Nitrification Control by Plants and Preference for Ammonium versus Nitrate: Positive Feedbacks Increase Productivity but Undermine Resilience.

AbstractSome plants, via their action on microorganisms, control soil nitrification (i.e., the transformation of ammonium into nitrate). We model how the covariation between plant control of nitrification and preference for ammonium versus nitrate impacts ecosystem properties such as productivity, nitrogen (N) losses, and overall resilience. We show that the control of nitrification can maximize productivity by minimizing total inorganic N losses. We initially predicted that plants with an ammonium preference should achieve the highest biomass when inhibiting nitrification, and conversely that plants preferring nitrate should achieve the highest biomass by stimulating nitrification. With a parametrization derived from the Lamto savanna (Ivory Coast), we find that productivity is maximal for plants that slightly prefer ammonium and inhibit nitrification. Such situations, however, lead to strong positive feedbacks that can cause abrupt shifts from a highly to a lowly productive ecosystem. The comparison with other parameter sets (Pawnee short-grass prairie [United States], intensively cultivated field, and a hypothetical parameter set in which ammonium is highly volatilized and nitrate inputs are high) shows that strategies yielding the highest biomass may be counterintuitive (i.e., preferring nitrate but inhibiting nitrification). We argue that the level of control yielding the highest productivity depends on ecosystem properties (quantity of N deposition, leaching rates, and baseline nitrification rates), not only preference. Finally, while contrasting N preferences offer, as expected, the possibility of coexistence through niche partitioning, we stress how control of nitrification can be framed as a niche construction process that adds an additional dimension to coexistence conditions.

Plant-soil synchrony in nutrient cycles: Learning from ecosystems to design sustainable agrosystems.

Redesigning agrosystems to include more ecological regulations can help feed a growing human population, preserve soils for future productivity, limit dependency on synthetic fertilizers, and reduce agriculture contribution to global changes such as eutrophication and warming. However, guidelines for redesigning cropping systems from natural systems to make them more sustainable remain limited. Synthetizing the knowledge on biogeochemical cycles in natural ecosystems, we outline four ecological systems that synchronize the supply of soluble nutrients by soil biota with the fluctuating nutrient demand of plants. This synchrony limits deficiencies and excesses of soluble nutrients, which usually penalize both production and regulating services of agrosystems such as nutrient retention and soil carbon storage. In the ecological systems outlined, synchrony emerges from plant-soil and plant-plant interactions, eco-physiological processes, soil physicochemical processes, and the dynamics of various nutrient reservoirs, including soil organic matter, soil minerals, atmosphere, and a common market. We discuss the relative importance of these ecological systems in regulating nutrient cycles depending on the pedoclimatic context and on the functional diversity of plants and microbes. We offer ideas about how these systems could be stimulated within agrosystems to improve their sustainability. A review of the latest advances in agronomy shows that some of the practices suggested to promote synchrony (e.g., reduced tillage, rotation with perennial plant cover, crop diversification) have already been tested and shown to be effective in reducing nutrient losses, fertilizer use, and N2 O emissions and/or improving biomass production and soil carbon storage. Our framework also highlights new management strategies and defines the conditions for the success of these nature-based practices allowing for site-specific modifications. This new synthetized knowledge should help practitioners to improve the long-term productivity of agrosystems while reducing the negative impact of agriculture on the environment and the climate.

Global distribution of soil fauna functional groups and their estimated litter consumption across biomes.

Soil invertebrates (i.e., soil fauna) are important drivers of many key processes in soils including soil aggregate formation, water retention, and soil organic matter transformation. Many soil fauna groups directly or indirectly participate in litter consumption. However, the quantity of litter consumed by major faunal groups across biomes remains unknown. To estimate this quantity, we reviewed > 1000 observations from 70 studies that determined the biomass of soil fauna across various biomes and 200 observations from 44 studies on litter consumption by soil fauna. To compare litter consumption with annual litterfall, we analyzed 692 observations from 24 litterfall studies and 183 observations from 28 litter stock studies. The biomass of faunal groups was highest in temperate grasslands and then decreased in the following order: boreal forest > temperate forest > tropical grassland > tundra > tropical forest > Mediterranean ecosystems > desert and semidesert. Tropical grasslands, desert biomes, and Mediterranean ecosystems were dominated by termites. Temperate grasslands were dominated by omnivores, while temperate forests were dominated by earthworms. On average, estimated litter consumption (relative to total litter input) ranged from a low of 14.9% in deserts to a high of 100.4% in temperate grassland. Litter consumption by soil fauna was greater in grasslands than in forests. This is the first study to estimate the effect of different soil fauna groups on litter consumption and related processes at global scale.

