Earthworms as catalysts in the formation and stabilization of soil microbial necromass.

Microbial necromass is a central component of soil organic matter (SOM), whose management may be essential in mitigating atmospheric CO2 concentrations and climate change. Current consensus regards the magnitude of microbial necromass production to be heavily dependent on the carbon use efficiency of microorganisms, which is strongly influenced by the quality of the organic matter inputs these organisms feed on. However, recent concepts neglect agents relevant in many soils: earthworms. We argue that the activity of earthworms accelerates the formation of microbial necromass stabilized in aggregates and organo-mineral associations and reduces the relevance of the quality of pre-existing organic matter in this process. Earthworms achieve this through the creation of transient hotspots (casts) characterized by elevated contents of bioavailable substrate and the efficient build-up and quick turnover of microbial biomass, thus converting SOM not mineralized in this process into a state more resistant against external disturbances, such as climate change. Promoting the abundance of earthworms may, therefore, be considered a central component of management strategies that aim to accelerate the formation of stabilized microbial necromass in wide locations of the soil commonly not considered hotspots of microbial SOM formation.

Is the climate change mitigation effect of enhanced silicate weathering governed by biological processes?

A number of negative emission technologies (NETs) have been proposed to actively remove CO2 from the atmosphere, with enhanced silicate weathering (ESW) as a relatively new NET with considerable climate change mitigation potential. Models calibrated to ESW rates in lab experiments estimate the global potential for inorganic carbon sequestration by ESW at about 0.5-5 Gt CO2  year-1 , suggesting ESW could be an important component of the future NETs mix. In real soils, however, weathering rates may differ strongly from lab conditions. Research on natural weathering has shown that biota such as plants, microbes, and macro-invertebrates can strongly affect weathering rates, but biotic effects were excluded from most ESW lab assessments. Moreover, ESW may alter soil organic carbon sequestration and greenhouse gas emissions by influencing physicochemical and biological processes, which holds the potential to perpetuate even larger negative emissions. Here, we argue that it is likely that the climate change mitigation effect of ESW will be governed by biological processes, emphasizing the need to put these processes on the agenda of this emerging research field.

Soil fauna diversity increases CO2 but suppresses N2 O emissions from soil.

Soil faunal activity can be a major control of greenhouse gas (GHG) emissions from soil. Effects of single faunal species, genera or families have been investigated, but it is unknown how soil fauna diversity may influence emissions of both carbon dioxide (CO2 , end product of decomposition of organic matter) and nitrous oxide (N2 O, an intermediate product of N transformation processes, in particular denitrification). Here, we studied how CO2 and N2 O emissions are affected by species and species mixtures of up to eight species of detritivorous/fungivorous soil fauna from four different taxonomic groups (earthworms, potworms, mites, springtails) using a microcosm set-up. We found that higher species richness and increased functional dissimilarity of species mixtures led to increased faunal-induced CO2 emission (up to 10%), but decreased N2 O emission (up to 62%). Large ecosystem engineers such as earthworms were key drivers of both CO2 and N2 O emissions. Interestingly, increased biodiversity of other soil fauna in the presence of earthworms decreased faunal-induced N2 O emission despite enhanced C cycling. We conclude that higher soil fauna functional diversity enhanced the intensity of belowground processes, leading to more complete litter decomposition and increased CO2 emission, but concurrently also resulting in more complete denitrification and reduced N2 O emission. Our results suggest that increased soil fauna species diversity has the potential to mitigate emissions of N2 O from soil ecosystems. Given the loss of soil biodiversity in managed soils, our findings call for adoption of management practices that enhance soil biodiversity and stimulate a functionally diverse faunal community to reduce N2 O emissions from managed soils.

Long-term nitrogen loading alleviates phosphorus limitation in terrestrial ecosystems.

