Application of modern coexistence theory to rare plant restoration provides early indication of restoration trajectories.

Restoration ecology commonly seeks to re-establish species of interest in degraded habitats. Despite a rich understanding of how succession influences re-establishment, there are several outstanding questions that remain unaddressed: are short-term abundances sufficient to determine long-term re-establishment success, and what factors contribute to unpredictable restorations outcomes? In other words, when restoration fails, is it because the restored habitat is substandard, because of strong competition with invasive species, or alternatively due to changing environmental conditions that would equally impact established populations? Here, we re-purpose tools developed from modern coexistence theory to address these questions, and apply them to an effort to restore the endangered Contra Costa goldfields (Lasthenia conjugens) in constructed ("restored") California vernal pools. Using 16 years of data, we construct a population model of L. conjugens, a species of conservation concern due primarily to habitat loss and invasion of exotic grasses. We show that initial, short-term appearances of restoration success from population abundances is misleading, as year-to-year fluctuations cause long-term population growth rates to fall below zero. The failure of constructed pools is driven by lower maximum growth rates compared with reference ("natural") pools, coupled with a stronger negative sensitivity to annual fluctuations in abiotic conditions that yield decreased maximum growth rates. Nonetheless, our modeling shows that fluctuations in competition (mainly with exotic grasses) benefit L. conjugens through periods of competitive release, especially in constructed pools of intermediate pool depth. We therefore show how reductions in invasives and seed addition in pools of particular depths could change the outcome of restoration for L. conjugens. By applying a largely theoretical framework to the urgent goal of ecological restoration, our study provides a blueprint for predicting restoration success, and identifies future actions to reverse species loss.

Soil chemical legacies trigger species-specific and context-dependent root responses in later arriving plants.

Soil legacies play an important role for the creation of priority effects. However, we still poorly understand to what extent the metabolome found in the soil solution of a plant community is conditioned by its species composition and whether soil chemical legacies affect subsequent species during assembly. To test these hypotheses, we collected soil solutions from forb or grass communities and evaluated how the metabolome of these soil solutions affected the growth, biomass allocation and functional traits of a forb (Dianthus deltoides) and a grass species (Festuca rubra). Results showed that the metabolomes found in the soil solutions of forb and grass communities differed in composition and chemical diversity. While soil chemical legacies did not have any effect on F. rubra, root foraging by D. deltoides decreased when plants received the soil solution from a grass or a forb community. Structural equation modelling showed that reduced soil exploration by D. deltoides arose via either a root growth-dependent pathway (forb metabolome) or a root trait-dependent pathway (grass metabolome). Reduced root foraging was not connected to a decrease in total N uptake. Our findings reveal that soil chemical legacies can create belowground priority effects by affecting root foraging in later arriving plants.

Legacy effects of pre-crop plant functional group on fungal root symbionts of barley.

Arbuscular mycorrhizal (AM) fungi, a group of widespread fungal symbionts of crops, could be important in driving crop yield across crop rotations through plant-soil feedbacks (PSF). However, whether preceding crops have a legacy effect on the AM fungi of the subsequent crop is poorly known. We set up an outdoor mesocosm crop rotation experiment that consisted of a first phase growing either one of four pre-crops establishing AM and/or rhizobial symbiosis or not (spring barley, faba bean, lupine, canola), followed by an AM crop, winter barley. After the pre-crop harvest, carbon-rich organic substrates were applied to test whether it attenuated, accentuated or modified the effect of pre-crops. The pre-crop mycorrhizal status, but not its rhizobial status, affected the richness and composition of AM fungi, and this difference, in particular community composition, persisted and increased in the roots of winter barley. The effect of a pre-crop was driven by its single symbiotic group, not its mixed symbiotic group and/or by a crop-species-specific effect. This demonstrates that the pre-crop symbiotic group has lasting legacy effects on the AM fungal communities and may steer the AM fungal community succession across rotation phases. This effect was accentuated by sawdust amendment, but not wheat straw. Based on the previous observation of decreased crop yield after AM pre-crops, our findings suggest negative PSF at the level of the plant symbiotic group driven by a legacy effect of crop rotation history on AM fungal communities, and that a focus on crop symbiotic group offers additional understanding of PSF.

The exotic species Senecio inaequidens pays the price for arriving late in temperate European grassland communities.