Short-term impact of fire on the total soil microbial and nitrifier communities in a wet savanna.

Savannas are characterized by the coexistence of grasses and trees. Fires are critical for their coexistence, because they decrease the survival of tree seedlings and saplings and their recruitment to the adult stage. In some humid savannas, perennial grasses inhibit nitrification and trees stimulate nitrification, which likely favors coexistence between trees and grasses. However, fires may influence plant capacity to control nitrogen cycling, which could subsequently influence tree-grass coexistence and savanna nitrogen budget. Therefore, we sampled soil in a humid savanna of Ivory Coast under the dominant nitrification-inhibiting grass species and the dominant nitrification-stimulating tree species and under bare soil before and after (i.e., 5 days) fire during the long dry season. We quantified the total microbial and nitrifier abundances and transcriptional activities and the nitrification enzyme activity. Fire decreased soil water content, probably by increasing evaporation and, maybe, by triggering the growth of grasses, and increased soil ammonium availability likely due to ash deposition and increased mineralization. Fire did not impact the total archaeal, bacterial, or fungal abundances, or that of the nitrifiers. Fire did not impact archaeal transcriptional activity and increased bacterial and fungal total transcriptional activities. In contrast, fire decreased the archaeal nitrifier transcriptional activities and the nitrification enzymatic activity, likely due to the often reported resumption of the growth of nitrification-inhibiting grasses quickly after the fire (and the subsequent increase in root exudation). These results pave the way for a better understanding of the short-term effects of fire on nitrogen cycling and tree-grass competition for nitrogen.

Plant functional trait variability and trait syndromes among wheat varieties: the footprint of artificial selection.

Although widely used in ecology, trait-based approaches are seldom used to study agroecosystems. In particular, there is a need to evaluate how functional trait variability among varieties of a crop species compares to the variability among wild plant species and how variety selection can modify trait syndromes. Here, we quantified 18 above- and below-ground functional traits for 57 varieties of common wheat representative of different modern selection histories. We compared trait variability among varieties and among Pooideae species, and analyzed the effect of selection histories on trait values and trait syndromes. For traits under strong selection, trait variability among varieties was less than 10% of the variability observed among Pooideae species. However, for traits not directly selected, such as root N uptake capacity, the variability was up to 75% of the variability among Pooideae species. Ammonium absorption capacity by roots was counter-selected for conventional varieties compared with organic varieties and landraces. Artificial selection also altered some trait syndromes classically reported for Pooideae. Identifying traits that have high or low variability among varieties and characterizing the hidden effects of selection on trait values and syndromes will benefit the selection of varieties to be used especially for lower N input agroecosystems.

KEYLINK: towards a more integrative soil representation for inclusion in ecosystem scale models. I. review and model concept.

The relatively poor simulation of the below-ground processes is a severe drawback for many ecosystem models, especially when predicting responses to climate change and management. For a meaningful estimation of ecosystem production and the cycling of water, energy, nutrients and carbon, the integration of soil processes and the exchanges at the surface is crucial. It is increasingly recognized that soil biota play an important role in soil organic carbon and nutrient cycling, shaping soil structure and hydrological properties through their activity, and in water and nutrient uptake by plants through mycorrhizal processes. In this article, we review the main soil biological actors (microbiota, fauna and roots) and their effects on soil functioning. We review to what extent they have been included in soil models and propose which of them could be included in ecosystem models. We show that the model representation of the soil food web, the impact of soil ecosystem engineers on soil structure and the related effects on hydrology and soil organic matter (SOM) stabilization are key issues in improving ecosystem-scale soil representation in models. Finally, we describe a new core model concept (KEYLINK) that integrates insights from SOM models, structural models and food web models to simulate the living soil at an ecosystem scale.