Increased human-derived nitrogen (N) deposition to terrestrial ecosystems has resulted in widespread phosphorus (P) limitation of net primary productivity. However, it remains unclear if and how N-induced P limitation varies over time. Soil extracellular phosphatases catalyze the hydrolysis of P from soil organic matter, an important adaptive mechanism for ecosystems to cope with N-induced P limitation. Here we show, using a meta-analysis of 140 studies and 668 observations worldwide, that N stimulation of soil phosphatase activity diminishes over time. Whereas short-term N loading (≤5 years) significantly increased soil phosphatase activity by 28%, long-term N loading had no significant effect. Nitrogen loading did not affect soil available P and total P content in either short- or long-term studies. Together, these results suggest that N-induced P limitation in ecosystems is alleviated in the long-term through the initial stimulation of soil phosphatase activity, thereby securing P supply to support plant growth. Our results suggest that increases in terrestrial carbon uptake due to ongoing anthropogenic N loading may be greater than previously thought.

What plant functional traits can reduce nitrous oxide emissions from intensively managed grasslands?

Plant species exert a dominant control over the nitrogen (N) cycle of natural and managed grasslands. Although in intensively managed systems that receive large external N inputs the emission of the potent greenhouse gas nitrous oxide (N2 O) is a crucial component of this cycle, a mechanistic relationship between plant species and N2 O emissions has not yet been established. Here we use a plant functional trait approach to study the relation between plant species strategies and N2 O emissions from soils. Compared to species with conservative strategies, species with acquisitive strategies have higher N uptake when there is ample N in the soil, but also trigger N mineralization when soil N is limiting. Therefore, we hypothesized that (1) compared to conservative species, species with acquisitive traits reduce N2 O emissions after a high N addition; and (2) species with conservative traits have lower N2 O emissions than acquisitive plants if there is no high N addition. This was tested in a greenhouse experiment using monocultures of six grass species with differing above- and below-ground traits, growing across a gradient of soil N availability. We found that acquisitive species reduced N2 O emissions at all levels of N availability, produced higher biomass and showed larger N uptake. As such, acquisitive species had 87% lower N2 O emissions per unit of N uptake than conservative species (p < .05). Structural equation modelling revealed that specific leaf area and root length density were key traits regulating the effects of plants on N2 O emission and biomass productivity. These results provide the first framework to understand the mechanisms through which plants modulate N2 O emissions, pointing the way to develop productive grasslands that contribute optimally to climate change mitigation.

Plant species identity surpasses species richness as a key driver of N(2)O emissions from grassland.

Grassland ecosystems worldwide not only provide many important ecosystem services but they also function as a major source of the greenhouse gas nitrous oxide (N2O), especially in response to nitrogen deposition by grazing animals. To explore the role of plants as mediators of these emissions, we tested whether and how N2O emissions are dependent on grass species richness and/or specific grass species composition in the absence and presence of urine deposition. We hypothesized that: (i) N2O emissions relate negatively to plant productivity; (ii) four-species mixtures have lower emissions than monocultures (as they are expected to be more productive); (iii) emissions are lowest in combinations of species with diverging root morphology and high root biomass; and (iv) the identity of the key species that reduce N2O emissions is dependent on urine deposition. We established monocultures and two- and four-species mixtures of common grass species with diverging functional traits: Lolium perenne L. (Lp), Festuca arundinacea Schreb. (Fa), Phleum pratense L. (Php) and Poa trivialis L. (Pt), and quantified N2O emissions for 42 days. We found no relation between plant species richness and N2O emissions. However, N2O emissions were significantly reduced in specific plant species combinations. In the absence of urine, plant communities of Fa+Php acted as a sink for N2O, whereas the monocultures of these species constituted a N2O source. With urine application Lp+Pt plant communities reduced (P < 0.001) N2O emissions by 44% compared to monocultures of Lp. Reductions in N2O emissions by species mixtures could be explained by total biomass productivity and by complementarity in root morphology. This study shows that plant species composition is a key component underlying N2O emissions from grassland ecosystems. Selection of specific grass species combinations in the context of the expected nitrogen deposition regimes may therefore provide a key for mitigation of N2O emissions.

Soil biochar amendment in a nature restoration area: effects on plant productivity and community composition.

