Temporary (ley) grassland introduced into cropping cycles has been advocated as being beneficial ... more Temporary (ley) grassland introduced into cropping cycles has been advocated as being beneficial for the delivery of ecosystem services by agricultural soils. The management of these temporary grasslands has unknown effects on soil organic matter (SOM) concentrations and biogeochemical properties of the cropland soils following the grassland phase. Here, we investigated the legacy effect of differently managed temporary grasslands, i.e. change of soil properties lasting beyond three years of crop. We assessed soil organic carbon (SOC) quantity and SOM biogeochemical signature (composition of soil neutral carbohydrates and lignin), as well as microbial activities (potential C and N mineralization and denitrification). We used a long-term field experiment on Cambisol with temperate climate in western France, where temporary grassland management practices differed in terms of duration (3 or 6 years) and presence or absence of N fertilisation. Topsoil (10 cm) samples were collected after a 3-yr crop rotation (maize, wheat, barley). Our results showed that N fertilisation during the grassland phase was necessary to maintain soil C and N concentrations beyond three years of crop. Temporary grassland management may affect microbial activities as indicated by contrasting polysaccharide and lignin composition. It had however, no effect on potential CO 2 and N 2 O emissions during laboratory incubations. The biogeochemical signature of SOM was close to continuous grassland only in treatments with 6 yrs of fertilized temporary grassland. We thus, conclude that the legacy effects of a grassland phase on SOC quantity and properties of SOM depend on its management.
African humid savannas are highly productive ecosystems, despite very low soil fertility, where g... more African humid savannas are highly productive ecosystems, despite very low soil fertility, where grasses and trees coexist. Earlier results showed that some perennial grass species are capable of biological nitrification inhibition (BNI) while trees likely influence differently on nitrogen cycling. Here we assessed the impact of the dominant grass and tree species of the Lamto savanna (Ivory Coast) on soil nitrifying and denitrifying enzyme activities (NEA and DEA, respectively) and on the abundances of archaeal and bacterial ammonia oxidizers (AOA and AOB, respectively) and nitrite reducers. This is one of the first studies linking nitrifying and denitrifying activities and the abundances of the involved groups of microorganisms in savanna soils. NEA was 72-times lower under grasses than under trees while AOA and AOB abundances were 34-and 3-times lower. This strongly suggests that all dominant grasses inhibit nitrification while trees stimulate nitrification, and that archaea are probably more involved in nitrification than bacteria in this savanna. While nitrite reducer abundances were similar between locations and dominated by nirS genes, DEA was 9-times lower under grasses than trees, which is likely explained by BNI decreasing nitrate availability under grasses. The nirS dominance could be due to the ferruginous characteristics of these soils as nirS and nirK genes require different metallic co-enzymes (Fe or Cu). Our results show that the coexistence of grasses and trees in this savanna creates a strong heterogeneity in soil nitrogen cycling that must be considered to understand savanna dynamics and functioning. These results will have to be taken into account to predict the feedbacks between climate changes, nitrogen cycling and tree/grass dynamics at a time when savannas face worldwide threats.
This is our ninth annual horizon scan to identify emerging issues that we believe could affect gl... more This is our ninth annual horizon scan to identify emerging issues that we believe could affect global biological diversity, natural capital and ecosystem services, and conservation efforts. Our diverse and international team, with expertise in horizon scanning, science communication, as well as conservation science, practice, and policy, reviewed 117 potential issues. We identified the 15 that may have the greatest positive or negative effects but are not yet well recog- nised by the global conservation community. Themes among these topics include new mechanisms driving the emergence and geographic expansion of diseases, innovative biotechnologies, reassessments of global change, and the development of strategic infrastructure to facilitate global economic priorities.
Although many environments like soils are constantly subjected to invasion by alien microbes, inv... more Although many environments like soils are constantly subjected to invasion by alien microbes, invaders usually fail to succeed, succumbing to the robust diversity often found in nature. So far, only successful invasions have been explored, and it remains unknown to what extent an unsuccessful invasion can impact resident communities. Here we hypothesized that unsuccessful invasions can cause impacts to soil functioning by decreasing the diversity and niche breadth of resident bacterial communities, which could cause shifts to community composition and niche structure-an effect that is likely exacerbated when diversity is compromised. To examine this question, diversity gradients of soil microbial communities were subjected to invasion by the frequent, yet oft-unsuccessful soil invader, Escherichia coli, and evaluated for changes to diversity, bacterial community composition, niche breadth, and niche structure. Contrary to expectations, diversity and niche breadth increased across treatments upon invasion. Community composition and niche structure were also altered, with shifts of niche structure revealing an escape by the resident community away from the invader's resources. Importantly, the extent of the escape varied in response to the community's diversity, where less diverse communities experienced larger shifts. Thus, although transient and unsuccessful, the invader competed for resources with resident species and caused tangible impacts that modified both the diversity and functioning of resident communities, which can likely generate a legacy effect that influences future invasion attempts.
The moist savanna zone covers 0.5 × 10 6 km 2 in West Africa and is characterized by very low soi... more The moist savanna zone covers 0.5 × 10 6 km 2 in West Africa and is characterized by very low soil N levels limiting primary production, but the ecology of nitrifiers in these (agro)ecosystems is largely unknown. We compared the effects of six agricultural practices on nitrifier activity, abundance and diversity at nine sites in central Ivory Coast. Treatments, including repeated fertilization with ammonium and urea, had no effect on nitrification and crop N status after 3 to 5 crop cycles. Nitrification was actually higher at low than medium ammonium level. The nitrifying community was always dominated by ammonia oxidizing archaea and Nitrospira. However, the abundances of ammonia oxidizing bacteria, AOB, and Nitrobacter increased with fertilization after 5 crop cycles. Several AOB populations, some affiliated to Nitrosospira strains with urease activity or adapted to fluctuating ammonium levels, emerged in fertilized plots, which was correlated to nitrifying community ability to benefit from fertilization. In these soils, dominant nitrifiers adapted to very low ammonium levels have to be replaced by high-N nitrifiers before fertilization can stimulate nitrification. Our results show that the delay required for this replacement is much longer than ever observed for other terrestrial ecosystems, i.e. > 5 crop cycles, and demonstrate for the first time that nitrifier characteristics jeopardize the efficiency of fertilization in moist savanna soils. Nitrogen, N, limits primary productivity in many terrestrial ecosystems 1 and its dynamics depends on key microbial activities such as N 2 fixation, mineralisation, nitrification, denitrification and anaerobic ammonium oxidation. Nitrification is particularly important for soil fertility. It consists in the oxidation of ammonia to nitrite by ammonia oxidizing bacteria and archaea (AOB and AOA, respectively) 2, 3 , and the oxidation of nitrite to nitrate by nitrite oxidizing bacteria (NOB) 4, 5. Nitrification plays a key role in determining how much and which forms of soil inorganic N are available for plants, and consequently in driving N losses from ecosystems through nitrate leaching 6 and nitrogen oxide emission 7, 8. Soil N-availability influences the abundance and the composition of nitrifying groups. Indeed, within soil ammonia-oxidizers, AOA and AOB occupy to some extent different ecological niches 9-11. AOA are generally favored by low ammonium levels 12-14 and different studies reported that N addition does not influence or decrease AOA abundance in grassland soils 15-19 (but see refs 20, 21). In contrast, AOB exhibit high activity in environments with high ammonium availability 22, 23. Besides, two major genera of NOB are present in soil, i.e. Nitrobacter and Nitrospira 24, 25 , although NOB are actually more diverse and their ecology is more complex than previously estimated 26. Functional diversity exists within each of the two groups, but Nitrospira are generally assumed to thrive in low N levels, whereas Nitrobacter outcompete Nitrospira under high N levels 27-29. These ecological traits are consistent with the observed responses of soil NOB to environmental changes and agricultural or forestry practices 5, 19, 29, 30. Accordingly, the composition of nitrifying communities can influence the capacity of soil to respond to environmental changes, such as changes in land use or management. For instance, in an experiment mimicking a reversion of grazing regime through urea application and plant clipping in grasslands from central
Maize inoculation by Azospirillum stimulates root growth, along with soil nitrogen (N) uptake and... more Maize inoculation by Azospirillum stimulates root growth, along with soil nitrogen (N) uptake and root carbon (C) exudation, thus increasing N use efficiency. However, inoculation effects on soil N-cycling microbial communities have been overlooked. We hypothesized that inoculation would (i) increase roots-nitrifiers competition for ammonium, and thus decrease nitrifier abundance; and (ii) increase roots-denitrifiers competition for nitrate and C supply to denitrifiers by root exudation, and thus limit or benefit denitrifiers depending on the resource (N or C) mostly limiting these microorganisms. We quantified (de)nitrifiers abundance and activity in the rhizosphere of inoculated and non-inoculated maize on 4 sites over 2 years, and ancillary soil variables. Inoculation effects on nitrification and nitrifiers (AOA, AOB) were not consistent between the three sampling dates. Inoculation influenced denitrifiers abundance (nirK, nirS) differently among sites. In sites with high C limitation for denitrifiers (i.e. limitation of denitrification by C > 66%), inoculation increased nirS-denitrifier abundance (up to 56%) and gross N 2 O production (up to 84%), likely due to increased root C exudation. Conversely, in sites with low C limitation (<47%), inoculation decreased nirS-denitrifier abundance (down to −23%) and gross N 2 O production (down to −18%) likely due to an increased roots-denitrifiers competition for nitrate. The rhizosphere provides a peculiar environment where a huge variety of positive, negative and neutral interactions between roots and microorganisms occur 1. Such interactions can significantly influence plant growth as well as the functioning, the abundance and the diversity of rhizospheric microbial communities 2. Beneficial interactions are known to be established by plant growth-promoting rhizobacteria, PGPRs, with host plants through several mechanisms, including associative N 2 fixation, phosphate solubilization or phytosiderophore production 3, 4. This can result in improved root growth 5, 6 , increased number and length of lateral roots 7 , as well as an increased root and shoot biomass 8, 9 and physiology 10. The better root development induced by inoculation can consequently enhance nutrient 11 and water 12 uptake by plant, stimulate ion transport systems in root 13 and increase the amount of root carbon, C, exudation 14, 15. Azospirillum spp. are well-known PGPRs that are able to colonize the roots of many crop plant species including maize 16, 17. These PGPRs produce phytohormones that can promote root growth and improve nutrient and water absorption by plants 18-21. In particular, inoculation of cereal crops by PGPRs like the well-studied Azospirillum lipoferum CRT1 is often expected to improve crop capacity to retrieve mineral nitrogen, N, from soil. This could pave the way for improving the sustainability of these cropping systems under low N inputs conditions 8. However, inoculated plants could differently affect N dynamics in their rhizosphere, thus influencing the levels and types of mineral N forms available and possibly N losses from soil through leaching of nitrate, NO 3 − , or emission of nitrous oxide, N 2 O, a potent greenhouse gas 22 .