Soil carbon mineralization in response to nitrogen enrichment in surface and subsurface layers in two land use types.

Atmospheric nitrogen (N) deposition increases N availability in soils, with consequences affecting the decomposition of soil carbon (C). The impacts of increasing N availability on surface soil C dynamics are well studied. However, subsurface soils have been paid less attention although more than 50% soil C stock is present below this depth (below 20 cm). This study was designed to investigate the response of surface (0-20 cm) and subsurface (20-40 cm and 40-60 cm) C dynamics to 0 (0 kg N ha-1), low (70 kg N ha-1) and high (120 kg N ha-1) levels of N enrichment. The soils were sampled from a cropland and a grass lawn and incubated at 25 °C and 60% water holding capacity for 45 days. Results showed that N enrichment significantly decreased soil C mineralization (Rs) in all the three soil layers in the two studied sites (p < 0.05). The mineralization per unit soil organic carbon (SOC) increased with profile depth in both soils, indicating the higher decomposability of soil C down the soil profile. Moreover, high N level exhibited stronger suppression effect on Rs than low N level. Rs was significantly and positively correlated with microbial biomass carbon explaining 80% of variation in Rs. Overall; these results suggest that N enrichment may increase C sequestration both in surface and subsurface layers, by reducing C loss through mineralization.

Urban ecology, stakeholders and the future of ecology.

The world human population is more and more urban and cities have a strong impact on the biosphere. This explains the development of urban ecology. In this context, the goal of our work is fourfold: to describe the diversity of scientific questions in urban ecology, show how these questions are organized, to assess how these questions can be built in close interactions with stakeholders, to better understand the role urban ecology can play within ecological sciences. A workshop with scientists from all relevant fields (from ecology to sociology) and stakeholders was organized by the Foundation for Research on Biodiversity (FRB). Three types of scientific issues were outlined about (1) the biodiversity of organisms living in urban areas, (2) the functioning of urban organisms and ecosystems, (3) interactions between human societies and urban ecological systems. For all types of issues we outlined it was possible to distinguish both fundamental and applied scientific questions. This allowed building a unique research agenda encompassing all possible types of scientific issues in urban ecology. As all types of ecological and evolutionary questions can be asked in urban areas, urban ecology will likely be more and more influential in the development of ecology. Taken together, the future of towns, their biodiversity and the life of city dwellers is at stake. Increasing the space for ecosystems and biodiversity within towns is more and more viewed as crucial for the well-being of town dwellers. Depending on research and the way its results are taken into account, very different towns could emerge. Urban areas can be viewed as a test and a laboratory for the future of the interactions between human and ecological systems.

Influence of the residence time of street trees and their soils on trace element contamination in Paris (France).

With the actual increasing interest for urban soils, the evaluation of soil contamination by trace elements and the dynamics of this contamination appear mandatory to preserve plant and thereby human health. Street trees and the associated soil placed in pits located nearby roads could represent convenient indicators of urban and vehicle traffic influences on soils and plants. However, data on these soils remain scarce, many studies investigating park soils rather than street tree soils. Furthermore, trace elements could be one of the main factors causing the observed urban tree decline, while practitioners more and more question the possible reuse of these soils after the death of trees as well as tree litter collected in the streets. We evaluated the contamination in anthropogenic trace elements (TE), namely Zn, Pb, and Cd, of street trees (Tilia tomentosa) and their soils distributed all over Paris (France). Street tree soils are imported from rural areas at the plantation of each new tree so that tree age corresponds to the time of residence of the soil within an urban environment allowing the evaluation of temporal trends on TE concentration in soils and trees. The TE concentration revealed an important soil pollution, especially for the older soils (mean age of 80 years old). The consideration of the residence time of trees and soils in an urban environment evidenced an accumulation of Zn and Pb (ca. 4.5 mg kg-1 year-1 and 4 mg kg-1 year-1 for Zn and Pb, respectively). However, leaf concentrations in TE were low and indicate that soil-root transfer was not significant compared to the contamination by atmospheric deposition. These results underlined the necessity to deepen the evaluation of the recycling of urban soils or plants submitted to urban contamination.