Biochar (pyrolyzed biomass) amendment to soils has been shown to have a multitude of positive effects, e.g., on crop yield, soil quality, nutrient cycling, and carbon sequestration. So far the majority of studies have focused on agricultural systems, typically with relatively low species diversity and annual cropping schemes. How biochar amendment affects plant communities in more complex and diverse ecosystems that can evolve over time is largely unknown. We investigated such effects in a field experiment at a Dutch nature restoration area. In April 2011, we set up an experiment using biochar produced from cuttings collected from a local natural grassland. The material was pyrolyzed at 400 degrees C or at 600 degrees C. After biochar or residue (non-pyrolyzed cuttings) application (10 Mg/ha), all plots, including control (0 Mg/ ha) plots, were sown with an 18-species grassland mixture. In August 2011, we determined characteristics of the developed plant community, as well as soil nutrient status. Biochar amendment did not alter total plant productivity, but it had a strong and significant effect on plant community composition. Legumes were three times as abundant and individual legume plants increased four times in biomass in plots that received biochar as compared to the control treatment. Biomass of the most abundant forb (Plantago lanceolata) was not affected by biochar addition. Available phosphorous, potassium, and pH were significantly higher in soils that received biochar than in Control soils. The rate of biological nitrogen fixation and seed germination were not altered by biochar amendment, but the total amount of biological N fixed per Trifolium pratense (red clover) plant was more than four times greater in biochar-amended soil. This study demonstrates that biochar amendment has a strong and rapid effect on plant communities and soil nutrients. Over time these changes may cascade up to other trophic groups, including above- and belowground organisms. Our results emphasize the need for long-term studies that examine not only the short-term effects of biochar amendment, but also follow how these effects evolve over time and affect ecosystem functioning.

Design and Construction of an Experimental Setup to Enhance Mineral Weathering through the Activity of Soil Organisms.

Enhanced weathering (EW) is an emerging carbon dioxide (CO2) removal technology that can contribute to climate change mitigation. This technology relies on accelerating the natural process of mineral weathering in soils by manipulating the abiotic variables that govern this process, in particular mineral grain size and exposure to acids dissolved in water. EW mainly aims at reducing atmospheric CO2 concentrations by enhancing inorganic carbon sequestration. Until now, knowledge of EW has been mainly gained through experiments that focused on the abiotic variables known for stimulating mineral weathering, thereby neglecting the potential influence of biotic components. While bacteria, fungi, and earthworms are known to increase mineral weathering rates, the use of soil organisms in the context of EW remains underexplored. This protocol describes the design and construction of an experimental setup developed to enhance mineral weathering rates through soil organisms while concurrently controlling abiotic conditions. The setup is designed to maximize weathering rates while maintaining soil organisms' activity. It consists of a large number of columns filled with rock powder and organic material, located in a climate chamber and with water applied via a downflow irrigation system. Columns are placed above a fridge containing jerrycans to collect the leachate. Representative results demonstrate that this setup is suitable to ensure the activity of soil organisms and quantify their effect on inorganic carbon sequestration. Challenges remain in minimizing leachate losses, ensuring homogeneous ventilation through the climate chamber, and avoiding flooding of the columns. With this setup, an innovative and promising approach is proposed to enhance mineral weathering rates through the activity of soil biota and disentangle the effect of biotic and abiotic factors as drivers of EW.

Association of earthworm-denitrifier interactions with increased emission of nitrous oxide from soil mesocosms amended with crop residue.

Earthworm activity is known to increase emissions of nitrous oxide (N(2)O) from arable soils. Earthworm gut, casts, and burrows have exhibited higher denitrification activities than the bulk soil, implicating priming of denitrifying organisms as a possible mechanism for this effect. Furthermore, the earthworm feeding strategy may drive N(2)O emissions, as it determines access to fresh organic matter for denitrification. Here, we determined whether interactions between earthworm feeding strategy and the soil denitrifier community can predict N(2)O emissions from the soil. We set up a 90-day mesocosm experiment in which (15)N-labeled maize (Zea mays L.) was either mixed in or applied on top of the soil in the presence or absence of the epigeic earthworm Lumbricus rubellus and/or the endogeic earthworm Aporrectodea caliginosa. We measured N(2)O fluxes and tested the bulk soil for denitrification enzyme activity and the abundance of 16S rRNA and denitrifier genes nirS and nosZ through real-time quantitative PCR. Compared to the control, L. rubellus increased denitrification enzyme activity and N(2)O emissions on days 21 and 90 (day 21, P = 0.034 and P = 0.002, respectively; day 90, P = 0.001 and P = 0.007, respectively), as well as cumulative N(2)O emissions (76%; P = 0.014). A. caliginosa activity led to a transient increase of N(2)O emissions on days 8 to 18 of the experiment. Abundance of nosZ was significantly increased (100%) on day 90 in the treatment mixture containing L. rubellus alone. We conclude that L. rubellus increased cumulative N(2)O emissions by affecting denitrifier community activity via incorporation of fresh residue into the soil and supplying a steady, labile carbon source.

