Yakov Kuzyakov

Review of mechanisms and quantification of priming effects.

Abstract Priming effects are strong short-term changes in the turnover of soil organic matter caused by comparatively moderate treatments of the soil. In the course of priming effects large amounts of C, N and other nutrients can be released or immobilized in soil in a very short time. These effects have been measured in many field and laboratory experiments; however, only a few of the studies were aimed at an extended investigation of the mechanisms of such phenomena. The aim of this overview is to reveal possible causes and processes leading to priming actions using the references on agricultural ecosystems and model experiments. Multiple mechanisms and sources of released C and N are presented and summarized in Tables for positive and negative real and apparent priming effects induced after the addition of different organic and mineral substances to the soil. Soil microbial biomass plays the key role in the processes leading to the real priming effects. The most important mechanisms for the real priming effects are the acceleration or retardation of soil organic matter turnover due to increased activity or amount of microbial biomass. Isotopic exchange, pool substitution, and different uncontrolled losses of mineralized N from the soil are responsible for the apparent N priming effects. Other multiple mechanisms (predation, competition for nutrients between roots and microorganisms, preferred uptake, inhibition, etc.) in response to addition of different substances are also discussed. These mechanisms can be distinguished from each other by the simultaneous monitoring of C and N release dynamics; its comparison with the course of microbial activity; and by the labelling of different pools with 14 C or 13 C and 15 N. Quantitative methods for describing priming effects and their dynamics using 14 C and 15 N isotopes, as well as for non-isotopic studies are proposed.

Carbon input by plants into the soil. Review

The methods used for estimating below-ground carbon (C) translocation by plants, and the results obtained for different plant species are reviewed. Three tracer techniques using C isotopes to quantify root-derived C are discussed: pulse labeling, continuous labeling, and a method based on the difference in 13 C natural abundance in C3 and C4 plants. It is shown, that only the tracer methods provided adequate results for the whole below-ground C translocation. This included roots, exudates and other organic substances, quickly decomposable by soil microorganisms, and CO 2 produced by root respiration. Advantages due to coupling of two different tracer techniques are shown. The differences in the below-ground C translocation pattern between plant species (cereals, grasses, and trees) are discussed. Cereals (wheat and barley) transfer 20%-30% of total assimilated C into the soil. Half of this amount is subsequently found in the roots and about one-third in CO2 evolved from the soil by root respiration and microbial utilization of rootborne organic substances. The remaining part of below-ground translocated C is incorporated into the soil microorganisms and soil organic matter. The portion of assimilated C allocated below the ground by cereals decreases during growth and by increasing N fertilization. Pasture plants translocated about 30%-50% of assimilates below-ground, and their translocation patterns were similar to those of crop plants. On average, the total C amounts translocated into the soil by cereals and pasture plants are approximately the same (1500 kg C ha -1 ), when the same growth period is considered. However, during one vegetation period the cereals and grasses allocated beneath the ground about 1500 and 2200kg C ha -1 , respectively. Finally, a simple approach is suggested for a rough calculation of C input into the soil and for root-derived CO 2 efflux from the soil.

Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review

The number of studies on priming effects (PE) in soil has strongly increased during the last years. The information regarding real versus apparent PE as well as their mechanisms remains controversial. Based on a meta-analysis of studies published since 1980, we evaluated the intensity, direction, and the reality of PE in dependence on the amount and quality of added primers, the microbial biomass and community structure, enzyme activities, soil pH, and aggregate size. The meta-analysis allowed revealing quantitative relationships between the amounts of added substrates as related to microbial biomass C and induced PE. Additions of easily available organic C up to 15% of microbial biomass C induce a linear increase of extra CO2. When the added amount of easily available organic C is higher than 50% of the microbial biomass C, an exponential decrease of the PE or even a switch to negative values is often observed. A new approach based on the assessment of changes in the production of extracellular enzymes is suggested to distinguish real and apparent PE. To distinguish real and apparent PE, we discuss approaches based on the C budget. The importance of fungi for long-term changes of SOM decomposition is underlined. Priming effects can be linked with microbial community structure only considering changes in functional diversity. We conclude that the PE involves not only one mechanism but a succession of processes partly connected with succession of microbial community and functions. An overview of the dynamics and intensity of these processes as related to microbial biomass changes and C and N availability is presented.

Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance

Demand of all living organisms on the same nutrients forms the basis for interspecific competition between plants and microorganisms in soils. This competition is especially strong in the rhizosphere. To evaluate competitive and mutualistic interactions between plants and microorganisms and to analyse ecological consequences of these interactions, we analysed 424 data pairs from 41 (15)N-labelling studies that investigated (15)N redistribution between roots and microorganisms. Calculated Michaelis-Menten kinetics based on K(m) (Michaelis constant) and V(max) (maximum uptake capacity) values from 77 studies on the uptake of nitrate, ammonia, and amino acids by roots and microorganisms clearly showed that, shortly after nitrogen (N) mobilization from soil organic matter and litter, microorganisms take up most N. Lower K(m) values of microorganisms suggest that they are especially efficient at low N concentrations, but can also acquire more N at higher N concentrations (V(max)) compared with roots. Because of the unidirectional flow of nutrients from soil to roots, plants are the winners for N acquisition in the long run. Therefore, despite strong competition between roots and microorganisms for N, a temporal niche differentiation reflecting their generation times leads to mutualistic relationships in the rhizosphere. This temporal niche differentiation is highly relevant ecologically because it: protects ecosystems from N losses by leaching during periods of slow or no root uptake; continuously provides roots with available N according to plant demand; and contributes to the evolutionary development of mutualistic interactions between roots and microorganisms.

Carbon partitioning and below-ground translocation by Lolium perenne

Carbon (C) balance, rhizodeposition and root respiration during development of Lolium perenne were studied on a loamy Gleyic Cambisol by 14 CO2 pulse labeling of shoots in a two-compartment chamber under controlled laboratory conditions. The losses from shoot respiration were about 36% of the total assimilated C. The highest respiration intensity was measured in the first night after the labeling, and diminishes exponentially over time. Total 14 CO2 efflux from the soil (root respiration, microbial respiration of exudates and dead roots) in the first eight days after the 14 C pulse labeling increased with plant development from 2.7 to 11% of the total 14 C assimilated by plants. A model approach used for the partitioning of rhizosphere respiration showed that measured root respiration was between 1.4 and 3.5% of assimilated 14 C, while microbial respiration of easily available rhizodeposits and dead root residues was between 0.9 and 6.8% of assimilated C. Both respiration processes increased during plant development. However, only the increase in root respiration was significant. The average contribution of root respiration to total 14 CO2 efflux from the soil was approximately 46%. Total CO2 efflux from the soil was separated into plant-derived and soil-derived CO2 using 14 C labeling. Additional decomposition of soil organic matter (positive priming effects) in rhizosphere was calculated by subtracting the CO2 efflux from bare soil from soil-derived CO2 efflux from soil with plants. Priming effects due to plant rhizodeposition reach 60 kg of C ha 21 d 21 . 14 C incorporated in soil micro-organisms (extraction‐fumigation) amounts to 0.8‐3.2% of assimilated C. The total below-ground transfer of organic C by Lolium perenne was about 2800 kg of C ha 21 . The C input into the soil consists of about 50% of easily available organic substances. q 2001 Elsevier Science Ltd. All

Biochar stability in soil: meta‐analysis of decomposition and priming effects

The stability and decomposition of biochar are fundamental to understand its persistence in soil, its contribution to carbon (C) sequestration, and thus its role in the global C cycle. Our current knowledge about the degradability of biochar, however, is limited. Using 128 observations of biochar‐derived CO2 from 24 studies with stable (13C) and radioactive (14C) carbon isotopes, we meta‐analyzed the biochar decomposition in soil and estimated its mean residence time (MRT). The decomposed amount of biochar increased logarithmically with experimental duration, and the decomposition rate decreased with time. The biochar decomposition rate varied significantly with experimental duration, feedstock, pyrolysis temperature, and soil clay content. The MRTs of labile and recalcitrant biochar C pools were estimated to be about 108 days and 556 years with pool sizes of 3% and 97%, respectively. These results show that only a small part of biochar is bioavailable and that the remaining 97% contribute directly to long‐term C sequestration in soil. The second database (116 observations from 21 studies) was used to evaluate the priming effects after biochar addition. Biochar slightly retarded the mineralization of soil organic matter (SOM; overall mean: −3.8%, 95% CI = −8.1–0.8%) compared to the soil without biochar addition. Significant negative priming was common for studies with a duration shorter than half a year (−8.6%), crop‐derived biochar (−20.3%), fast pyrolysis (−18.9%), the lowest pyrolysis temperature (−18.5%), and small application amounts (−11.9%). In contrast, biochar addition to sandy soils strongly stimulated SOM mineralization by 20.8%. This indicates that biochar stimulates microbial activities especially in soils with low fertility. Furthermore, abiotic and biotic processes, as well as the characteristics of biochar and soils, affecting biochar decomposition are discussed. We conclude that biochar can persist in soils on a centennial scale and that it has a positive effect on SOM dynamics and thus on C sequestration.