Genotypic variability enhances the reproducibility of an ecological study.

Many scientific disciplines are currently experiencing a 'reproducibility crisis' because numerous scientific findings cannot be repeated consistently. A novel but controversial hypothesis postulates that stringent levels of environmental and biotic standardization in experimental studies reduce reproducibility by amplifying the impacts of laboratory-specific environmental factors not accounted for in study designs. A corollary to this hypothesis is that a deliberate introduction of controlled systematic variability (CSV) in experimental designs may lead to increased reproducibility. To test this hypothesis, we had 14 European laboratories run a simple microcosm experiment using grass (Brachypodium distachyon L.) monocultures and grass and legume (Medicago truncatula Gaertn.) mixtures. Each laboratory introduced environmental and genotypic CSV within and among replicated microcosms established in either growth chambers (with stringent control of environmental conditions) or glasshouses (with more variable environmental conditions). The introduction of genotypic CSV led to 18% lower among-laboratory variability in growth chambers, indicating increased reproducibility, but had no significant effect in glasshouses where reproducibility was generally lower. Environmental CSV had little effect on reproducibility. Although there are multiple causes for the 'reproducibility crisis', deliberately including genetic variability may be a simple solution for increasing the reproducibility of ecological studies performed under stringently controlled environmental conditions.

Trace element concentrations along a gradient of urban pressure in forest and lawn soils of the Paris region (France).

The concentration, degree of contamination and pollution of 7 trace elements (TEs) along an urban pressure gradient were measured in 180 lawn and wood soils of the Paris region (France). Iron (Fe), a major element, was used as reference element. Copper (Cu), cadmium (Cd), lead (Pb) and zinc (Zn) were of anthropogenic origin, while arsenic (As), chromium (Cr) and nickel (Ni) were of natural origin. Road traffic was identified as the main source of anthropogenic TEs. In addition, the industrial activity of the Paris region, especially cement plants, was identified as secondary source of Cd. Soil characteristics (such as texture, organic carbon (OC) and total nitrogen (tot N) contents) tell the story of the soil origins and legacies along the urban pressure gradient and often can explain TE concentrations. The history of the land-use types was identified as a factor that allowed understanding the contamination and pollution by TEs. Urban wood soils were found to be more contaminated and polluted than urban lawns, probably because woods are much older than lawns and because of the legacy of the historical management of soils in the Paris region (Haussmann period). Lawn soils are similar to the fertile agricultural soils and relatively recently (mostly from the 1950s onwards) imported from the surrounding of Paris, so that they may be less influenced by urban conditions in terms of TE concentrations. Urban wood soils are heavily polluted by Cd, posing a high risk to the biological communities. The concentration of anthropogenic TEs increased from the rural to the urban areas, and the concentrations of most anthropogenic TEs in urban areas were equivalent to or above the regulatory reference values, raising the question of longer-term monitoring.

Multifunctionality is affected by interactions between green roof plant species, substrate depth, and substrate type.

Green roofs provide ecosystem services through evapotranspiration and nutrient cycling that depend, among others, on plant species, substrate type, and substrate depth. However, no study has assessed thoroughly how interactions between these factors alter ecosystem functions and multifunctionality of green roofs. We simulated some green roof conditions in a pot experiment. We planted 20 plant species from 10 genera and five families (Asteraceae, Caryophyllaceae, Crassulaceae, Fabaceae, and Poaceae) on two substrate types (natural vs. artificial) and two substrate depths (10 cm vs. 30 cm). As indicators of major ecosystem functions, we measured aboveground and belowground biomasses, foliar nitrogen and carbon content, foliar transpiration, substrate water retention, and dissolved organic carbon and nitrates in leachates. Interactions between substrate type and depth strongly affected ecosystem functions. Biomass production was increased in the artificial substrate and deeper substrates, as was water retention in most cases. In contrast, dissolved organic carbon leaching was higher in the artificial substrates. Except for the Fabaceae species, nitrate leaching was reduced in deep, natural soils. The highest transpiration rates were associated with natural soils. All functions were modulated by plant families or species. Plant effects differed according to the observed function and the type and depth of the substrate. Fabaceae species grown on natural soils had the most noticeable patterns, allowing high biomass production and high water retention but also high nitrate leaching from deep pots. No single combination of factors enhanced simultaneously all studied ecosystem functions, highlighting that soil-plant interactions induce trade-offs between ecosystem functions. Substrate type and depth interactions are major drivers for green roof multifunctionality.