Isotopic analysis of dissolved organic nitrogen in soils.

Determination of the isotopic signature of dissolved organic nitrogen (DON) is important to assess its dynamics in terrestrial ecosystems. Analysis of (15)N-DON, however, has been hindered by the lack of simple, reliable, and established methods. We evaluate three off-line techniques for measuring the (15)N signature of DON in the presence of inorganic N using a persulfate digestion followed by microdiffusion. The (15)N-DON signature is calculated from the difference between total dissolved (15)N ((15)N-TDN) and inorganic (15)N. We quantified the (15)N recovery and signature of DON, NH(4)(+), and NO(3)(-) in a series of inorganic N/DON mixtures (with a TDN concentration of 10 mg N L(-1)) for three lab protocols. Phenylalanine was used as a model compound for DON. The best lab protocol determined the concentration of inorganic N and TDN prior to diffusion using improved spectrophotometric techniques. An accuracy of 88% for (15)N-DON should be routinely possible; coefficient of variation was <2.9%. Hence, reliable (15)N-DON values are obtained over an DON concentration range of 2.3-10 mg L(-1). High levels of DON could influence the accuracy of (15)N-NO(3)(-) mainly at DON:NO(3)(-) ratios above 0.4. Evaluation of alternative NO(3)(-) measurements is still necessary. Our method is applicable for soil solution samples and soil extracts and has no risk of cross-contamination. Potential applications are large, in particular for (15)N tracer studies, and will increase our insight in DON behavior in soils.

Mitigation of greenhouse gas emissions and reduced irrigation water use in rice production through water-saving irrigation scheduling, reduced tillage and fertiliser application strategies.

Rice production systems are the largest anthropogenic wetlands on earth and feed more than half of the world's population. However, they are also a major source of global anthropogenic greenhouse gas (GHG) emissions. Several agronomic strategies have been proposed to improve water-use efficiency and reduce GHG emissions. The aim of this study was to evaluate the impact of water-saving irrigation (alternate wetting and drying (AWD) vs. soil water potential (SWP)), contrasting land establishment (puddling vs. reduced tillage) and fertiliser application methods (broadcast vs. liquid fertilisation) on water-use efficiency, GHG emissions and rice yield. The experiment was laid out in a randomised complete block design with eight treatments (all combinations of the three factors) and four replicates. AWD combined with broadcasting fertilisation was superior to SWP in terms of maintaining yield. However, seasonal nitrous oxide (N2O) emissions were significantly reduced by 64% and 66% in the Broadcast-SWP and Liquid fertiliser-SWP treatments, respectively, compared to corresponding treatments in AWD. The SWP also significantly reduced seasonal methane (CH4) emissions by 34 and 30% in the broadcast and liquid fertilisation treatments, respectively. Area-scaled GWPs were reduced by 48% and 54% in Broadcast-SWP and Liquid fertiliser-SWP treatments respectively compared to the corresponding treatments in AWD. Compared to AWD, the broadcast and liquid fertilisation in SWP irrigation treatments reduced yield-scaled GWPs by 46% and 37%, respectively. In terms of suitability, based on yield-scaled GWPs, the treatments can be ordered as follows: Broadcast-SWP < Broadcast-AWD = Liquid fertiliser-SWP < Liquid fertiliser-AWD. Growing-season water use was 15% lower in the SWP treatments compared with the water-saving AWD. Reduced tillage reduced additional water use during land preparation. The conclusions of this study are that improved water management and timely coordination of N fertiliser with crop demand can reduce water use, N loss via N2O emissions, and CH4 emissions.