Separating microbial respiration of exudates from root respiration in non-sterile soils: a comparison of four methods

Partitioning the root-derived CO2 efflux from the soil into actual root respiration (RR) and microbial respiration of exudates and root residues is very important for determining the carbon (C) and energy balance of soils. Studies based on artificial root environments like hydroponics or sterile soils give unrealistic figures for C partitioning and are unsuitable for predicting C flows under natural conditions. To date, only four methods have been suggested to separate RR and rhizomicrobial respiration in non-sterile soils: (1) the isotope dilution method, (2) the model rhizodeposition technique, (3) modeling of 14CO2 efflux dynamics, and (4) the exudate elution procedure. All four methods are based on the pulse labeling of shoots in a 14CO2 atmosphere and subsequent monitoring of 14CO2 efflux from the soil. However, the basic assumptions and principles of these methods, as well as the results observed in the original papers, all differ from one another. This study describes the separation of RR of Lolium perenne grown on a loamy Haplic Luvisol from microbial respiration of rhizodeposits by means of all four methods under the same experimental conditions. In spite of alternative principles, the isotope dilution and the 14CO2 dynamics methods show a similar level of RR: accordingly, 39 and 45% of total root-derived CO2 efflux were accounted for by RR. The remainder is rhizomicrobial respiration. The exudate elution method, which underestimates the total rhizodeposition, shows that at least 19% of root-derived CO2 is produced by exudate decomposition. The microbial respiration of rhizodeposits calculated using the model rhizodeposition technique is also underestimated. The exudate elution method is the only procedure allowing physical separation of both C flows. The assumptions and principles of all four methods are reviewed and the effects of possible shortcomings on the separation results are discussed. In conclusion, RR contributes about 40–50% to the root-derived CO2 efflux. The remaining 50–60% comprise the microbial decomposition of root exudates and other rhizodeposits. The longer the period of monitoring the CO2 efflux after the pulse labeling is, the higher the contribution of rhizomicrobial respiration to the total root-derived CO2 efflux from soil.

Contribution of Lolium perenne rhizodeposition to carbon turnover of pasture soil

Carbon rhizodeposition and root respiration during eight development stages of Lolium perenne were studied on a loamy Gleyic Cambisol by 14CO2 pulse labelling of shoots in a two compartment chamber under controlled laboratory conditions. Total 14CO2 efflux from the soil (root respiration, microbial respiration of exudates and dead roots) in the first 8 days after 14C pulse labelling decreased during plant development from 14 to 6.5% of the total 14C input. Root respiration accounted for was between 1.5 and 6.5% while microbial respiration of easily available rhizodeposits and dead root remains were between 2 and 8% of the 14C input. Both respiration processes were found to decline during plant development, but only the decrease in root respiration was significant. The average contribution of root respiration to total 14CO2 efflux from the soil was approximately 41%. Close correlation was found between cumulative 14CO2 efflux from the soil and the time when maximum 14CO2 efflux occurred (r=0.97). The average total of CO2 Defflux from the soil with Lolium perenne was approximately 21 μg C-CO2 d−1 g−1. It increased slightly during plant development. The contribution of plant roots to total CO2 efflux from the soil, calculated as the remainder from respiration of bare soil, was about 51%. The total 14C content after 8 days in the soil with roots ranged from 8.2 to 27.7% of assimilated carbon. This corresponds to an underground carbon transfer by Lolium perenne of 6–10 g C m−2 at the beginning of the growth period and 50–65 g C m−2 towards the end of the growth period. The conventional root washing procedure was found to be inadequate for the determination of total carbon input in the soil because 90% of the young fine roots can be lost.

Carbon flows in the rhizosphere of ryegrass (Lolium perenne)