The exotic South African ragwort (Senecio inaequidens DC.) rapidly spread across Central Europe after its introduction, but we still do not know to what extent its timing of arrival in a plant community (i.e. before or after natives) and the composition of the native community being invaded affect (1) its capacity to invade a European grassland, (2) the performance of the native species, and (3) the direction and strength of priority effects. In a greenhouse experiment, we manipulated the timing of arrival of the exotic species (Senecio) and the composition of the native community to test the influence of these factors on the productivity and N content of exotic and native species. We also investigated if the plant species origin (native or exotic) and the native community composition affected the benefit of arriving early and the cost of arriving late in the community. The establishment success of Senecio strongly depended on its timing of arrival in a grassland community. Senecio benefited more from arriving early than did the natives. The presence of legumes in the community did not favour invasion by Senecio. When natives arrived later than Senecio, however, priority effects were weaker when legumes were part of the native community. Our results showed that inhibitory priority effects created by natives can lower the risk of invasion by Senecio. An early arrival of this species at a site with low native species abundance is a scenario that could favour invasion.

Legacy effects of land-use modulate tree growth responses to climate extremes.

Climate change can impact forest ecosystem processes via individual tree and community responses. While the importance of land-use legacies in modulating these processes have been increasingly recognised, evidence of former land-use mediated climate-growth relationships remain rare. We analysed how differences in former land-use (i.e. forest continuity) affect the growth response of European beech to climate extremes. Here, using dendrochronological and fine root data, we show that ancient forests (forests with a long forest continuity) and recent forests (forests afforested on former farmland) clearly differ with regard to climate-growth relationships. We found that sensitivity to climatic extremes was lower for trees growing in ancient forests, as reflected by significantly lower growth reductions during adverse climatic conditions. Fine root morphology also differed significantly between the former land-use types: on average, trees with high specific root length (SRL) and specific root area (SRA) and low root tissue density (RTD) were associated with recent forests, whereas the opposite traits were characteristic of ancient forests. Moreover, we found that trees of ancient forests hold a larger fine root system than trees of recent forests. Our results demonstrate that land-use legacy-mediated modifications in the size and morphology of the fine root system act as a mechanism in regulating drought resistance of beech, emphasising the need to consider the 'ecological memory' of forests when assessing or predicting the sensitivity of forest ecosystems to global environmental change.

Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment.

Biodiversity is rapidly declining, and this may negatively affect ecosystem processes, including economically important ecosystem services. Previous studies have shown that biodiversity has positive effects on organisms and processes across trophic levels. However, only a few studies have so far incorporated an explicit food-web perspective. In an eight-year biodiversity experiment, we studied an unprecedented range of above- and below-ground organisms and multitrophic interactions. A multitrophic data set originating from a single long-term experiment allows mechanistic insights that would not be gained from meta-analysis of different experiments. Here we show that plant diversity effects dampen with increasing trophic level and degree of omnivory. This was true both for abundance and species richness of organisms. Furthermore, we present comprehensive above-ground/below-ground biodiversity food webs. Both above ground and below ground, herbivores responded more strongly to changes in plant diversity than did carnivores or omnivores. Density and richness of carnivorous taxa was independent of vegetation structure. Below-ground responses to plant diversity were consistently weaker than above-ground responses. Responses to increasing plant diversity were generally positive, but were negative for biological invasion, pathogen infestation and hyperparasitism. Our results suggest that plant diversity has strong bottom-up effects on multitrophic interaction networks, with particularly strong effects on lower trophic levels. Effects on higher trophic levels are indirectly mediated through bottom-up trophic cascades.

Two-way NxP fertilisation experiment on barley (Hordeum vulgare) reveals shift from additive to synergistic N-P interactions at critical phosphorus fertilisation level.

In a pot experiment, we investigated synergistic interaction of N and P fertilisation on barley biomass (Hordeum vulgare) on both shoot and root level with the aim to determine whether N-P interaction would be the same for all levels of N and P fertilisation. We further aimed to determine whether there was a critical level of N and/or P fertilisation rate, above which, a decrease in resource allocation to roots (as nutrient availability increased) could be demonstrated. Barley plants were grown from seed on a nutrient poor substrate and subjected to a two-way NxP fertilisation gradient using a modified Hoagland fertilisation solution. We observed N-P interactions in shoot and root biomass, and N and P use-efficiencies. A synergistic response in biomass was observed only above a critical level of P fertilisation when P was not limiting growth. Furthermore, we found that the same incremental increase in N:P ratio of applied fertiliser elicited different responses in shoot and root biomass depending on P treatment and concluded that barley plants were less able to cope with increasing stoichiometric imbalance when P was deficient. We provide, for the first time, stoichiometric evidence that critical levels for synergistic interactions between N-P may exist in crop plants.

The social-ecological ladder of restoration ambition.