Towards optimal use of phosphorus fertiliser.

Because phosphorus (P) is one of the most limiting nutrients in agricultural systems, P fertilisation is essential to feed the world. However, declining P reserves demand far more effective use of this crucial resource. Here, we use meta-analysis to synthesize yield responses to P fertilisation in grasslands, the most common type of agricultural land, to identify under which conditions P fertilisation is most effective. Yield responses to P fertilisation were 40-100% higher in (a) tropical vs temperate regions; (b) grass/legume mixtures vs grass monocultures; and (c) soil pH of 5-6 vs other pHs. The agronomic efficiency of P fertilisation decreased for greater P application rates. Moreover, soils with low P availability reacted disproportionately strong to fertilisation. Hence, low fertiliser application rates to P-deficient soils result in stronger absolute yield benefits than high rates applied to soils with a higher P status. Overall, our results suggest that optimising P fertiliser use is key to sustainable intensification of agricultural systems.

Can flooding-induced greenhouse gas emissions be mitigated by trait-based plant species choice?

Intensively managed grasslands are large sources of the potent greenhouse gas nitrous oxide (N2O) and important regulators of methane (CH4) consumption and production. The predicted increase in flooding frequency and severity due to climate change could increase N2O emissions and shift grasslands from a net CH4 sink to a source. Therefore, effective management strategies are critical for mitigating greenhouse gas emissions from flood-prone grasslands. We tested how repeated flooding affected the N2O and CH4 emissions from 11 different plant communities (Festuca arundinacea, Lolium perenne, Poa trivialis, and Trifolium repens in monoculture, 2- and 4-species mixtures), using intact soil cores from an 18-month old grassland field experiment in a 4-month greenhouse experiment. To elucidate potential underlying mechanisms, we related plant functional traits to cumulative N2O and CH4 emissions. We hypothesized that traits related with fast nitrogen uptake and growth would lower N2O and CH4 emissions in ambient (non-flooded) conditions, and that traits related to tissue toughness would lower N2O and CH4 emissions in flooded conditions. We found that flooding increased cumulative N2O emissions by 97 fold and cumulative CH4 emissions by 1.6 fold on average. Plant community composition mediated the flood-induced increase in N2O emissions. In flooded conditions, increasing abundance of the grass F. arundinacea was related with lower N2O emissions; whereas increases in abundance of the legume T. repens resulted in higher N2O emissions. In non-flooded conditions, N2O emissions were not clearly mediated by plant traits related with nitrogen uptake or biomass production. In flooded conditions, plant communities with high root carbon to nitrogen ratio were related with lower cumulative N2O emissions, and a lower global warming potential (CO2 equivalent of N2O and CH4). We conclude that plant functional traits related to slower decomposition and nitrogen mineralization could play a significant role in mitigating N2O emissions in flooded grasslands.

Dissolved organic nitrogen: an overlooked pathway of nitrogen loss from agricultural systems?

Conventional wisdom postulates that leaching losses of N from agriculture systems are dominated by NO(3)(-). Although the export of dissolved organic nitrogen (DON) into the groundwater has been recognized for more than 100 yr, it is often ignored when total N budgets are constructed. Leaching of DON into stream and drinking water reservoirs leads to eutrophication and acidification, and can pose a potential risk to human health. The main objective of this review was to determine whether DON losses from agricultural systems are significant, and to what extent they pose a risk to human health and the environment. Dissolved organic N losses across agricultural systems varied widely with minimum losses of 0.3 kg DON ha(-1)yr(-1) in a pasture to a maximum loss of 127 kg DON ha(-1)yr(-1) in a grassland following the application of urine. The mean and median values for DON leaching losses were found to be 12.7 and 4.0 kg N ha(-1)yr(-1), respectively. On average, DON losses accounted for 26% of the total soluble N (NO(3)(-) plus DON) losses, with a median value of 19%. With a few exceptions, DON concentrations exceeded the criteria recommendations for drinking water quality. The extent of DON losses increased with increasing precipitation/irrigation, higher total inputs of N, and increasing sand content. It is concluded that DON leaching can be an important N loss pathway from agricultural systems. Models used to simulate and predict N losses from agricultural systems should include DON losses.