In the past two decades, a large number of studies have investigated the relationship between bio... more In the past two decades, a large number of studies have investigated the relationship between biodiversity and ecosystem functioning, most of which focussed on a limited set of ecosystem variables. The Jena Experiment was set up in 2002 to investigate the effects of plant diversity on element cycling and trophic interactions, using a multi-disciplinary approach. Here, we review the results of 15 years of research in the Jena Experiment, focussing on the effects of manipulating plant species richness and plant functional richness. With more than 85,000 measures taken from the plant diversity plots, the Jena Experiment has allowed answering fundamental questions important for functional biodiversity research. First, the question was how general the effect of plant species richness is, regarding the many different processes that take place in an ecosystem. About 45% of different types of ecosystem processes measured in the ‘main experiment’, where plant species richness ranged from 1 to 60 species, were significantly affected by plant species richness, providing strong support for the view that biodiversity is a significant driver of ecosystem functioning. Many measures were not saturating at the 60-species level, but increased linearly with the logarithm of species richness. There was, however, great variability in the strength of response among different processes. One striking pattern was that many processes, in particular belowground processes, took several years to respond to the manipulation of plant species richness, showing that biodiversity experiments have to be long-term, to distinguish trends from transitory patterns. In addition, the results from the Jena Experiment provide further evidence that diversity begets stability, for example stability against invasion of plant species, but unexpectedly some results also suggested the opposite, e.g. when plant communities experience severe perturbations or elevated resource availability. This highlights the need to revisit diversity–stability theory. Second, we explored whether individual plant species or individual plant functional groups, or biodiversity itself is more important for ecosystem functioning, in particular biomass production. We found strong effects of individual species and plant functional groups on biomass production, yet these effects mostly occurred in addition to, but not instead of, effects of plant species richness. Third, the Jena Experiment assessed the effect of diversity on multitrophic interactions. The diversity of most organisms responded positively to increases in plant species richness, and the effect was stronger for above- than for belowground organisms, and stronger for herbivores than for carnivores or detritivores. Thus, diversity begets diversity. In addition, the effect on organismic diversity was stronger than the effect on species abundances. Fourth, the Jena Experiment aimed to assess the effect of diversity on N, P and C cycling and the water balance of the plots, separating between element input into the ecosystem, element turnover, element stocks, and output from the ecosystem. While inputs were generally less affected by plant species richness, measures of element stocks, turnover and output were often positively affected by plant diversity, e.g. carbon storage strongly increased with increasing plant species richness. Variables of the N cycle responded less strongly to plant species richness than variables of the C cycle. Fifth, plant traits are often used to unravel mechanisms underlying the biodiversity–ecosystem functioning relationship. In the Jena Experiment, most investigated plant traits, both above- and belowground, were plastic and trait expression depended on plant diversity in a complex way, suggesting limitation to using database traits for linking plant traits to particular functions. Sixth, plant diversity effects on ecosystem processes are often caused by plant diversity effects on species interactions. Analyses in the Jena Experiment including structural equation modelling suggest complex interactions that changed with diversity, e.g. soil carbon storage and greenhouse gas emission were affected by changes in the composition and activity of the belowground microbial community. Manipulation experiments, in which particular organisms, e.g. belowground invertebrates, were excluded from plots in split-plot experiments, supported the important role of the biotic component for element and water fluxes. Seventh, the Jena Experiment aimed to put the results into the context of agricultural practices in managed grasslands. The effect of increasing plant species richness from 1 to 16 species on plant biomass was, in absolute terms, as strong as the effect of a more intensive grassland management, using fertiliser and increasing mowing frequency. Potential bioenergy production from high-diversity plots was similar to that of conventionally used energy crops. These results suggest that diverse ‘High Nature Value Grasslands’ are multifunctional and can deliver a range of ecosystem services including production-related services. A final task was to assess the importance of potential artefacts in biodiversity–ecosystem functioning relationships, caused by the weeding of the plant community to maintain plant species composition. While the effort (in hours) needed to weed a plot was often negatively related to plant species richness, species richness still affected the majority of ecosystem variables. Weeding also did not negatively affect monoculture performance; rather, monocultures deteriorated over time for a number of biological reasons, as shown in plant-soil feedback experiments. To summarize, the Jena Experiment has allowed for a comprehensive analysis of the functional role of biodiversity in an ecosystem. A main challenge for future biodiversity research is to increase our mechanistic understanding of why the magnitude of biodiversity effects differs among processes and contexts. It is likely that there will be no simple answer. For example, among the multitude of mechanisms suggested to underlie the positive plant species richness effect on biomass, some have received limited support in the Jena Experiment, such as vertical root niche partitioning. However, others could not be rejected in targeted analyses. Thus, from the current results in the Jena Experiment, it seems likely that the positive biodiversity effect results from several mechanisms acting simultaneously in more diverse communities, such as reduced pathogen attack, the presence of more plant growth promoting organisms, less seed limitation, and increased trait differences leading to complementarity in resource uptake. Distinguishing between different mechanisms requires careful testing of competing hypotheses. Biodiversity research has matured such that predictive approaches testing particular mechanisms are now possible.
The effect of plant diversity on aboveground organisms and processes was largely studied but ther... more The effect of plant diversity on aboveground organisms and processes was largely studied but there is still a lack of knowledge regarding the link between plant diversity and soil characteristics. Here, we analyzed the effect of plant identity and diversity on the diversity of extractible soil organic compounds (ESOC) using 87 experimental grassland plots with different levels of plant diversity and based on a pool of over 50 plant species. Two pools of low molecular weight organic compounds, LMW1 and LMW2, were characterized by GC-MS and HPLC-DAD, respectively. These pools include specific organic acids, fatty acids and phenolics, with more organic acids in LMW1 and more phenolics in LMW2. Plant effect on the diversity of LMW1 and LMW2 compounds was strong and weak, respectively. LMW1 richness observed for bare soil was lower than that observed for all planted soils; and the richness of these soil compounds increased twofold when dominant plant species richness increased from 1 to 6. Comparing the richness of LMW1 compounds observed for a range of plant mixtures and for plant monocultures of species present in these mixtures, we showed that plant species richness increases the richness of these ESOC mainly through complementarity effects among plant species associated with contrasted spectra of soil compounds. This could explain previously reported effects of plant diversity on the diversity of soil heterotrophic microorganisms.
The study of natural ecosystems and experiments using mixtures of plant species demonstrates that... more The study of natural ecosystems and experiments using mixtures of plant species demonstrates that both species and genetic diversity generally promote ecosystem functioning. Therefore, mixing crop varieties is a promising alternative practice to transform modern high-input agriculture that is associated with a drastic reduction of within-field crop genetic diversity and is widely recognized as unsustainable. Here, we review the effects of mixtures of varieties on ecosystem functioning , and their underlying ecological mechanisms, as studied in ecology and agronomy, and outline how this knowledge can help designing more efficient mixtures. We recommend the development of two complementary strategies to optimize variety mixtures by fostering the ecological mechanisms leading to a positive relationship between biodiversity and ecosystem functioning and its stability through time, i.e., sampling and complementarity effects. (1) In the "trait-blind" approach , the design of high-performance mixtures is based on estimations of the mixing abilities of varieties. While this approach is operational because it does not require detailed trait knowledge, it relies on heavy experimental designs to evaluate mixing ability. (2) The trait-based approach is particularly efficient to design mixtures of varieties to provide particular baskets of services but requires building databases of traits for crop varieties and documenting the relations between traits and services. The performance of mixtures requires eventually to be evaluated in real economic, social, and agronomic contexts. We conclude that the need of a multifunctional low-input agriculture strongly increases the attractiveness of mixtures but that new breeding approaches are required to create varieties with higher mixing abilities, to foster complementar-ity and selection effects through an increase in the variance of relevant traits and to explore new combinations of trait values.
Keywords: Denitrification nirK nirS nosZ Soil nitrate Soil organic carbon A B S T R A C T Increas... more Keywords: Denitrification nirK nirS nosZ Soil nitrate Soil organic carbon A B S T R A C T Increasing attention has been paid to microorganisms able to produce nitrous oxide (N 2 O), a potent greenhouse gas, or reduce it to harmless N 2. Based on previous studies, niche differentiation could exist between nirK-and nirS-nitrite reducers and nosZI-and nosZII-N 2 O reducers, and nosZII-bacteria would have a key role for N 2 O reduction in soils. Most previous studies have been performed for agricultural systems but never in the moist savanna zone which covers half a million km 2 in West Africa and whose soils are among the poorest in nitrogen (N) on earth. Here, we quantified potential gross and net N 2 O production rates along with the abundances of nirK-, nirS-, nosZI-and nosZII-harbouring bacteria for soils under six agricultural practices with maize rotations (slash-and-burn, chemical fertilization, mulching with or without inclusion of crop legumes, and without any input) after 4 and 5 crop cycles at nine sites in Ivory Coast. Sites and practices influenced denitrifier abundances and activities, the ratio of total abundances of nitrite-toN 2 O reducers being highest and lowest for the mulching + green soya and slash-and-burn practices, respectively. Using structural equation modelling, we showed that nirS-and nosZI-bacteria both strongly depended on nitrate availability whereas nirK-and nosZII-bacteria were related to soil organic carbon and pH. Furthermore, potential gross and net N 2 O production rates depended strongly and only on the abundances of nirS-and nosZI-bacteria. Our results support the view of a clear niche differentiation between these four microbial groups but invalidate the assumption of a prominent functional role of soil nosZII-N 2 O reducers.