Expanding in both scope and scale, ecosystem restoration needs to embrace complex social-ecological dynamics. To help scientists and practitioners navigate ever new demands on restoration, we propose the "social-ecological ladder of restoration ambition" as a conceptual model to approach dynamically shifting social and ecological restoration goals. The model focuses on three dynamic aspects of restoration, namely degrading processes, restoration goals and remedial actions. As these three change through time, new reinforcing and balancing feedback mechanisms characterize the restoration process. We illustrate our model through case studies in which restoration has become increasingly ambitious through time, namely forest landscape restoration in Rwanda and grassland restoration in Germany. The ladder of restoration ambition offers a new way of applying social-ecological systems thinking to ecosystem restoration. Additionally, it raises awareness of social-ecological trade-offs, power imbalances and conflicting goals in restoration projects, thereby laying an important foundation for finding more practicable and fairer solutions.

Root-root interactions: extending our perspective to be more inclusive of the range of theories in ecology and agriculture using in-vivo analyses.

BACKGROUND: There is a large body of literature on competitive interactions among plants, but many studies have only focused on above-ground interactions and little is known about root-root dynamics between interacting plants. The perspective on possible mechanisms that explain the outcome of root-root interactions has recently been extended to include non-resource-driven mechanisms (as well as resource-driven mechanisms) of root competition and positive interactions such as facilitation. These approaches have often suffered from being static, partly due to the lack of appropriate methodologies for in-situ non-destructive root characterization. SCOPE: Recent studies show that interactive effects of plant neighbourhood interactions follow non-linear and non-additive paths that are hard to explain. Common outcomes such as accumulation of roots mainly in the topsoil cannot be explained solely by competition theory but require a more inclusive theoretical, as well as an improved methodological framework. This will include the question of whether we can apply the same conceptual framework to crop versus natural species. CONCLUSIONS: The development of non-invasive methods to dynamically study root-root interactions in vivo will provide the necessary tools to study a more inclusive conceptual framework for root-root interactions. By following the dynamics of root-root interactions through time in a whole range of scenarios and systems, using a wide variety of non-invasive methods, (such as fluorescent protein which now allows us to separately identify the roots of several individuals within soil), we will be much better equipped to answer some of the key questions in root physiology, ecology and agronomy.

A comparison of the strength of biodiversity effects across multiple functions.

In order to predict which ecosystem functions are most at risk from biodiversity loss, meta-analyses have generalised results from biodiversity experiments over different sites and ecosystem types. In contrast, comparing the strength of biodiversity effects across a large number of ecosystem processes measured in a single experiment permits more direct comparisons. Here, we present an analysis of 418 separate measures of 38 ecosystem processes. Overall, 45 % of processes were significantly affected by plant species richness, suggesting that, while diversity affects a large number of processes not all respond to biodiversity. We therefore compared the strength of plant diversity effects between different categories of ecosystem processes, grouping processes according to the year of measurement, their biogeochemical cycle, trophic level and compartment (above- or belowground) and according to whether they were measures of biodiversity or other ecosystem processes, biotic or abiotic and static or dynamic. Overall, and for several individual processes, we found that biodiversity effects became stronger over time. Measures of the carbon cycle were also affected more strongly by plant species richness than were the measures associated with the nitrogen cycle. Further, we found greater plant species richness effects on measures of biodiversity than on other processes. The differential effects of plant diversity on the various types of ecosystem processes indicate that future research and political effort should shift from a general debate about whether biodiversity loss impairs ecosystem functions to focussing on the specific functions of interest and ways to preserve them individually or in combination.

Biodiversity-stability relationships strengthen over time in a long-term grassland experiment.

Numerous studies have demonstrated that biodiversity drives ecosystem functioning, yet how biodiversity loss alters ecosystems functioning and stability in the long-term lacks experimental evidence. We report temporal effects of species richness on community productivity, stability, species asynchrony, and complementarity, and how the relationships among them change over 17 years in a grassland biodiversity experiment. Productivity declined more rapidly in less diverse communities resulting in temporally strengthening positive effects of richness on productivity, complementarity, and stability. In later years asynchrony played a more important role in increasing community stability as the negative effect of richness on population stability diminished. Only during later years did species complementarity relate to species asynchrony. These results show that species complementarity and asynchrony can take more than a decade to develop strong stabilizing effects on ecosystem functioning in diverse plant communities. Thus, the mechanisms stabilizing ecosystem functioning change with community age.

Making the UN Decade on Ecosystem Restoration a Social-Ecological Endeavour.