The effective mitigation of greenhouse gas emissions from rice paddies without compromising yield by early-season drainage.

Global rice production systems face two opposing challenges: the need to increase production to accommodate the world's growing population while simultaneously reducing greenhouse gas (GHG) emissions. Adaptations to drainage regimes are one of the most promising options for methane mitigation in rice production. Whereas several studies have focused on mid-season drainage (MD) to mitigate GHG emissions, early-season drainage (ED) varying in timing and duration has not been extensively studied. However, such ED periods could potentially be very effective since initial available C levels (and thereby the potential for methanogenesis) can be very high in paddy systems with rice straw incorporation. This study tested the effectiveness of seven drainage regimes varying in their timing and duration (combinations of ED and MD) to mitigate CH4 and N2O emissions in a 101-day growth chamber experiment. Emissions were considerably reduced by early-season drainage compared to both conventional continuous flooding (CF) and the MD drainage regime. The results suggest that ED+MD drainage may have the potential to reduce CH4 emissions and yield-scaled GWP by 85-90% compared to CF and by 75-77% compared to MD only. A combination of (short or long) ED drainage and one MD drainage episode was found to be the most effective in mitigating CH4 emissions without negatively affecting yield. In particular, compared with CF, the long early-season drainage treatments LE+SM and LE+LM significantly (p<0.01) decreased yield-scaled GWP by 85% and 87% respectively. This was associated with carbon being stabilised early in the season, thereby reducing available C for methanogenesis. Overall N2O emissions were small and not significantly affected by ED. It is concluded that ED+MD drainage might be an effective low-tech option for small-scale farmers to reduce GHG emissions and save water while maintaining yield.

Reduced greenhouse gas mitigation potential of no-tillage soils through earthworm activity.

Concerns about rising greenhouse gas (GHG) concentrations have spurred the promotion of no-tillage practices as a means to stimulate carbon storage and reduce CO2 emissions in agro-ecosystems. Recent research has ignited debate about the effect of earthworms on the GHG balance of soil. It is unclear how earthworms interact with soil management practices, making long-term predictions on their effect in agro-ecosystems problematic. Here we show, in a unique two-year experiment, that earthworm presence increases the combined cumulative emissions of CO2 and N2O from a simulated no-tillage (NT) system to the same level as a simulated conventional tillage (CT) system. We found no evidence for increased soil C storage in the presence of earthworms. Because NT agriculture stimulates earthworm presence, our results identify a possible biological pathway for the limited potential of no-tillage soils with respect to GHG mitigation.

Management of irrigation frequency and nitrogen fertilization to mitigate GHG and NO emissions from drip-fertigated crops.

Drip irrigation combined with split application of fertilizer nitrogen (N) dissolved in the irrigation water (i.e. drip fertigation) is commonly considered best management practice for water and nutrient efficiency. As a consequence, its use is becoming widespread. Some of the main factors (water-filled pore space, NH4(+) and NO3(-)) regulating the emissions of greenhouse gases (i.e. N2O, CO2 and CH4) and NO from agroecosystems can easily be manipulated by drip fertigation without yield penalties. In this study, we tested management options to reduce these emissions in a field experiment with a melon (Cucumis melo L.) crop. Treatments included drip irrigation frequency (weekly/daily) and type of N fertilizer (urea/calcium nitrate) applied by fertigation. Crop yield, environmental parameters, soil mineral N concentrations and fluxes of N2O, NO, CH4 and CO2 were measured during 85 days. Fertigation with urea instead of calcium nitrate increased N2O and NO emissions by a factor of 2.4 and 2.9, respectively (P<0.005). Daily irrigation reduced NO emissions by 42% (P<0.005) but increased CO2 emissions by 21% (P<0.05) compared with weekly irrigation. We found no relation between irrigation frequency and N2O emissions. Based on yield-scaled Global Warming Potential as well as NO cumulative emissions, we conclude that weekly fertigation with a NO3(-)-based fertilizer is the best option to combine agronomic productivity with environmental sustainability. Our study shows that adequate management of drip fertigation, while contributing to the attainment of water and food security, may provide an opportunity for climate change mitigation.