment A), plant biomass (experiment B), and number of colonizing plant species (both experiments). Second, we used a linear mixed effect model (t-values with Satterthwaite approximation) to test the effects of sown plant diversity (PD) in weeded and non-weeded plots independently on microbial respiration, microbial biomass (both experiments), plant cover (experiment A only), and plant biomass (experiment B only). Both analyses were performed using the core functions within the R statistical environment (R Development Core Team 2013) and the lme4 package .
LM table of t- and P-values on the effects of plant diversity (PD: 1, 2, 4, 8, 16, and 60 plant species) in weeded or non-weeded plots on number of colonizing plant species, plant cover (2011), plant biomass (2014), soil basal respiration, soil microbial biomass and soil water content of 2011 and 2014
Number of colonizing plant species
Soil basal respiration
Soil microbial biomass
Soil water content
Number of colonizing plant species
Soil basal respiration
Soil microbial biomass
Soil water content
Experiment A—effects of 2 years of plant colonization
GLM table of t- and P-values on the effects of plant diversity (PD: 1, 2, 4, 8, 16, and 60 plant species) and plant colonization (COL) on plant cover (2011), plant biomass (2014), soil basal respiration, soil microbial biomass and soil water content of 2011 and 2014
Soil basal respiration
Soil microbial biomass
Soil water content
PD × COL
Soil basal respiration
Soil microbial biomass
Soil water content
PD × COL
Experiment B—effects of 5 years of plant colonization
In experiment B, plant biomass increased with increasing plant diversity in weeded subplots, however this positive relationship disappeared in non-weeded subplots (Table 1; Fig. 2d; Additional file 2: Figure S2d). Despite these different trends, the interaction effect of plant diversity and plant colonization was not significant (Fig. 2d; Additional file 2: Figure S2d). Generally, plant biomass was significantly higher in non-weeded subplots than in weeded subplots (+120 %). In weeded subplots, soil basal respiration (Table 1; Fig. 3c; Additional file 3: Figure S3c) and microbial biomass (Table 1; Fig. 3d; Additional file 3: Figure S3d) increased significantly with increasing sown plant diversity. However, basal respiration and soil microbial biomass were not affected by sown plant diversity in non-weeded subplots, although the interaction effect of plant diversity and plant colonization was not significant (Tables 1, 2; Fig. 3c, d; Additional file 3: Figure S3c, d). Both basal respiration (+90 %) and soil microbial biomass (+104 %) were significantly higher in non-weeded subplots than in weeded subplots. Soil water content increased significantly with increasing plant diversity in weeded subplots but was not significantly affected by plant diversity after plant colonization in non-weeded subplots (Tables 1, 2).
Total productivity (plant coverage and biomass, respectively) of resident plant communities increased with increasing plant diversity in both experiments, confirming hypothesis 1 . In addition, numbers of colonizing plant species typically were high in species-poor plant communities and decreased with increasing plant diversity. In line with our findings, previous studies suggested that diverse plant communities better resist plant colonization than less diverse communities [29, 38] due to lower levels of available resources . Consequently, less resources are available for potential new colonizer species [40, 41]. Furthermore, there is evidence that large niche overlap between resident and colonizer species increases resistance against colonization [42, 43]. Generally, empty niche space is assumed to decline with increasing species richness [7, 13]. Thus, a diverse plant community should be more resistant to colonizer plant species when depending on similar resources [40, 44].
Importantly, colonizing plant species may change the quantity and quality of inputs to soil [45, 46], which has the potential to alter soil microbial functions and processes. In line with hypothesis 2, soil basal respiration and microbial biomass increased with increasing plant diversity in weeded subplots of both experiments . Type and number of plant species present have considerable influence on the functions and diversity of soil microorganisms [27, 47]. Soil microorganisms are involved in processes like decomposition and nutrient mineralization and their community composition and abundances have been shown to vary with plant species . Since increasing plant biomass production and release of rhizodeposits is associated with higher availability and diversity of plant-derived resources, we suggest that plant colonization positively influenced soil microbial properties in both experiments [26, 46]. Moreover, root morphological characteristics, litter types, and plant tissue qualities may affect the biomass of soil microorganisms . Therefore, an increase of plant species richness, presumably resulting in a convergence of plant community composition  in non-weeded subplots in both experiments, may have induced a shift in soil microbial properties equalizing the effects of the initially sown plant diversity gradient, confirming hypothesis 3. After 2 and 5 years of plant colonization, basal respiration and soil microbial biomass increased in species-poor plant communities in non-weeded subplots in comparison to weeded subplots. However, in species-rich plant communities soil microbial respiration and biomass decreased after 2 years of plant colonization, which is hard to explain. In contrast, after 5 years of plant colonization, basal respiration and soil microbial biomass were considerably higher across all plant diversity levels in non-weeded subplots, but particularly at low plant diversity. This indicates that time could play a crucial role in the establishment of plant diversity effects on soil microbial properties. Previous studies [31, 50] showed that several years are required to display significant plant diversity effects on soil microbial biomass due to the slow accumulation of plant-derived resources in the soil over time [51, 52]. Although such a temporal effect could explain the differences between the two experiments in the present study, please note that we only have two sampling dates, which does not allow us to infer temporal trends.