The continuously increasing concentration of atmospheric CO2 has considerably altered ecosystem f... more The continuously increasing concentration of atmospheric CO2 has considerably altered ecosystem functioning. However, few studies have examined the long-term (i.e. over a decade) effect of elevated CO2 on soil microbial communities. Using 16S rRNA gene amplicons and a GeoChip microarray, we investigated soil microbial communities from a Californian annual grassland after 14 years of experimentally elevated CO2 (275 ppm higher than ambient). Both taxonomic and functional gene compositions of the soil microbial community were modified by elevated CO2. There was decrease in relative abundance for taxa with higher ribosomal RNA operon (rrn) copy number under elevated CO2, which is a functional trait that responds positively to resource availability in culture. In contrast, taxa with lower rrn copy number were increased by elevated CO2. As a consequence, the abundance-weighted average rrn copy number of significantly changed OTUs declined from 2.27 at ambient CO2 to 2.01 at elevated CO2. The nitrogen (N) fixation gene nifH and the ammonium-oxidizing gene amoA significantly decreased under elevated CO2 by 12.6% and 6.1%, respectively. Concomitantly, nitrifying enzyme activity decreased by 48.3% under elevated CO2, albeit this change was not significant. There was also a substantial but insignificant decrease in available soil N, with both nitrate (NO3−) (−27.4%) and ammonium (NH4+) (−15.4%) declining. Further, a large number of microbial genes related to carbon (C) degradation were also affected by elevated CO2, whereas those related to C fixation remained largely unchanged. The overall changes in microbial communities and soil N pools induced by long-term elevated CO2 suggest constrained microbial N decomposition, thereby slowing the potential maximum growth rate of the microbial community.
We present the results of our tenth annual horizon scan. We identified 15 emerging priority topic... more We present the results of our tenth annual horizon scan. We identified 15 emerging priority topics that may have major positive or negative effects on the future conservation of global biodiversity, but currently have low awareness within the conservation community. We hope to increase research and policy attention on these areas, improving the capacity of the community to mitigate impacts of potentially negative issues, and maximise the benefits of issues that provide opportunities. Topics include advances in crop breeding, which may affect insects and land use; manipulations of natural water flows and weather systems on the Tibetan Plateau; release of carbon and mercury from melting polar ice and thawing permafrost; new funding schemes and regulations; and land-use changes across Indo-Malaysia. Aims of Horizon Scanning We present the 15 topics identified in our tenth annual horizon scan of emerging issues that are likely to be relevant to global conservation. These are issues that could have significant impacts on society's ability to conserve regional or global biodiversity, but for which the conservation community currently has generally low awareness. These topics were identified by a group of 28 participants, including experts in futures research and horizon scanning, advisors to policy makers, researchers, and practitioners of conservation and other aspects of environmental science. The areas highlighted are highly varied, ranging from major infrastructure projects and new technological developments, to new funding schemes and regulations that are likely to transform food production and land use. We aim to draw the attention of the global conservation community to the potential opportunities and risks associated with these issues. We hope that by raising awareness, we will encourage research, discussion, and allocation of funds, in addition to management and policy change, resulting in improved understanding and greater preparedness. This could facilitate the global conservation community and wider society to respond effectively to the development of these issues. Our work therefore may inform researchers, funding bodies, policy makers, regulatory bodies, conservation organisations, and practitioners. Our approach is supported by the maturing of many issues from previous scans. For example, overexploitation of sand resources was highlighted by Sutherland et al. [1], and subsequent evidence has demonstrated that sand extraction has negative effects on seagrass meadows, nesting terrapins, and migratory waterbirds [2]. In another example, WWF, in partnership with Highlights We present the 15 topics identified in our tenth annual horizon scan for global conservation. Scoring was carried out by a diverse group of experts using a Delphi-like process. Scores were based on the topics' novelty, likelihood, and potential for major impacts on biodiversity. Emerging themes include conservation impacts of biotechnological advances in agriculture. Other issues included climate change-induced release of carbon and mercury from polar ice.
A 15 N labeling and lysimeter experiment was conducted with mesocosms of a semi-arid Leymus chine... more A 15 N labeling and lysimeter experiment was conducted with mesocosms of a semi-arid Leymus chinensis grassland. The aim of the study was to evaluate the effects of N fertilization timing (fertilization in fall or spring) and rate (0, 56, and 112 kg-N ha −1 year −1) on ecosystem services (seed yield and forage yield), ecosystem disservices (N leaching surveyed during 1 year and emissions of NH 3 and N 2 O integrated over 76 days after fertilization), and recovery of added fertilizer N in plants and soil. Seed and forage yields increased more under fall than spring N fertilization. Further, N fertilization was linked to higher soil NH 3 and N 2 O emissions, particularly under high N rate for both NH 3 (2.0 and 1.6 kg-N ha −1 under fall and spring N fertilization, respectively) and N 2 O (0.24 and 0.21 kg-N ha −1 , respectively). N leaching was never observed. A significant N fertilization timing × rate interaction effect was observed on plant recovery efficiency of added fertilizer N (Plant-NRE). Plant-NRE was higher for high than moderate N rate, with + 13.2% (from 22.8 to 36%) and + 16.4% (from 28.2 to 44.7%) for fall and spring fertilization, respectively. Fertilizer N recovered in soil was highest for moderate N rate in fall (68% of total N fertilizer) and lowest for high N rate in spring (46%). Our results show synergies among the ecosystem services (seed and forage yields) and among the disservices (NH 3 and N 2 O emissions), and trade-offs between the services and disservices, some of these synergies and trade-offs being modulated by N fertilization timing and rate. Our study is the first one analyzing the possibly interactive effects of the N fertilization timing and rate on this range of ecosystem services and disservices in semi-arid perennial grasslands, which can be useful for N risk: benefit analysis when evaluating N fertilization strategies.
1. Nitrogen (N) and phosphorus (P) often limit biological processes in terrestrial ecosystems. Ba... more 1. Nitrogen (N) and phosphorus (P) often limit biological processes in terrestrial ecosystems. Based on previous studies mainly focusing on plants, the concept of resource limitation has evolved towards a theory of (co)limitations by multiple resources. However, this ecological framework has not been applied to analyse how soil microorganisms and plants concurrently respond to N and/or P addition, and whether these responses are constrained by phylogenetic relatedness. 2. Here, we applied this framework to analyse microbial and plant responses at community and taxon levels to different fertilization treatments (four N levels without P; four P levels without N and four NP levels) in Tibetan grasslands. 3. Total plant biomass showed serial limitation by N then P, and most plant species were limited by N only. Total archaeal abundance decreased with P addition, but diverse nutrient limitation types were observed for archaeal taxa. Closely related archaeal taxa tended to similarly respond to N, and functional similarity between distant archaeal groups was observed for response to P, possibly due to functional convergence. In contrast, total bacteria slightly increased with P addition only when plants remained N limited, whereas without N limitation, plants rather than bacteria benefited from P addition. Most bacterial taxa were limited by other resources than N and P, and no clear phylogenetic signals were observed regarding bacterial responses to N/P additions. 4. Synthesis. We propose a novel approach for characterizing microbial response types to nutrient addition. It demonstrates that in Tibetan meadows, most dominant plant species, archaea and bacteria, respectively, depend on N, both N and P and other resources.
Seed inoculation by plant growth promoting rhizobacteria (PGPRs) is an agronomic practice that st... more Seed inoculation by plant growth promoting rhizobacteria (PGPRs) is an agronomic practice that stimulates root carbon (C) exudation and nitrogen (N) uptake. Inoculation thus increases and decreases C and N availabilities to denitrifiers in the rhizosphere, respectively. Hence, denitrification rates in the rhizosphere can be positively or negatively influenced by root activity depending on the balance between these two processes. We assumed that inoculation effect on denitrifiers could strongly differ according to soil conditions. Would denitrifiers be mostly limited by C, inoculation would increase denitrifier abundance and activity through increased labile C availability. Would denitrifiers be limited by N rather than C, inoculation would decrease denitrifier abundance and activity through increased competition for N. Here we manipulated denitrification limitation by C and N (i) in a field trial through the use of different fertilization levels, and (ii) in a growth chamber experiment by mimicking root exudate inputs. We analyzed how the effects of maize inoculation by the PGPR Azospirillum lipoferum CRT1 on potential gross and net N 2 O production rates and NO 2 −-and N 2 O-reducer abundances were related to C and N limitation levels. An increase in potential gross (up to +113%) and to a lesser extent net (+37%) N 2 O production was observed for soils where denitrification was highly limited by C. This was explained by strong and moderate increases in the abundances of NO 2 −-and N 2 O-reducers, respectively. In contrast, when deni-trification was weakly limited by C, gross and net N 2 O productions were negatively affected by inoculation (−15 and −40%, respectively). Our results show that the inoculation practice should be evaluated in term of possible increased crop yield but also possible modified N 2 O emission, paying much attention to cropland soils where denitrifiers are highly limited by C.
The three-dimensional (3-D) architecture of a peach tree (Prunus persica L. Batsch) growing in an... more The three-dimensional (3-D) architecture of a peach tree (Prunus persica L. Batsch) growing in an orchard near Avignon, France, was digitized in April 1999 and again four weeks later in May 1999 to quantify increases in leaf area and crown volume as shoots developed. A 3-D model of radiation transfer was used to determine effects of changes in leaf area density and canopy volume on the spatial distribution of absorbed quantum irradiance (PAR a). Effects of changes in PAR a on leaf morphological and physiological properties were determined. Leaf mass per unit area (M a) and leaf nitrogen concentration per unit leaf area (N a) were both nonlinearly related to PAR a , and there was a weak linear relationship between leaf nitrogen concentration per unit leaf mass (N m) and PAR a. Photosynthetic capacity, defined as maximal rates of ribulose-1,5-bisphosphate carboxylase (Rubisco) carboxylation (V cmax) and electron transport (J max), was measured on leaf samples representing sunlit and shaded micro-environments at the same time that the tree crown was digitized. Both V cmax and J max were linearly related to N a during May, but not in April when the range of N a was low. Photosynthetic capacity per unit N a appeared to decline between April and May. Variability in leaf nitrogen partitioning between Rubisco carboxylation and electron transport was small, and the partitioning coefficients were unrelated to N a. Spatial variability in photosynthetic capacity resulted from acclimation to varying PAR a as the crown developed, and acclimation was driven principally by changes in M a rather than the amount or partitioning of leaf nitrogen.