Impact of temperature shifts on the joint evolution of seed dormancy and size.

Seed dormancy and size are two important life-history traits that interplay as adaptation to varying environmental settings. As evolution of both traits involves correlated selective pressures, it is of interest to comparatively investigate the evolution of the two traits jointly as well as independently. We explore evolutionary trajectories of seed dormancy and size using adaptive dynamics in scenarios of deterministic or stochastic temperature variations. Ecological dynamics usually result in unbalanced population structures, and temperature shifts or fluctuations of high magnitude give rise to more balanced ecological structures. When only seed dormancy evolves, it is counter-selected and temperature shifts hasten this evolution. Evolution of seed size results in the fixation of a given strategy and evolved seed size decreases when seed dormancy is lowered. When coevolution is allowed, evolutionary variations are reduced while the speed of evolution becomes faster given temperature shifts. Such coevolution scenarios systematically result in reduced seed dormancy and size and similar unbalanced population structures. We discuss how this may be linked to the system stability. Dormancy is counter-selected because population dynamics lead to stable equilibrium, while small seeds are selected as the outcome of size-number trade-offs. Our results suggest that unlike random temperature variation between generations, temperature shifts with high magnitude can considerably alter population structures and accelerate life-history evolution. This study increases our understanding of plant evolution and persistence in the context of climate changes.

Priming effect and microbial diversity in ecosystem functioning and response to global change: a modeling approach using the SYMPHONY model.

Integration of the priming effect (PE) in ecosystem models is crucial to better predict the consequences of global change on ecosystem carbon (C) dynamics and its feedbacks on climate. Over the last decade, many attempts have been made to model PE in soil. However, PE has not yet been incorporated into any ecosystem models. Here, we build plant/soil models to explore how PE and microbial diversity influence soil/plant interactions and ecosystem C and nitrogen (N) dynamics in response to global change (elevated CO2 and atmospheric N depositions). Our results show that plant persistence, soil organic matter (SOM) accumulation, and low N leaching in undisturbed ecosystems relies on a fine adjustment of microbial N mineralization to plant N uptake. This adjustment can be modeled in the SYMPHONY model by considering the destruction of SOM through PE, and the interactions between two microbial functional groups: SOM decomposers and SOM builders. After estimation of parameters, SYMPHONY provided realistic predictions on forage production, soil C storage and N leaching for a permanent grassland. Consistent with recent observations, SYMPHONY predicted a CO2 -induced modification of soil microbial communities leading to an intensification of SOM mineralization and a decrease in the soil C stock. SYMPHONY also indicated that atmospheric N deposition may promote SOM accumulation via changes in the structure and metabolic activities of microbial communities. Collectively, these results suggest that the PE and functional role of microbial diversity may be incorporated in ecosystem models with a few additional parameters, improving accuracy of predictions.

Signal molecules mediate the impact of the earthworm Aporrectodea caliginosa on growth, development and defence of the plant Arabidopsis thaliana.

Earthworms have generally a positive impact on plant growth, which is often attributed to a trophic mechanism: namely, earthworms increase the release of mineral nutrients from soil litter and organic matter. An alternative hypothesis has been proposed since the discovery of a signal molecule (Indole Acetic Acid) in earthworm faeces. In this study, we used methodologies developed in plant science to gain information on ecological mechanisms involved in plant-earthworm interaction, by looking at plant response to earthworm presence at a molecular level. First, we looked at plant overall response to earthworm faeces in an in vitro device where only signal molecules could have an effect on plant growth; we observed that earthworms were inducing positive or negative effects on different plant species. Then, using an Arabidopsis thaliana mutant with an impaired auxin transport, we demonstrated the potential of earthworms to stimulate root growth and to revert the dwarf mutant phenotype. Finally, we performed a comparative transcriptomic analysis of Arabidopsis thaliana in the presence and absence of earthworms; we found that genes modulated in the presence of earthworms are known to respond to biotic and abiotic stresses, or to the application of exogenous hormones. A comparison of our results with other studies found in databases revealed strong analogies with systemic resistance, induced by signal molecules emitted by Plant Growth Promoting Rhizobacteria and/or elicitors emitted by non-virulent pathogens. Signal molecules such as auxin and ethylene, which are considered as major in plant-microorganisms interactions, can also be of prior importance to explain plant-macroinvertebrates interactions. This could imply revisiting ecological theories which generally stress on the role of trophic relationships.