Our study highlights the consequences of plant colonization for resident plant communities and soil microbial properties. The results confirmed previous findings that experimental communities with higher numbers of resident plant species are more resistant to colonization than species-poor ones [30, 38]. Further, the present results show that plant community convergence induces the convergence of microbial properties in the soil. Colonizing plant species are likely to change the quantity and quality of inputs to the soil, thereby altering soil microbial functions and processes. Future studies should investigate the potential convergence of soil microbial community composition and multiple microbial functions. Further, it remains to explore specific plant traits effects on particular microbial taxa and functions in the soil, and if novel plant traits in a colonized plant community and convergence of the functional composition of plant communities are the underlying mechanisms of the observed convergence of soil microbial properties.
KS, TS, BJ, SS, and NE designed the study, KS, TS, BJ, and EL collected the data, KS analyzed the data and wrote the first draft of the manuscript, and all authors contributed to the subsequent version of the manuscript. All authors read and approved the final manuscript.
We would like to thank Madhav Prakash Thakur for his suggestions in data analysis. The Jena Experiment was funded by the Deutsche Forschungsgemeinschaft (German Research Foundation; FOR 1451). NE acknowledged funding by the German Research Foundation (Ei 862/3-2). We thank the gardeners, technicians, and managers for their work in maintaining the field site and also many student helpers for weeding of the experimental plots. We would like to thank two anonymous reviewers for their helpful comments, which considerably improved the manuscript.
Availability of data and materials
The data sets supporting the results of this article are uploaded in the data portal of the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany.
Availability of supporting data
The data sets supporting the results of this article are included within the article and its additional files.
The authors declare that they have no competing interests.
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Deutsche Forschungsgemeinschaft (German Research Foundation): FOR 1451 and Ei 862/3-2.
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- Wardle DA, Bardgett RD, Callaway RM, Van der Putten WH. Terrestrial ecosystem responses to species gains and losses. Science. 2011;332:1273–7.View ArticlePubMedGoogle Scholar
- Strayer DL. Eight questions about invasions and ecosystem functioning. Ecol Lett. 2012;15:1199–210.View ArticlePubMedGoogle Scholar
- Yachi S, Loreau M. Biodiversity and ecosystem productivity in a fluctuating environment : the insurance hypothesis. Proc Natl Acad Sci USA. 1999;96:1463–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Tilman D, Downing JA. Biodiversity and stability in grasslands. In: Samson FB et al, editors. Ecosystem management SE-1. New York: Springer; 1996. p. 3–7.View ArticleGoogle Scholar
- Isbell F, Craven D, Connolly J, Loreau M, Schmid B, Beierkuhnlein C, Bezemer TM, Bonin C, Bruelheide H, de Luca E, Ebeling A, Griffin JN, Guo Q, Hautier Y, Hector A, Jentsch A, Kreyling J, Lanta V, Manning P, Meyer ST, Mori AS, Naeem S, Niklaus PA, Polley HW, Reich PB, Roscher C, Seabloom EW, Smith MD, Thakur MP, Tilman D, et al. Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature. 2015;526:574–7.View ArticlePubMedGoogle Scholar
- Lehman CL, Tilman D. Biodiversity, Stability, and Productivity in Competitive Communities. Am Nat. 2000;156:534–52.View ArticleGoogle Scholar
- Tilman D. Niche tradeoffs, neutrality, and community structure : a stochastic theory of resource competition, invasion, and community assembly. PNAS. 2004;101:10854–61.View ArticlePubMedPubMed CentralGoogle Scholar
- Elton CS. The ecology of invasions by animals and plants. London: English Language Book Society; 1958.View ArticleGoogle Scholar
- Kennedy TA, Naeem S, Howe KM, Knops JMH, Tilman D, Reich P. Biodiversity as a barrier to ecological invasion. Nature. 2002;417:636–8.View ArticlePubMedGoogle Scholar