Seedlings of seven temperate tree species (Acer pseudoplatanus L., Betula pendula Roth, Fagus syl... more Seedlings of seven temperate tree species (Acer pseudoplatanus L., Betula pendula Roth, Fagus sylvatica L., Fraxinus excelsior L., Juglans regia L., Quercus petraea Matt. Liebl. and Quercus robur L.) were grown in a nursery under neutral filters transmitting 45% of incident global irradiance. During the second or third year of growth, leaf photosynthetic capacity (i.e., maximal carboxylation rate, V cmax , maximal photosynthetic electron transport rate, J max , and dark respiration, R d) was estimated for five leaves from each species at five or six leaf temperatures (10, 18, 25, 32, 36 and 40 °C). Values of V cmax and J max were obtained by fitting the equations of the Farquhar model on response curves of net CO2 assimilation (A) to sub-stomatal CO2 mole fraction (c i), at high irradiance. Primary parameters describing the kinetic properties of Rubisco (specificity factor, affinity for CO2 and for O2 , and their temperature responses) were taken from published data obtained with spinach and tobacco, and were used for all species. The temperature responses of V cmax and J max , which were fitted to a thermodynamic model, differed. Mean values of V cmax and J max at a reference temperature of 25 °C were 77.3 and 139 µmol m –2 s –1 , respectively. The activation energy was higher for V cmax than for J max (mean values of 73.1 versus 57.9 kJ mol –1) resulting in a decrease in J max /V cmax ratio with increasing temperature. The mean optimal temperature was higher for V cmax than for J max (38.9 versus 35.9 °C). In addition, differences in these temperature responses were observed among species. Temperature optima ranged between 35.9 and above 45 °C for V cmax and between 31.7 and 43.3 °C for J max , but because of data scatter and the limited range of temperatures tested (10 to 40 °C), there were few statistically significant differences among species. The optimal temperature for J max was highest in Q. robur, Q. petraea and J. regia, and lowest in A. pseudo-platanus and F. excelsior. Measurements of chlorophyll a fluorescence revealed that the critical temperature at which basal fluorescence begins to increase was close to 47 °C, with no difference among species. These results should improve the parameterization of photosynthesis models, and be of particular interest when adapted to heterogeneous forests comprising mixtures of species with diverse ecological requirements.
The function and dynamics of savanna ecosystems result from complex interactions and feedbacks be... more The function and dynamics of savanna ecosystems result from complex interactions and feedbacks between grasses and trees, involving numerous processes (i.e. competition for light, water and nutrients, fire, and herbivory). These interactions are characterised by strong relationships between vegetation structure and function. Given the heterogeneous structure of savannas, modelling appears as a convenient approach to study tree – grass interactions. Most current models that describe carbon and water fluxes are not spatially explicit, which restricts their ability to simulate plant interactions at small scales in heterogeneous ecosystems. We present here a new 3D process-based model called TREEGRASS. The model aims at predicting, in heterogeneous tree – grass systems, plant individual radiation, carbon and water fluxes at a local spatial scale. It is run at a daily time-step over periods ranging from one to a few years. The model includes (i) a 3D mechanistic submodel simulating radiation and energy (i.e. transpiration) budgets; (ii) a soil water balance submodel, and (iii) a physiologically based submodel of primary production and leaf area development. The ability of TREEGRASS to predict the seasonal courses of grass dead and leaf mass, soil water content and light regime as observed in the field has been tested for grassy and shrubby areas of Lamto savannas (Ivory Coast). Simulations showed that the spatial distribution of primary production can be strongly affected by the spatial vegetation structure. Potential applications involve predicting net primary production and water balance from the individual to the ecosystem and from the day to the annual vegetation cycle (e.g. effects of tree spatial patterns on carbon and water fluxes at the ecosystem level).
The spatial variations in the stable carbon isotope composition (d 13 C) of air and leaves (total... more The spatial variations in the stable carbon isotope composition (d 13 C) of air and leaves (total matter and soluble sugars) were quantified within the crown of a well-watered, 20-year-old walnut tree growing in a low-density orchard. The observed leaf carbon isotope discrimination (D) was compared with that computed by a three-dimensional model simulating the intracanopy distribution of irradiance, transpiration and photosynthesis (previously parameterized and tested for the same tree canopy) coupled to a biophysically based model of carbon isotope discrimination. The importance of discrimination associated with CO2 gradients encountered from the substomatal sites to the carboxylation sites was evaluated. We also assessed by simulation the effect of current irradiance on leaf gas exchange and the effect of long-term acclimation of photosynthetic capacity and stomatal and internal conductances to light regime on intracanopy gradients in D. The main conclusions of this study are: (i) leaf D can exhibit important variations (5 and 8‰ in total leaf material and soluble sugars, respectively) along light gradients within the foliage of an isolated tree; (ii) internal conductance must be taken into account to adequately predict leaf D , and (iii) the spatial variations in D and water-use efficiency resulted from the short-term response of leaf gas exchange to variations in local irradiance and, to a much lesser extent, from the long-term acclimation of leaf characteristics to the local light regime.
Temporary (ley) grassland introduced into cropping cycles has been advocated as being beneficial ... more Temporary (ley) grassland introduced into cropping cycles has been advocated as being beneficial for the delivery of ecosystem services by agricultural soils. The management of these temporary grasslands has unknown effects on soil organic matter (SOM) concentrations and biogeochemical properties of the cropland soils following the grassland phase. Here, we investigated the legacy effect of differently managed temporary grasslands, i.e. change of soil properties lasting beyond three years of crop. We assessed soil organic carbon (SOC) quantity and SOM biogeochemical signature (composition of soil neutral carbohydrates and lignin), as well as microbial activities (potential C and N mineralization and denitrification). We used a long-term field experiment on Cambisol with temperate climate in western France, where temporary grassland management practices differed in terms of duration (3 or 6 years) and presence or absence of N fertilisation. Topsoil (10 cm) samples were collected after a 3-yr crop rotation (maize, wheat, barley). Our results showed that N fertilisation during the grassland phase was necessary to maintain soil C and N concentrations beyond three years of crop. Temporary grassland management may affect microbial activities as indicated by contrasting polysaccharide and lignin composition. It had however, no effect on potential CO 2 and N 2 O emissions during laboratory incubations. The biogeochemical signature of SOM was close to continuous grassland only in treatments with 6 yrs of fertilized temporary grassland. We thus, conclude that the legacy effects of a grassland phase on SOC quantity and properties of SOM depend on its management.
African humid savannas are highly productive ecosystems, despite very low soil fertility, where g... more African humid savannas are highly productive ecosystems, despite very low soil fertility, where grasses and trees coexist. Earlier results showed that some perennial grass species are capable of biological nitrification inhibition (BNI) while trees likely influence differently on nitrogen cycling. Here we assessed the impact of the dominant grass and tree species of the Lamto savanna (Ivory Coast) on soil nitrifying and denitrifying enzyme activities (NEA and DEA, respectively) and on the abundances of archaeal and bacterial ammonia oxidizers (AOA and AOB, respectively) and nitrite reducers. This is one of the first studies linking nitrifying and denitrifying activities and the abundances of the involved groups of microorganisms in savanna soils. NEA was 72-times lower under grasses than under trees while AOA and AOB abundances were 34-and 3-times lower. This strongly suggests that all dominant grasses inhibit nitrification while trees stimulate nitrification, and that archaea are probably more involved in nitrification than bacteria in this savanna. While nitrite reducer abundances were similar between locations and dominated by nirS genes, DEA was 9-times lower under grasses than trees, which is likely explained by BNI decreasing nitrate availability under grasses. The nirS dominance could be due to the ferruginous characteristics of these soils as nirS and nirK genes require different metallic co-enzymes (Fe or Cu). Our results show that the coexistence of grasses and trees in this savanna creates a strong heterogeneity in soil nitrogen cycling that must be considered to understand savanna dynamics and functioning. These results will have to be taken into account to predict the feedbacks between climate changes, nitrogen cycling and tree/grass dynamics at a time when savannas face worldwide threats.
This is our ninth annual horizon scan to identify emerging issues that we believe could affect gl... more This is our ninth annual horizon scan to identify emerging issues that we believe could affect global biological diversity, natural capital and ecosystem services, and conservation efforts. Our diverse and international team, with expertise in horizon scanning, science communication, as well as conservation science, practice, and policy, reviewed 117 potential issues. We identified the 15 that may have the greatest positive or negative effects but are not yet well recog- nised by the global conservation community. Themes among these topics include new mechanisms driving the emergence and geographic expansion of diseases, innovative biotechnologies, reassessments of global change, and the development of strategic infrastructure to facilitate global economic priorities.
Although many environments like soils are constantly subjected to invasion by alien microbes, inv... more Although many environments like soils are constantly subjected to invasion by alien microbes, invaders usually fail to succeed, succumbing to the robust diversity often found in nature. So far, only successful invasions have been explored, and it remains unknown to what extent an unsuccessful invasion can impact resident communities. Here we hypothesized that unsuccessful invasions can cause impacts to soil functioning by decreasing the diversity and niche breadth of resident bacterial communities, which could cause shifts to community composition and niche structure-an effect that is likely exacerbated when diversity is compromised. To examine this question, diversity gradients of soil microbial communities were subjected to invasion by the frequent, yet oft-unsuccessful soil invader, Escherichia coli, and evaluated for changes to diversity, bacterial community composition, niche breadth, and niche structure. Contrary to expectations, diversity and niche breadth increased across treatments upon invasion. Community composition and niche structure were also altered, with shifts of niche structure revealing an escape by the resident community away from the invader's resources. Importantly, the extent of the escape varied in response to the community's diversity, where less diverse communities experienced larger shifts. Thus, although transient and unsuccessful, the invader competed for resources with resident species and caused tangible impacts that modified both the diversity and functioning of resident communities, which can likely generate a legacy effect that influences future invasion attempts.