A tale of four stories: soil ecology, theory, evolution and the publication system.

BACKGROUND: Soil ecology has produced a huge corpus of results on relations between soil organisms, ecosystem processes controlled by these organisms and links between belowground and aboveground processes. However, some soil scientists think that soil ecology is short of modelling and evolutionary approaches and has developed too independently from general ecology. We have tested quantitatively these hypotheses through a bibliographic study (about 23000 articles) comparing soil ecology journals, generalist ecology journals, evolutionary ecology journals and theoretical ecology journals. FINDINGS: We have shown that soil ecology is not well represented in generalist ecology journals and that soil ecologists poorly use modelling and evolutionary approaches. Moreover, the articles published by a typical soil ecology journal (Soil Biology and Biochemistry) are cited by and cite low percentages of articles published in generalist ecology journals, evolutionary ecology journals and theoretical ecology journals. CONCLUSION: This confirms our hypotheses and suggests that soil ecology would benefit from an effort towards modelling and evolutionary approaches. This effort should promote the building of a general conceptual framework for soil ecology and bridges between soil ecology and general ecology. We give some historical reasons for the parsimonious use of modelling and evolutionary approaches by soil ecologists. We finally suggest that a publication system that classifies journals according to their Impact Factors and their level of generality is probably inadequate to integrate "particularity" (empirical observations) and "generality" (general theories), which is the goal of all natural sciences. Such a system might also be particularly detrimental to the development of a science such as ecology that is intrinsically multidisciplinary.

Stability of organic carbon in deep soil layers controlled by fresh carbon supply.

The world's soils store more carbon than is present in biomass and in the atmosphere. Little is known, however, about the factors controlling the stability of soil organic carbon stocks and the response of the soil carbon pool to climate change remains uncertain. We investigated the stability of carbon in deep soil layers in one soil profile by combining physical and chemical characterization of organic carbon, soil incubations and radiocarbon dating. Here we show that the supply of fresh plant-derived carbon to the subsoil (0.6-0.8 m depth) stimulated the microbial mineralization of 2,567 +/- 226-year-old carbon. Our results support the previously suggested idea that in the absence of fresh organic carbon, an essential source of energy for soil microbes, the stability of organic carbon in deep soil layers is maintained. We propose that a lack of supply of fresh carbon may prevent the decomposition of the organic carbon pool in deep soil layers in response to future changes in temperature. Any change in land use and agricultural practice that increases the distribution of fresh carbon along the soil profile could however stimulate the loss of ancient buried carbon.

How do sessile dioecious species cope with their males?

In terrestrial plants the segregation of male and female reproductions on different individuals results in the seed-shadow handicap: males do not disperse any seed so that the number of local patches reached by seeds is potentially reduced in dioecious populations in comparison to hermaphrodite populations. An analytical model, incorporating a lottery-based recruitment and dispersal stochasticity, was built. The spatially mediated cost of the seed-shadow handicap has been assessed considering the criterions for the invasion of a resident hermaphrodite species by a dioecious species and the reverse invasion, both species having the same demographic parameters but assuming a likely higher fecundity for dioecious females. The reciprocal invasion of a dioecious and hermaphrodite species differing only by their fecundity is never possible. The seed-shadow handicap disappears when the dispersal or survival rate is high enough. This latter point is due to dispersal stochasticity, which allows for the existence of empty patches. A low fecundity and an aggregated seed distribution increase dispersal stochasticity and increase the positive impact of a low mortality rate on the relative competitivity of dioecy and hermaphroditism. Adding a dispersal cost has a comparable effect but also requires higher dispersal rates for the dioecious invasion.