- Tilman D. Resource competition and community structure. Princeton: Monographes in Population Biology (Princeton University Press); 1982.Google Scholar
- Harpole WS, Tilman D. Grassland species loss resulting from reduced niche dimension. Nature. 2007;446:791–3.View ArticlePubMedGoogle Scholar
- Emery SM. Limiting similarity between invaders and dominant species in herbaceous plant communities? J Ecol. 2007;95:1027–35.View ArticleGoogle Scholar
- Eisenhauer N, Dobies T, Cesarz S, Hobbie SE, Meyer RJ, Worm K, Reich PB. Plant diversity effects on soil food webs are stronger than those of elevated CO2 and N deposition in a long-term grassland experiment. Proc Natl Acad Sci. 2013;110:6889–94.View ArticlePubMedPubMed CentralGoogle Scholar
- Hooper DU, Dukes JS. Functional composition controls invasion success in a California serpentine grassland. J Ecol. 2010;98:764–77.View ArticleGoogle Scholar
- Tilman D, Reich PB, Knops JMH. Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature. 2006;441:629–32.View ArticlePubMedGoogle Scholar
- Cardinale BJ, Wright JP, Cadotte MW, Carroll IT, Hector A, Srivastava DS, Loreau M, Weis JJ. Impacts of plant diversity on biomass production increase through time because of species complementarity. Proc Natl Acad Sci USA. 2007;104:18123–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Wardle DA. Experimental demonstration that plant diversity reduces invasibility—evidence of a biological mechanism or a consequence of sampling effect ? Oikos. 2001;95:161–70.View ArticleGoogle Scholar
- Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH, Setala H. Ecological linkages between aboveground and belowground biota. Science. 2004;304:1629–33.View ArticlePubMedGoogle Scholar
- Weidenhamer JD, Callaway RM. Direct and indirect effects of invasive plants on soil chemistry and ecosystem function. J Chem Ecol. 2010;36:59–69.View ArticlePubMedGoogle Scholar
- Ehrenfeld JG. Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst. 2010;41:59–80.View ArticleGoogle Scholar
- Batten KM, Scow KM, Davies KF, Harrison SP. Two invasive plants alter soil microbial community composition in serpentine grasslands. Biol Invasions. 2006;8:217–30.View ArticleGoogle Scholar
- Inderjit, van der Putten WH. Impacts of soil microbial communities on exotic plant invasions. Trends Ecol Evol. 2010;25:512–9.View ArticlePubMedGoogle Scholar
- Stephan A, Meyer AH, Schmid B. Plant diversity affects culturable soil bacteria in experimental grassland communities. J Ecol Ecol. 2000;88:988–98.View ArticleGoogle Scholar
- Chung H, Zak DR, Reich PB, Ellsworth DS. Plant species richness, elevated CO2, and atmospheric nitrogen deposition alter soil microbial community composition and function. Glob Chang Biol. 2007;13:980–9.View ArticleGoogle Scholar
- Steinauer K, Tilman GD, Wragg PD, Cesarz S, Cowles JM, Pritsch K, Reich PB, Weisser WW, Eisenhauer N. Plant diversity effects on soil microbial functions and enzymes are stronger than warming in a grassland experiment. Ecology. 2015;96:99–112.View ArticlePubMedGoogle Scholar
- Zak DR, Holmes WE, White DC, Peacock AD, Tilman D. Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology. 2003;84:2042–50.View ArticleGoogle Scholar
- Lange M, Eisenhauer N, Sierra CA, Bessler H, Engels C, Griffiths RI, Mellado-Vazquez PG, Malik AA, Roy J, Scheu S, Steinbeiss S, Thomson BC, Trumbore SE, Gleixner G, Mellado-va PG, Thomson BC, Trumbore SE, Gleixner G. Plant diversity increases soil microbial activity and soil carbon storage. Nat Commun. 2015;6(6707):1–8.Google Scholar
- Hooper DU, Bignell DE, Brown VK, Brussaard L, Dangerfiled Mark, Wall DH, Wardle DA, Coleman DC. Interactions between aboveground and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms, and feedbacks. Bioscience. 2000;50:1049–61.View ArticleGoogle Scholar
- Roscher C, Beßler H, Oelmann Y, Engels C, Wilcke W, Schulze ED. Resources, recruitment limitation and invader species identity determine pattern of spontaneous invasion in experimental grasslands. J Ecol. 2009;97:32–47.View ArticleGoogle Scholar