The moist savanna zone covers 0.5 × 10 6 km 2 in West Africa and is characterized by very low soi... more The moist savanna zone covers 0.5 × 10 6 km 2 in West Africa and is characterized by very low soil N levels limiting primary production, but the ecology of nitrifiers in these (agro)ecosystems is largely unknown. We compared the effects of six agricultural practices on nitrifier activity, abundance and diversity at nine sites in central Ivory Coast. Treatments, including repeated fertilization with ammonium and urea, had no effect on nitrification and crop N status after 3 to 5 crop cycles. Nitrification was actually higher at low than medium ammonium level. The nitrifying community was always dominated by ammonia oxidizing archaea and Nitrospira. However, the abundances of ammonia oxidizing bacteria, AOB, and Nitrobacter increased with fertilization after 5 crop cycles. Several AOB populations, some affiliated to Nitrosospira strains with urease activity or adapted to fluctuating ammonium levels, emerged in fertilized plots, which was correlated to nitrifying community ability to benefit from fertilization. In these soils, dominant nitrifiers adapted to very low ammonium levels have to be replaced by high-N nitrifiers before fertilization can stimulate nitrification. Our results show that the delay required for this replacement is much longer than ever observed for other terrestrial ecosystems, i.e. > 5 crop cycles, and demonstrate for the first time that nitrifier characteristics jeopardize the efficiency of fertilization in moist savanna soils. Nitrogen, N, limits primary productivity in many terrestrial ecosystems 1 and its dynamics depends on key microbial activities such as N 2 fixation, mineralisation, nitrification, denitrification and anaerobic ammonium oxidation. Nitrification is particularly important for soil fertility. It consists in the oxidation of ammonia to nitrite by ammonia oxidizing bacteria and archaea (AOB and AOA, respectively) 2, 3 , and the oxidation of nitrite to nitrate by nitrite oxidizing bacteria (NOB) 4, 5. Nitrification plays a key role in determining how much and which forms of soil inorganic N are available for plants, and consequently in driving N losses from ecosystems through nitrate leaching 6 and nitrogen oxide emission 7, 8. Soil N-availability influences the abundance and the composition of nitrifying groups. Indeed, within soil ammonia-oxidizers, AOA and AOB occupy to some extent different ecological niches 9-11. AOA are generally favored by low ammonium levels 12-14 and different studies reported that N addition does not influence or decrease AOA abundance in grassland soils 15-19 (but see refs 20, 21). In contrast, AOB exhibit high activity in environments with high ammonium availability 22, 23. Besides, two major genera of NOB are present in soil, i.e. Nitrobacter and Nitrospira 24, 25 , although NOB are actually more diverse and their ecology is more complex than previously estimated 26. Functional diversity exists within each of the two groups, but Nitrospira are generally assumed to thrive in low N levels, whereas Nitrobacter outcompete Nitrospira under high N levels 27-29. These ecological traits are consistent with the observed responses of soil NOB to environmental changes and agricultural or forestry practices 5, 19, 29, 30. Accordingly, the composition of nitrifying communities can influence the capacity of soil to respond to environmental changes, such as changes in land use or management. For instance, in an experiment mimicking a reversion of grazing regime through urea application and plant clipping in grasslands from central
Maize inoculation by Azospirillum stimulates root growth, along with soil nitrogen (N) uptake and... more Maize inoculation by Azospirillum stimulates root growth, along with soil nitrogen (N) uptake and root carbon (C) exudation, thus increasing N use efficiency. However, inoculation effects on soil N-cycling microbial communities have been overlooked. We hypothesized that inoculation would (i) increase roots-nitrifiers competition for ammonium, and thus decrease nitrifier abundance; and (ii) increase roots-denitrifiers competition for nitrate and C supply to denitrifiers by root exudation, and thus limit or benefit denitrifiers depending on the resource (N or C) mostly limiting these microorganisms. We quantified (de)nitrifiers abundance and activity in the rhizosphere of inoculated and non-inoculated maize on 4 sites over 2 years, and ancillary soil variables. Inoculation effects on nitrification and nitrifiers (AOA, AOB) were not consistent between the three sampling dates. Inoculation influenced denitrifiers abundance (nirK, nirS) differently among sites. In sites with high C limitation for denitrifiers (i.e. limitation of denitrification by C > 66%), inoculation increased nirS-denitrifier abundance (up to 56%) and gross N 2 O production (up to 84%), likely due to increased root C exudation. Conversely, in sites with low C limitation (<47%), inoculation decreased nirS-denitrifier abundance (down to −23%) and gross N 2 O production (down to −18%) likely due to an increased roots-denitrifiers competition for nitrate. The rhizosphere provides a peculiar environment where a huge variety of positive, negative and neutral interactions between roots and microorganisms occur 1. Such interactions can significantly influence plant growth as well as the functioning, the abundance and the diversity of rhizospheric microbial communities 2. Beneficial interactions are known to be established by plant growth-promoting rhizobacteria, PGPRs, with host plants through several mechanisms, including associative N 2 fixation, phosphate solubilization or phytosiderophore production 3, 4. This can result in improved root growth 5, 6 , increased number and length of lateral roots 7 , as well as an increased root and shoot biomass 8, 9 and physiology 10. The better root development induced by inoculation can consequently enhance nutrient 11 and water 12 uptake by plant, stimulate ion transport systems in root 13 and increase the amount of root carbon, C, exudation 14, 15. Azospirillum spp. are well-known PGPRs that are able to colonize the roots of many crop plant species including maize 16, 17. These PGPRs produce phytohormones that can promote root growth and improve nutrient and water absorption by plants 18-21. In particular, inoculation of cereal crops by PGPRs like the well-studied Azospirillum lipoferum CRT1 is often expected to improve crop capacity to retrieve mineral nitrogen, N, from soil. This could pave the way for improving the sustainability of these cropping systems under low N inputs conditions 8. However, inoculated plants could differently affect N dynamics in their rhizosphere, thus influencing the levels and types of mineral N forms available and possibly N losses from soil through leaching of nitrate, NO 3 − , or emission of nitrous oxide, N 2 O, a potent greenhouse gas 22 .
In the past two decades, a large number of studies have investigated the relationship between bio... more In the past two decades, a large number of studies have investigated the relationship between biodiversity and ecosystem functioning, most of which focussed on a limited set of ecosystem variables. The Jena Experiment was set up in 2002 to investigate the effects of plant diversity on element cycling and trophic interactions, using a multi-disciplinary approach. Here, we review the results of 15 years of research in the Jena Experiment, focussing on the effects of manipulating plant species richness and plant functional richness. With more than 85,000 measures taken from the plant diversity plots, the Jena Experiment has allowed answering fundamental questions important for functional biodiversity research. First, the question was how general the effect of plant species richness is, regarding the many different processes that take place in an ecosystem. About 45% of different types of ecosystem processes measured in the ‘main experiment’, where plant species richness ranged from 1 to 60 species, were significantly affected by plant species richness, providing strong support for the view that biodiversity is a significant driver of ecosystem functioning. Many measures were not saturating at the 60-species level, but increased linearly with the logarithm of species richness. There was, however, great variability in the strength of response among different processes. One striking pattern was that many processes, in particular belowground processes, took several years to respond to the manipulation of plant species richness, showing that biodiversity experiments have to be long-term, to distinguish trends from transitory patterns. In addition, the results from the Jena Experiment provide further evidence that diversity begets stability, for example stability against invasion of plant species, but unexpectedly some results also suggested the opposite, e.g. when plant communities experience severe perturbations or elevated resource availability. This highlights the need to revisit diversity–stability theory. Second, we explored whether individual plant species or individual plant functional groups, or biodiversity itself is more important for ecosystem functioning, in particular biomass production. We found strong effects of individual species and plant functional groups on biomass production, yet these effects mostly occurred in addition to, but not instead of, effects of plant species richness. Third, the Jena Experiment assessed the effect of diversity on multitrophic interactions. The diversity of most organisms responded positively to increases in plant species richness, and the effect was stronger for above- than for belowground organisms, and stronger for herbivores than for carnivores or detritivores. Thus, diversity begets diversity. In addition, the effect on organismic diversity was stronger than the effect on species abundances. Fourth, the Jena Experiment aimed to assess the effect of diversity on N, P and C cycling and the water balance of the plots, separating between element input into the ecosystem, element turnover, element stocks, and output from the ecosystem. While inputs were generally less affected by plant species richness, measures of element stocks, turnover and output were often positively affected by plant diversity, e.g. carbon storage strongly increased with increasing plant species richness. Variables of the N cycle responded less strongly to plant species richness than variables of the C cycle. Fifth, plant traits are often used to unravel mechanisms underlying the biodiversity–ecosystem functioning relationship. In the Jena Experiment, most investigated plant traits, both above- and belowground, were plastic and trait expression depended on plant diversity in a complex way, suggesting limitation to using database traits for linking plant traits to particular functions. Sixth, plant diversity effects on ecosystem processes are often caused by plant diversity effects on species interactions. Analyses in the Jena Experiment including structural equation modelling suggest complex interactions that changed with diversity, e.g. soil carbon storage and greenhouse gas emission were affected by changes in the composition and activity of the belowground microbial community. Manipulation experiments, in which particular organisms, e.g. belowground invertebrates, were excluded from plots in split-plot experiments, supported the important role of the biotic component for element and water fluxes. Seventh, the Jena Experiment aimed to put the results into the context of agricultural practices in managed grasslands. The effect of increasing plant species richness from 1 to 16 species on plant biomass was, in absolute terms, as strong as the effect of a more intensive grassland management, using fertiliser and increasing mowing frequency. Potential bioenergy production from high-diversity plots was similar to that of conventionally used energy crops. These results suggest that diverse ‘High Nature Value Grasslands’ are multifunctional and can deliver a range of ecosystem services including production-related services. A final task was to assess the importance of potential artefacts in biodiversity–ecosystem functioning relationships, caused by the weeding of the plant community to maintain plant species composition. While the effort (in hours) needed to weed a plot was often negatively related to plant species richness, species richness still affected the majority of ecosystem variables. Weeding also did not negatively affect monoculture performance; rather, monocultures deteriorated over time for a number of biological reasons, as shown in plant-soil feedback experiments. To summarize, the Jena Experiment has allowed for a comprehensive analysis of the functional role of biodiversity in an ecosystem. A main challenge for future biodiversity research is to increase our mechanistic understanding of why the magnitude of biodiversity effects differs among processes and contexts. It is likely that there will be no simple answer. For example, among the multitude of mechanisms suggested to underlie the positive plant species richness effect on biomass, some have received limited support in the Jena Experiment, such as vertical root niche partitioning. However, others could not be rejected in targeted analyses. Thus, from the current results in the Jena Experiment, it seems likely that the positive biodiversity effect results from several mechanisms acting simultaneously in more diverse communities, such as reduced pathogen attack, the presence of more plant growth promoting organisms, less seed limitation, and increased trait differences leading to complementarity in resource uptake. Distinguishing between different mechanisms requires careful testing of competing hypotheses. Biodiversity research has matured such that predictive approaches testing particular mechanisms are now possible.