This study addresses the issue of carbon (C) fluxes through below ground pools within the rhizosphere of Lolium perenne using the 14C pulse labeling. Lolium perenne was grown in plexiglas chambers on topsoil of a Haplic Luvisol under controled laboratory conditions. 14C-CO2 efflux from soil, as well as 14C content in shoots, roots, soil, dissolved organic C (DOC), and microbial biomass were monitored for 11 days after the pulsing. Lolium allocates about 48 % of the total assimilated 14C below the soil surface, and roots were the primary sink for this C. Maximum 14C content in the roots was observed 12 hours after the labeling and it amounts to 42 % of the assimilated C. Only half of the 14C amount was found in the roots at the end of the monitoring period. The remainder was lost through root respiration, root decomposition, and rhizodeposition. Six hours after the 14C pulse labeling soil accounted for 11 %, DOC for 1.1 %, and microbial biomass for 4.9 % of assimilated C. 14C in CO2 efflux from soil was detected as early as 30 minutes after labeling. The maximum 14C-CO2 emission rate (0.34 % of assimilated 14C h—1) from the soil occurred between four and twelve hours after labeling. From the 5th day onwards, only insignificant changes in carbon partitioning occurred. The partitioning of assimilated C was completed after 5 days after assimilation. Based on the 14C partitioning pattern, we calculated the amount of assimilated C during 47 days of growth at 256 g C m—2. Of this amount 122 g C m—2 were allocated to below ground, shoots retained 64 g C m—2, and 70 g C m—2 were lost from the shoots due to respiration. Roots were the main sink for below ground C and they accounted for 74 g C m—2, while 28 g C m—2 were respired and 19 g C m—2 were found as residual 14C in soil and microorganisms. Kohlenstoffflusse in der Rhizosphare von Weidelgras (Lolium perenne) In dieser Arbeit wurden die Kohlenstoff (C)-Flusse in der Rhizosphare von Lolium perenne mit Hilfe von 14C-Pulsmarkierung unter kontrollierten Laborbedingungen auf einem lehmigen Haplic Luvisol (Parabraunerde) untersucht. Uber 11 Tage nach der Markierung wurde die 14C-Dynamik in Blattern, Wurzeln, Boden, gelostem organischen Kohlenstoff (DOC), CO2-Efflux aus dem Boden und mikrobieller Bodenbiomasse verfolgt. Lolium verlagerte 48 % des assimilierten 14C unter die Bodenoberflache, wobei C primar in die Wurzeln eingebaut wurde. 12 Stunden nach der Markierung erreichte 14C in den Wurzeln ein Maximum von 42 % des assimilierten 14C. Nur die Halfte dieser Menge wurde nach 11 Tagen in den Wurzeln wiedergefunden. Der Rest wurde durch Wurzelatmung, Wurzelabbau und Rhizodeposition verbraucht. 6 Stunden nach der Markierung wurden im Boden 11 %, im DOC 1,1 % und in der mikrobiellen Biomasse 4,9 % des assimilierten C gefunden. 14C in dem wurzelburtigen CO2 wurde schon 30 Minuten nach der Markierung festgestellt, wobei das Maximum des wurzelburtigen CO2-Effluxes (0,34 % des assimilierten 14C h—1) zwischen vier und zwolf Stunden nach der Markierung festgestellt wurde. Nach funf Tagen wurden keine signifikanten Anderungen mehr in der Umverteilung des assimilierten Kohlenstoffs gemessen. Im Laufe von 47 Tagen assimilierte Lolium 256 g C m—2, davon wurden 122 g C m—2 unter die Bodenoberflache transportiert, 64 g C m—2 wurden in den Blattern wiedergefunden und 70 g C m—2 wurden durch die Blattatmung verbraucht. In die Wurzel wurden 74 g C m—2 eingebaut, 28 g C m—2 wurden in der Rhizosphare veratmet und 19 g C m—2 verblieben im Boden sowie in der mikrobiellen Biomasse.

Losses of soil carbon by converting tropical forest to plantations: erosion and decomposition estimated by δ13C

Indonesia lost more tropical forest than all of Brazil in 2012, mainly driven by the rubber, oil palm, and timber industries. Nonetheless, the effects of converting forest to oil palm and rubber plantations on soil organic carbon (SOC) stocks remain unclear. We analyzed SOC losses after lowland rainforest conversion to oil palm, intensive rubber, and extensive rubber plantations in Jambi Province on Sumatra Island. The focus was on two processes: (1) erosion and (2) decomposition of soil organic matter. Carbon contents in the Ah horizon under oil palm and rubber plantations were strongly reduced up to 70% and 62%, respectively. The decrease was lower under extensive rubber plantations (41%). On average, converting forest to plantations led to a loss of 10 Mg C ha(-1) after about 15 years of conversion. The C content in the subsoil was similar under the forest and the plantations. We therefore assumed that a shift to higher δ(13) C values in plantation subsoil corresponds to the losses from the upper soil layer by erosion. Erosion was estimated by comparing the δ(13) C profiles in the soils under forest and under plantations. The estimated erosion was the strongest in oil palm (35 ± 8 cm) and rubber (33 ± 10 cm) plantations. The (13) C enrichment of SOC used as a proxy of its turnover indicates a decrease of SOC decomposition rate in the Ah horizon under oil palm plantations after forest conversion. Nonetheless, based on the lack of C input from litter, we expect further losses of SOC in oil palm plantations, which are a less sustainable land use compared to rubber plantations. We conclude that δ(13) C depth profiles may be a powerful tool to disentangle soil erosion and SOC mineralization after the conversion of natural ecosystems conversion to intensive plantations when soils show gradual increase of δ(13) C values with depth.