- Roscher C, Temperton VM, Buchmann N, Schulze ED. Community assembly and biomass production in regularly and never weeded experimental grasslands. Acta Oecol. 2009;35:206–17.View ArticleGoogle Scholar
- Eisenhauer N. Plant diversity effects on soil microorganisms support the singular hypothesis. Ecology. 2010;91:485–96.View ArticlePubMedGoogle Scholar
- Wardle D, Lavelle P. Linkages between soil biota, plant litter quality and decomposition. In: Cadisch G, Giller KE, editors. Driven by nature: plant litter quality and decomposition. Wallingford: CAB International; 1997. p. 107–25.Google Scholar
- Roscher C, Schumacher J, Baade J, Wilcke W, Gleixner G, Weisser WW, Schmid B, Schulze E-D. The role of biodiversity for element cycling and trophic interactions : an experimental approach in a grassland community. Basic Appl Ecol. 2004;5:107–21.View ArticleGoogle Scholar
- Londo. The decimal scale for releves of permanent quadrats. Vegetatio. 1976;33:61–4.View ArticleGoogle Scholar
- Scheu S. Automated measurement of the respiratory response of soil microcompartments: active microbial biomass in earthworm faeces. Soil Biol Biochem. 1992;11:1113–8.View ArticleGoogle Scholar
- Anderson JM, Domsch K. A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem. 1978;10:215–21.View ArticleGoogle Scholar
- Bates D, Maechler M, Bolker B. lme4: linear mixed-effects models using Eigen and S4. R package. 2015Google Scholar
- Petermann JS, Fergus AJF, Roscher C, Turnbull LA, Weigelt A, Schmid B. Biology, chance, or history? The predictable reassembly of temperate grassland communities. Ecology. 2010;91:408–21.View ArticlePubMedGoogle Scholar
- Fargione JE, Tilman D. Diversity decreases invasion via both sampling and complementarity effects. Ecol Lett. 2005;8:604–11.View ArticleGoogle Scholar
- Fargione JE, Brown CS, Tilman D. Community assembly and invasion: an experimental test of neutral versus niche processes. PNAS. 2003;100:8916–20.View ArticlePubMedPubMed CentralGoogle Scholar
- Hector A, Dobson K, Minns A, Bazeley-White E, Hartley Lawton J. Community diversity and invasion resistance: an experimental test in a grassland ecosystem and a review of comparable studies. Ecol Res. 2001;16:819–31.View ArticleGoogle Scholar
- Mwangi PN, Schmitz M, Scherber C, Roscher C, Schumacher J, Scherer-Lorenzen M, Weisser WW, Schmid B. Niche pre-emption increases with species richness in experimental plant communities. J Ecol. 2007;95:65–78.View ArticleGoogle Scholar
- Frankow-Lindberg BE. Grassland plant species diversity decreases invasion by increasing resource use. Oecologia. 2012;169:793–802.View ArticlePubMedGoogle Scholar
- Turnbull LA, Rahm S, Baudois O, Eichenberger-Glinz S, Wacker L, Schmid B. Experimental invasion by legumes reveals non-random assembly rules in grassland communities. J Ecol. 2005;93:1062–70.View ArticleGoogle Scholar
- Holly DC, Ervin GN, Jackson CR, Diehl SV, Kirker GT. Effect of an invasive grass on ambient rates of decomposition and microbial community structure: a search for causality. Biol Invasions. 2008;11:1855–68.View ArticleGoogle Scholar
- Ehrenfeld JG. Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems. 2003;6:503–23.View ArticleGoogle Scholar
- Spehn EM, Joshi J, Schmid B, Alphei J, Körner C. Plant diversity effects on soil heterotrophic activity in experimental grassland ecosystems. Plant Soil. 2000;224:217–30.View ArticleGoogle Scholar
- Ehrenfeld JG, Ravit B, Elgersma K. Feedback in the Plant-Soil System. Annu Rev Environ Resour. 2005;30:75–115.View ArticleGoogle Scholar
- Porazinska D, Bardgett R. Relationships at the aboveground-belowground interface: plants, soil biota, and soil processes. Ecol Monogr. 2003;73:377–95.View ArticleGoogle Scholar
- Thakur MP, Milcu A, Manning P. Plant diversity drives soil microbial biomass carbon in grasslands irrespective of global environmental change factors. Glob Chang Biol. 2015;21:4076–85.View ArticlePubMedGoogle Scholar
- Eisenhauer N, Reich PB. Above- and below-ground plant inputs both fuel soil food webs. Soil Biol Biochem. 2012;45:156–60.View ArticleGoogle Scholar
- Kuzyakov Y, Xu X. Tansley review Competition between roots and microorganisms for nitrogen : mechanisms and ecological relevance. New Phytol. 2013;198:656–69.View ArticlePubMedGoogle Scholar