The effect of plant diversity on aboveground organisms and processes was largely studied but ther... more The effect of plant diversity on aboveground organisms and processes was largely studied but there is still a lack of knowledge regarding the link between plant diversity and soil characteristics. Here, we analyzed the effect of plant identity and diversity on the diversity of extractible soil organic compounds (ESOC) using 87 experimental grassland plots with different levels of plant diversity and based on a pool of over 50 plant species. Two pools of low molecular weight organic compounds, LMW1 and LMW2, were characterized by GC-MS and HPLC-DAD, respectively. These pools include specific organic acids, fatty acids and phenolics, with more organic acids in LMW1 and more phenolics in LMW2. Plant effect on the diversity of LMW1 and LMW2 compounds was strong and weak, respectively. LMW1 richness observed for bare soil was lower than that observed for all planted soils; and the richness of these soil compounds increased twofold when dominant plant species richness increased from 1 to 6. Comparing the richness of LMW1 compounds observed for a range of plant mixtures and for plant monocultures of species present in these mixtures, we showed that plant species richness increases the richness of these ESOC mainly through complementarity effects among plant species associated with contrasted spectra of soil compounds. This could explain previously reported effects of plant diversity on the diversity of soil heterotrophic microorganisms.
The study of natural ecosystems and experiments using mixtures of plant species demonstrates that... more The study of natural ecosystems and experiments using mixtures of plant species demonstrates that both species and genetic diversity generally promote ecosystem functioning. Therefore, mixing crop varieties is a promising alternative practice to transform modern high-input agriculture that is associated with a drastic reduction of within-field crop genetic diversity and is widely recognized as unsustainable. Here, we review the effects of mixtures of varieties on ecosystem functioning , and their underlying ecological mechanisms, as studied in ecology and agronomy, and outline how this knowledge can help designing more efficient mixtures. We recommend the development of two complementary strategies to optimize variety mixtures by fostering the ecological mechanisms leading to a positive relationship between biodiversity and ecosystem functioning and its stability through time, i.e., sampling and complementarity effects. (1) In the "trait-blind" approach , the design of high-performance mixtures is based on estimations of the mixing abilities of varieties. While this approach is operational because it does not require detailed trait knowledge, it relies on heavy experimental designs to evaluate mixing ability. (2) The trait-based approach is particularly efficient to design mixtures of varieties to provide particular baskets of services but requires building databases of traits for crop varieties and documenting the relations between traits and services. The performance of mixtures requires eventually to be evaluated in real economic, social, and agronomic contexts. We conclude that the need of a multifunctional low-input agriculture strongly increases the attractiveness of mixtures but that new breeding approaches are required to create varieties with higher mixing abilities, to foster complementar-ity and selection effects through an increase in the variance of relevant traits and to explore new combinations of trait values.
Keywords: Denitrification nirK nirS nosZ Soil nitrate Soil organic carbon A B S T R A C T Increas... more Keywords: Denitrification nirK nirS nosZ Soil nitrate Soil organic carbon A B S T R A C T Increasing attention has been paid to microorganisms able to produce nitrous oxide (N 2 O), a potent greenhouse gas, or reduce it to harmless N 2. Based on previous studies, niche differentiation could exist between nirK-and nirS-nitrite reducers and nosZI-and nosZII-N 2 O reducers, and nosZII-bacteria would have a key role for N 2 O reduction in soils. Most previous studies have been performed for agricultural systems but never in the moist savanna zone which covers half a million km 2 in West Africa and whose soils are among the poorest in nitrogen (N) on earth. Here, we quantified potential gross and net N 2 O production rates along with the abundances of nirK-, nirS-, nosZI-and nosZII-harbouring bacteria for soils under six agricultural practices with maize rotations (slash-and-burn, chemical fertilization, mulching with or without inclusion of crop legumes, and without any input) after 4 and 5 crop cycles at nine sites in Ivory Coast. Sites and practices influenced denitrifier abundances and activities, the ratio of total abundances of nitrite-toN 2 O reducers being highest and lowest for the mulching + green soya and slash-and-burn practices, respectively. Using structural equation modelling, we showed that nirS-and nosZI-bacteria both strongly depended on nitrate availability whereas nirK-and nosZII-bacteria were related to soil organic carbon and pH. Furthermore, potential gross and net N 2 O production rates depended strongly and only on the abundances of nirS-and nosZI-bacteria. Our results support the view of a clear niche differentiation between these four microbial groups but invalidate the assumption of a prominent functional role of soil nosZII-N 2 O reducers.
The continuously increasing concentration of atmospheric CO2 has considerably altered ecosystem f... more The continuously increasing concentration of atmospheric CO2 has considerably altered ecosystem functioning. However, few studies have examined the long-term (i.e. over a decade) effect of elevated CO2 on soil microbial communities. Using 16S rRNA gene amplicons and a GeoChip microarray, we investigated soil microbial communities from a Californian annual grassland after 14 years of experimentally elevated CO2 (275 ppm higher than ambient). Both taxonomic and functional gene compositions of the soil microbial community were modified by elevated CO2. There was decrease in relative abundance for taxa with higher ribosomal RNA operon (rrn) copy number under elevated CO2, which is a functional trait that responds positively to resource availability in culture. In contrast, taxa with lower rrn copy number were increased by elevated CO2. As a consequence, the abundance-weighted average rrn copy number of significantly changed OTUs declined from 2.27 at ambient CO2 to 2.01 at elevated CO2. The nitrogen (N) fixation gene nifH and the ammonium-oxidizing gene amoA significantly decreased under elevated CO2 by 12.6% and 6.1%, respectively. Concomitantly, nitrifying enzyme activity decreased by 48.3% under elevated CO2, albeit this change was not significant. There was also a substantial but insignificant decrease in available soil N, with both nitrate (NO3−) (−27.4%) and ammonium (NH4+) (−15.4%) declining. Further, a large number of microbial genes related to carbon (C) degradation were also affected by elevated CO2, whereas those related to C fixation remained largely unchanged. The overall changes in microbial communities and soil N pools induced by long-term elevated CO2 suggest constrained microbial N decomposition, thereby slowing the potential maximum growth rate of the microbial community.
We present the results of our tenth annual horizon scan. We identified 15 emerging priority topic... more We present the results of our tenth annual horizon scan. We identified 15 emerging priority topics that may have major positive or negative effects on the future conservation of global biodiversity, but currently have low awareness within the conservation community. We hope to increase research and policy attention on these areas, improving the capacity of the community to mitigate impacts of potentially negative issues, and maximise the benefits of issues that provide opportunities. Topics include advances in crop breeding, which may affect insects and land use; manipulations of natural water flows and weather systems on the Tibetan Plateau; release of carbon and mercury from melting polar ice and thawing permafrost; new funding schemes and regulations; and land-use changes across Indo-Malaysia. Aims of Horizon Scanning We present the 15 topics identified in our tenth annual horizon scan of emerging issues that are likely to be relevant to global conservation. These are issues that could have significant impacts on society's ability to conserve regional or global biodiversity, but for which the conservation community currently has generally low awareness. These topics were identified by a group of 28 participants, including experts in futures research and horizon scanning, advisors to policy makers, researchers, and practitioners of conservation and other aspects of environmental science. The areas highlighted are highly varied, ranging from major infrastructure projects and new technological developments, to new funding schemes and regulations that are likely to transform food production and land use. We aim to draw the attention of the global conservation community to the potential opportunities and risks associated with these issues. We hope that by raising awareness, we will encourage research, discussion, and allocation of funds, in addition to management and policy change, resulting in improved understanding and greater preparedness. This could facilitate the global conservation community and wider society to respond effectively to the development of these issues. Our work therefore may inform researchers, funding bodies, policy makers, regulatory bodies, conservation organisations, and practitioners. Our approach is supported by the maturing of many issues from previous scans. For example, overexploitation of sand resources was highlighted by Sutherland et al. [1], and subsequent evidence has demonstrated that sand extraction has negative effects on seagrass meadows, nesting terrapins, and migratory waterbirds [2]. In another example, WWF, in partnership with Highlights We present the 15 topics identified in our tenth annual horizon scan for global conservation. Scoring was carried out by a diverse group of experts using a Delphi-like process. Scores were based on the topics' novelty, likelihood, and potential for major impacts on biodiversity. Emerging themes include conservation impacts of biotechnological advances in agriculture. Other issues included climate change-induced release of carbon and mercury from polar ice.
A 15 N labeling and lysimeter experiment was conducted with mesocosms of a semi-arid Leymus chine... more A 15 N labeling and lysimeter experiment was conducted with mesocosms of a semi-arid Leymus chinensis grassland. The aim of the study was to evaluate the effects of N fertilization timing (fertilization in fall or spring) and rate (0, 56, and 112 kg-N ha −1 year −1) on ecosystem services (seed yield and forage yield), ecosystem disservices (N leaching surveyed during 1 year and emissions of NH 3 and N 2 O integrated over 76 days after fertilization), and recovery of added fertilizer N in plants and soil. Seed and forage yields increased more under fall than spring N fertilization. Further, N fertilization was linked to higher soil NH 3 and N 2 O emissions, particularly under high N rate for both NH 3 (2.0 and 1.6 kg-N ha −1 under fall and spring N fertilization, respectively) and N 2 O (0.24 and 0.21 kg-N ha −1 , respectively). N leaching was never observed. A significant N fertilization timing × rate interaction effect was observed on plant recovery efficiency of added fertilizer N (Plant-NRE). Plant-NRE was higher for high than moderate N rate, with + 13.2% (from 22.8 to 36%) and + 16.4% (from 28.2 to 44.7%) for fall and spring fertilization, respectively. Fertilizer N recovered in soil was highest for moderate N rate in fall (68% of total N fertilizer) and lowest for high N rate in spring (46%). Our results show synergies among the ecosystem services (seed and forage yields) and among the disservices (NH 3 and N 2 O emissions), and trade-offs between the services and disservices, some of these synergies and trade-offs being modulated by N fertilization timing and rate. Our study is the first one analyzing the possibly interactive effects of the N fertilization timing and rate on this range of ecosystem services and disservices in semi-arid perennial grasslands, which can be useful for N risk: benefit analysis when evaluating N fertilization strategies.
1. Nitrogen (N) and phosphorus (P) often limit biological processes in terrestrial ecosystems. Ba... more 1. Nitrogen (N) and phosphorus (P) often limit biological processes in terrestrial ecosystems. Based on previous studies mainly focusing on plants, the concept of resource limitation has evolved towards a theory of (co)limitations by multiple resources. However, this ecological framework has not been applied to analyse how soil microorganisms and plants concurrently respond to N and/or P addition, and whether these responses are constrained by phylogenetic relatedness. 2. Here, we applied this framework to analyse microbial and plant responses at community and taxon levels to different fertilization treatments (four N levels without P; four P levels without N and four NP levels) in Tibetan grasslands. 3. Total plant biomass showed serial limitation by N then P, and most plant species were limited by N only. Total archaeal abundance decreased with P addition, but diverse nutrient limitation types were observed for archaeal taxa. Closely related archaeal taxa tended to similarly respond to N, and functional similarity between distant archaeal groups was observed for response to P, possibly due to functional convergence. In contrast, total bacteria slightly increased with P addition only when plants remained N limited, whereas without N limitation, plants rather than bacteria benefited from P addition. Most bacterial taxa were limited by other resources than N and P, and no clear phylogenetic signals were observed regarding bacterial responses to N/P additions. 4. Synthesis. We propose a novel approach for characterizing microbial response types to nutrient addition. It demonstrates that in Tibetan meadows, most dominant plant species, archaea and bacteria, respectively, depend on N, both N and P and other resources.
Seed inoculation by plant growth promoting rhizobacteria (PGPRs) is an agronomic practice that st... more Seed inoculation by plant growth promoting rhizobacteria (PGPRs) is an agronomic practice that stimulates root carbon (C) exudation and nitrogen (N) uptake. Inoculation thus increases and decreases C and N availabilities to denitrifiers in the rhizosphere, respectively. Hence, denitrification rates in the rhizosphere can be positively or negatively influenced by root activity depending on the balance between these two processes. We assumed that inoculation effect on denitrifiers could strongly differ according to soil conditions. Would denitrifiers be mostly limited by C, inoculation would increase denitrifier abundance and activity through increased labile C availability. Would denitrifiers be limited by N rather than C, inoculation would decrease denitrifier abundance and activity through increased competition for N. Here we manipulated denitrification limitation by C and N (i) in a field trial through the use of different fertilization levels, and (ii) in a growth chamber experiment by mimicking root exudate inputs. We analyzed how the effects of maize inoculation by the PGPR Azospirillum lipoferum CRT1 on potential gross and net N 2 O production rates and NO 2 −-and N 2 O-reducer abundances were related to C and N limitation levels. An increase in potential gross (up to +113%) and to a lesser extent net (+37%) N 2 O production was observed for soils where denitrification was highly limited by C. This was explained by strong and moderate increases in the abundances of NO 2 −-and N 2 O-reducers, respectively. In contrast, when deni-trification was weakly limited by C, gross and net N 2 O productions were negatively affected by inoculation (−15 and −40%, respectively). Our results show that the inoculation practice should be evaluated in term of possible increased crop yield but also possible modified N 2 O emission, paying much attention to cropland soils where denitrifiers are highly limited by C.
The three-dimensional (3-D) architecture of a peach tree (Prunus persica L. Batsch) growing in an... more The three-dimensional (3-D) architecture of a peach tree (Prunus persica L. Batsch) growing in an orchard near Avignon, France, was digitized in April 1999 and again four weeks later in May 1999 to quantify increases in leaf area and crown volume as shoots developed. A 3-D model of radiation transfer was used to determine effects of changes in leaf area density and canopy volume on the spatial distribution of absorbed quantum irradiance (PAR a). Effects of changes in PAR a on leaf morphological and physiological properties were determined. Leaf mass per unit area (M a) and leaf nitrogen concentration per unit leaf area (N a) were both nonlinearly related to PAR a , and there was a weak linear relationship between leaf nitrogen concentration per unit leaf mass (N m) and PAR a. Photosynthetic capacity, defined as maximal rates of ribulose-1,5-bisphosphate carboxylase (Rubisco) carboxylation (V cmax) and electron transport (J max), was measured on leaf samples representing sunlit and shaded micro-environments at the same time that the tree crown was digitized. Both V cmax and J max were linearly related to N a during May, but not in April when the range of N a was low. Photosynthetic capacity per unit N a appeared to decline between April and May. Variability in leaf nitrogen partitioning between Rubisco carboxylation and electron transport was small, and the partitioning coefficients were unrelated to N a. Spatial variability in photosynthetic capacity resulted from acclimation to varying PAR a as the crown developed, and acclimation was driven principally by changes in M a rather than the amount or partitioning of leaf nitrogen.
Seedlings of seven temperate tree species (Acer pseudoplatanus L., Betula pendula Roth, Fagus syl... more Seedlings of seven temperate tree species (Acer pseudoplatanus L., Betula pendula Roth, Fagus sylvatica L., Fraxinus excelsior L., Juglans regia L., Quercus petraea Matt. Liebl. and Quercus robur L.) were grown in a nursery under neutral filters transmitting 45% of incident global irradiance. During the second or third year of growth, leaf photosynthetic capacity (i.e., maximal carboxylation rate, V cmax , maximal photosynthetic electron transport rate, J max , and dark respiration, R d) was estimated for five leaves from each species at five or six leaf temperatures (10, 18, 25, 32, 36 and 40 °C). Values of V cmax and J max were obtained by fitting the equations of the Farquhar model on response curves of net CO2 assimilation (A) to sub-stomatal CO2 mole fraction (c i), at high irradiance. Primary parameters describing the kinetic properties of Rubisco (specificity factor, affinity for CO2 and for O2 , and their temperature responses) were taken from published data obtained with spinach and tobacco, and were used for all species. The temperature responses of V cmax and J max , which were fitted to a thermodynamic model, differed. Mean values of V cmax and J max at a reference temperature of 25 °C were 77.3 and 139 µmol m –2 s –1 , respectively. The activation energy was higher for V cmax than for J max (mean values of 73.1 versus 57.9 kJ mol –1) resulting in a decrease in J max /V cmax ratio with increasing temperature. The mean optimal temperature was higher for V cmax than for J max (38.9 versus 35.9 °C). In addition, differences in these temperature responses were observed among species. Temperature optima ranged between 35.9 and above 45 °C for V cmax and between 31.7 and 43.3 °C for J max , but because of data scatter and the limited range of temperatures tested (10 to 40 °C), there were few statistically significant differences among species. The optimal temperature for J max was highest in Q. robur, Q. petraea and J. regia, and lowest in A. pseudo-platanus and F. excelsior. Measurements of chlorophyll a fluorescence revealed that the critical temperature at which basal fluorescence begins to increase was close to 47 °C, with no difference among species. These results should improve the parameterization of photosynthesis models, and be of particular interest when adapted to heterogeneous forests comprising mixtures of species with diverse ecological requirements.
The function and dynamics of savanna ecosystems result from complex interactions and feedbacks be... more The function and dynamics of savanna ecosystems result from complex interactions and feedbacks between grasses and trees, involving numerous processes (i.e. competition for light, water and nutrients, fire, and herbivory). These interactions are characterised by strong relationships between vegetation structure and function. Given the heterogeneous structure of savannas, modelling appears as a convenient approach to study tree – grass interactions. Most current models that describe carbon and water fluxes are not spatially explicit, which restricts their ability to simulate plant interactions at small scales in heterogeneous ecosystems. We present here a new 3D process-based model called TREEGRASS. The model aims at predicting, in heterogeneous tree – grass systems, plant individual radiation, carbon and water fluxes at a local spatial scale. It is run at a daily time-step over periods ranging from one to a few years. The model includes (i) a 3D mechanistic submodel simulating radiation and energy (i.e. transpiration) budgets; (ii) a soil water balance submodel, and (iii) a physiologically based submodel of primary production and leaf area development. The ability of TREEGRASS to predict the seasonal courses of grass dead and leaf mass, soil water content and light regime as observed in the field has been tested for grassy and shrubby areas of Lamto savannas (Ivory Coast). Simulations showed that the spatial distribution of primary production can be strongly affected by the spatial vegetation structure. Potential applications involve predicting net primary production and water balance from the individual to the ecosystem and from the day to the annual vegetation cycle (e.g. effects of tree spatial patterns on carbon and water fluxes at the ecosystem level).
The spatial variations in the stable carbon isotope composition (d 13 C) of air and leaves (total... more The spatial variations in the stable carbon isotope composition (d 13 C) of air and leaves (total matter and soluble sugars) were quantified within the crown of a well-watered, 20-year-old walnut tree growing in a low-density orchard. The observed leaf carbon isotope discrimination (D) was compared with that computed by a three-dimensional model simulating the intracanopy distribution of irradiance, transpiration and photosynthesis (previously parameterized and tested for the same tree canopy) coupled to a biophysically based model of carbon isotope discrimination. The importance of discrimination associated with CO2 gradients encountered from the substomatal sites to the carboxylation sites was evaluated. We also assessed by simulation the effect of current irradiance on leaf gas exchange and the effect of long-term acclimation of photosynthetic capacity and stomatal and internal conductances to light regime on intracanopy gradients in D. The main conclusions of this study are: (i) leaf D can exhibit important variations (5 and 8‰ in total leaf material and soluble sugars, respectively) along light gradients within the foliage of an isolated tree; (ii) internal conductance must be taken into account to adequately predict leaf D , and (iii) the spatial variations in D and water-use efficiency resulted from the short-term response of leaf gas exchange to variations in local irradiance and, to a much lesser extent, from the long-term acclimation of leaf characteristics to the local light regime.
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First, the question was how general the effect of plant species richness is, regarding the many different processes that take place in an ecosystem. About 45% of different types of ecosystem processes measured in the ‘main experiment’, where plant species richness ranged from 1 to 60 species, were significantly affected by plant species richness, providing strong support for the view that biodiversity is a significant driver of ecosystem functioning. Many measures were not saturating at the 60-species level, but increased linearly with the logarithm of species richness. There was, however, great variability in the strength of response among different processes. One striking pattern was that many processes, in particular belowground processes, took several years to respond to the manipulation of plant species richness, showing that biodiversity experiments have to be long-term, to distinguish trends from transitory patterns. In addition, the results from the Jena Experiment provide further evidence that diversity begets stability, for example stability against invasion of plant species, but unexpectedly some results also suggested the opposite, e.g. when plant communities experience severe perturbations or elevated resource availability. This highlights the need to revisit diversity–stability theory.
Second, we explored whether individual plant species or individual plant functional groups, or biodiversity itself is more important for ecosystem functioning, in particular biomass production. We found strong effects of individual species and plant functional groups on biomass production, yet these effects mostly occurred in addition to, but not instead of, effects of plant species richness.
Third, the Jena Experiment assessed the effect of diversity on multitrophic interactions. The diversity of most organisms responded positively to increases in plant species richness, and the effect was stronger for above- than for belowground organisms, and stronger for herbivores than for carnivores or detritivores. Thus, diversity begets diversity. In addition, the effect on organismic diversity was stronger than the effect on species abundances.
Fourth, the Jena Experiment aimed to assess the effect of diversity on N, P and C cycling and the water balance of the plots, separating between element input into the ecosystem, element turnover, element stocks, and output from the ecosystem.
While inputs were generally less affected by plant species richness, measures of element stocks, turnover and output were often positively affected by plant diversity, e.g. carbon storage strongly increased with increasing plant species richness. Variables of the N cycle responded less strongly to plant species richness than variables of the C cycle.
Fifth, plant traits are often used to unravel mechanisms underlying the biodiversity–ecosystem functioning relationship. In the Jena Experiment, most investigated plant traits, both above- and belowground, were plastic and trait expression depended on plant diversity in a complex way, suggesting limitation to using database traits for linking plant traits to particular functions.
Sixth, plant diversity effects on ecosystem processes are often caused by plant diversity effects on species interactions. Analyses in the Jena Experiment including structural equation modelling suggest complex interactions that changed with diversity, e.g. soil carbon storage and greenhouse gas emission were affected by changes in the composition and activity of the belowground microbial community. Manipulation experiments, in which particular organisms, e.g. belowground invertebrates, were excluded from plots in split-plot experiments, supported the important role of the biotic component for element and water fluxes.
Seventh, the Jena Experiment aimed to put the results into the context of agricultural practices in managed grasslands. The effect of increasing plant species richness from 1 to 16 species on plant biomass was, in absolute terms, as strong as the effect of a more intensive grassland management, using fertiliser and increasing mowing frequency. Potential bioenergy production from high-diversity plots was similar to that of conventionally used energy crops. These results suggest that diverse ‘High Nature Value Grasslands’ are multifunctional and can deliver a range of ecosystem services including production-related services.
A final task was to assess the importance of potential artefacts in biodiversity–ecosystem functioning relationships, caused by the weeding of the plant community to maintain plant species composition. While the effort (in hours) needed to weed a plot was often negatively related to plant species richness, species richness still affected the majority of ecosystem variables. Weeding also did not negatively affect monoculture performance; rather, monocultures deteriorated over time for a number of biological reasons, as shown in plant-soil feedback experiments.
To summarize, the Jena Experiment has allowed for a comprehensive analysis of the functional role of biodiversity in an ecosystem. A main challenge for future biodiversity research is to increase our mechanistic understanding of why the magnitude of biodiversity effects differs among processes and contexts. It is likely that there will be no simple answer. For example, among the multitude of mechanisms suggested to underlie the positive plant species richness effect on biomass, some have received limited support in the Jena Experiment, such as vertical root niche partitioning. However, others could not be rejected in targeted analyses. Thus, from the current results in the Jena Experiment, it seems likely that the positive biodiversity effect results from several mechanisms acting simultaneously in more diverse communities, such as reduced pathogen attack, the presence of more plant growth promoting organisms, less seed limitation, and increased trait differences leading to complementarity in resource uptake. Distinguishing between different mechanisms requires careful testing of competing hypotheses. Biodiversity research has matured such that predictive approaches testing particular mechanisms are now possible.
2. Here, we applied this framework to analyse microbial and plant responses at community and taxon levels to different fertilization treatments (four N levels without P; four P levels without N and four NP levels) in Tibetan grasslands.
3. Total plant biomass showed serial limitation by N then P, and most plant species were limited by N only. Total archaeal abundance decreased with P addition, but diverse nutrient limitation types were observed for archaeal taxa. Closely related archaeal taxa tended to similarly respond to N, and functional similarity between distant archaeal groups was observed for response to P, possibly due to functional convergence. In contrast, total bacteria slightly increased with P addition only when plants remained N limited, whereas without N limitation, plants rather than bacteria benefited from P addition. Most bacterial taxa were limited by other resources than N and P, and no clear phylogenetic signals were observed regarding bacterial responses to N/P additions.
4. Synthesis. We propose a novel approach for characterizing microbial response types to nutrient addition. It demonstrates that in Tibetan meadows, most dominant plant species, archaea and bacteria, respectively, depend on N, both N and P and other resources.
First, the question was how general the effect of plant species richness is, regarding the many different processes that take place in an ecosystem. About 45% of different types of ecosystem processes measured in the ‘main experiment’, where plant species richness ranged from 1 to 60 species, were significantly affected by plant species richness, providing strong support for the view that biodiversity is a significant driver of ecosystem functioning. Many measures were not saturating at the 60-species level, but increased linearly with the logarithm of species richness. There was, however, great variability in the strength of response among different processes. One striking pattern was that many processes, in particular belowground processes, took several years to respond to the manipulation of plant species richness, showing that biodiversity experiments have to be long-term, to distinguish trends from transitory patterns. In addition, the results from the Jena Experiment provide further evidence that diversity begets stability, for example stability against invasion of plant species, but unexpectedly some results also suggested the opposite, e.g. when plant communities experience severe perturbations or elevated resource availability. This highlights the need to revisit diversity–stability theory.
Second, we explored whether individual plant species or individual plant functional groups, or biodiversity itself is more important for ecosystem functioning, in particular biomass production. We found strong effects of individual species and plant functional groups on biomass production, yet these effects mostly occurred in addition to, but not instead of, effects of plant species richness.
Third, the Jena Experiment assessed the effect of diversity on multitrophic interactions. The diversity of most organisms responded positively to increases in plant species richness, and the effect was stronger for above- than for belowground organisms, and stronger for herbivores than for carnivores or detritivores. Thus, diversity begets diversity. In addition, the effect on organismic diversity was stronger than the effect on species abundances.
Fourth, the Jena Experiment aimed to assess the effect of diversity on N, P and C cycling and the water balance of the plots, separating between element input into the ecosystem, element turnover, element stocks, and output from the ecosystem.
While inputs were generally less affected by plant species richness, measures of element stocks, turnover and output were often positively affected by plant diversity, e.g. carbon storage strongly increased with increasing plant species richness. Variables of the N cycle responded less strongly to plant species richness than variables of the C cycle.
Fifth, plant traits are often used to unravel mechanisms underlying the biodiversity–ecosystem functioning relationship. In the Jena Experiment, most investigated plant traits, both above- and belowground, were plastic and trait expression depended on plant diversity in a complex way, suggesting limitation to using database traits for linking plant traits to particular functions.
Sixth, plant diversity effects on ecosystem processes are often caused by plant diversity effects on species interactions. Analyses in the Jena Experiment including structural equation modelling suggest complex interactions that changed with diversity, e.g. soil carbon storage and greenhouse gas emission were affected by changes in the composition and activity of the belowground microbial community. Manipulation experiments, in which particular organisms, e.g. belowground invertebrates, were excluded from plots in split-plot experiments, supported the important role of the biotic component for element and water fluxes.
Seventh, the Jena Experiment aimed to put the results into the context of agricultural practices in managed grasslands. The effect of increasing plant species richness from 1 to 16 species on plant biomass was, in absolute terms, as strong as the effect of a more intensive grassland management, using fertiliser and increasing mowing frequency. Potential bioenergy production from high-diversity plots was similar to that of conventionally used energy crops. These results suggest that diverse ‘High Nature Value Grasslands’ are multifunctional and can deliver a range of ecosystem services including production-related services.
A final task was to assess the importance of potential artefacts in biodiversity–ecosystem functioning relationships, caused by the weeding of the plant community to maintain plant species composition. While the effort (in hours) needed to weed a plot was often negatively related to plant species richness, species richness still affected the majority of ecosystem variables. Weeding also did not negatively affect monoculture performance; rather, monocultures deteriorated over time for a number of biological reasons, as shown in plant-soil feedback experiments.
To summarize, the Jena Experiment has allowed for a comprehensive analysis of the functional role of biodiversity in an ecosystem. A main challenge for future biodiversity research is to increase our mechanistic understanding of why the magnitude of biodiversity effects differs among processes and contexts. It is likely that there will be no simple answer. For example, among the multitude of mechanisms suggested to underlie the positive plant species richness effect on biomass, some have received limited support in the Jena Experiment, such as vertical root niche partitioning. However, others could not be rejected in targeted analyses. Thus, from the current results in the Jena Experiment, it seems likely that the positive biodiversity effect results from several mechanisms acting simultaneously in more diverse communities, such as reduced pathogen attack, the presence of more plant growth promoting organisms, less seed limitation, and increased trait differences leading to complementarity in resource uptake. Distinguishing between different mechanisms requires careful testing of competing hypotheses. Biodiversity research has matured such that predictive approaches testing particular mechanisms are now possible.
2. Here, we applied this framework to analyse microbial and plant responses at community and taxon levels to different fertilization treatments (four N levels without P; four P levels without N and four NP levels) in Tibetan grasslands.
3. Total plant biomass showed serial limitation by N then P, and most plant species were limited by N only. Total archaeal abundance decreased with P addition, but diverse nutrient limitation types were observed for archaeal taxa. Closely related archaeal taxa tended to similarly respond to N, and functional similarity between distant archaeal groups was observed for response to P, possibly due to functional convergence. In contrast, total bacteria slightly increased with P addition only when plants remained N limited, whereas without N limitation, plants rather than bacteria benefited from P addition. Most bacterial taxa were limited by other resources than N and P, and no clear phylogenetic signals were observed regarding bacterial responses to N/P additions.
4. Synthesis. We propose a novel approach for characterizing microbial response types to nutrient addition. It demonstrates that in Tibetan meadows, most dominant plant species, archaea and bacteria, respectively, depend on N, both N and P and other resources.