The United Nations (UN) recently declared 2021 to 2030 the Decade on Ecosystem Restoration. Against this background, we review recent social-ecological systems research and summarize key themes that could help to improve ecosystem restoration in dynamic social contexts. The themes relate to resilience and adaptability, ecosystem stewardship and navigation of change, relational values, the coevolution of human and ecological systems, long-range social-ecological connections, and leverage points for transformation. We recommend two cross-cutting new research foci; namely: (i) post hoc cross-sectional assessments of social-ecological restoration projects; and (ii) transdisciplinary social-ecological 'living labs' that accompany new restoration projects as they unfold. With global agendas increasingly taking a social-ecological perspective, the recasting of ecosystem restoration as a social-ecological endeavor offers exciting new opportunities for both research and practice.

Timing matters: Distinct effects of nitrogen and phosphorus fertilizer application timing on root system architecture responses.

Aims: Although different plant foraging responses to the two macronutrients nitrogen (N) and phosphorus (P) are well researched, the effect of timing of fertilizer application on root system architecture (RSA) remains largely unknown. We, therefore, aimed to understand how RSA of Hordeum vulgare L. responds to timing of N and P application. Methods: Plants were grown in rhizoboxes for 38 days in nutrient-poor soil and watered with nutrient solution, lacking either N or P, with the absent nutrient applied once either 2/3/4 weeks after sowing. Positive controls were continuously receiving N and P and a negative control receiving both N and P only after 3 weeks. We tracked root growth over time, measured plant biomass and nutrient uptake. Results: Late N application strongly reduced total root biomass and visible root length compared with continuous NP and late P application. Root mass fractions (total root biomass/total plant biomass) remained similar over all treatments, but relative allocation (% of total root biomass) was higher in lower depth with late N application. Shoot P concentrations remained relatively stable, but the plants receiving P later had higher N concentrations. Conclusions: Late N application had overall more negative effects on early plant growth compared with late P. We propose that future studies under field conditions should try to disentangle the effect of timing from the nutrient availability on RSA responses and hence ultimately plant performance.

Combined MRI-PET dissects dynamic changes in plant structures and functions.

Unravelling the factors determining the allocation of carbon to various plant organs is one of the great challenges of modern plant biology. Studying allocation under close to natural conditions requires non-invasive methods, which are now becoming available for measuring plants on a par with those developed for humans. By combining magnetic resonance imaging (MRI) and positron emission tomography (PET), we investigated three contrasting root/shoot systems growing in sand or soil, with respect to their structures, transport routes and the translocation dynamics of recently fixed photoassimilates labelled with the short-lived radioactive carbon isotope (11)C. Storage organs of sugar beet (Beta vulgaris) and radish plants (Raphanus sativus) were assessed using MRI, providing images of the internal structures of the organs with high spatial resolution, and while species-specific transport sectoralities, properties of assimilate allocation and unloading characteristics were measured using PET. Growth and carbon allocation within complex root systems were monitored in maize plants (Zea mays), and the results may be used to identify factors affecting root growth in natural substrates or in competition with roots of other plants. MRI-PET co-registration opens the door for non-invasive analysis of plant structures and transport processes that may change in response to genomic, developmental or environmental challenges. It is our aim to make the methods applicable for quantitative analyses of plant traits in phenotyping as well as in understanding the dynamics of key processes that are essential to plant performance.

Plant traits alone are poor predictors of ecosystem properties and long-term ecosystem functioning.

Earth is home to over 350,000 vascular plant species that differ in their traits in innumerable ways. A key challenge is to predict how natural or anthropogenically driven changes in the identity, abundance and diversity of co-occurring plant species drive important ecosystem-level properties such as biomass production or carbon storage. Here, we analyse the extent to which 42 different ecosystem properties can be predicted by 41 plant traits in 78 experimentally manipulated grassland plots over 10 years. Despite the unprecedented number of traits analysed, the average percentage of variation in ecosystem properties jointly explained was only moderate (32.6%) within individual years, and even much lower (12.7%) across years. Most other studies linking ecosystem properties to plant traits analysed no more than six traits and, when including only six traits in our analysis, the average percentage of variation explained in across-year levels of ecosystem properties dropped to 4.8%. Furthermore, we found on average only 12.2% overlap in significant predictors among ecosystem properties, indicating that a small set of key traits able to explain multiple ecosystem properties does not exist. Our results therefore suggest that there are specific limits to the extent to which traits per se can predict the long-term functional consequences of biodiversity change, so that data on additional drivers, such as interacting abiotic factors, may be required to improve predictions of ecosystem property levels.

Plant species richness and functional composition drive overyielding in a six-year grassland experiment.

Plant diversity has been shown to increase community biomass in experimental communities, but the mechanisms resulting in such positive biodiversity effects have remained largely unknown. We used a large-scale six-year biodiversity experiment near Jena, Germany, to examine how aboveground community biomass in grasslands is affected by different components of plant diversity and thereby infer the mechanisms that may underlie positive biodiversity effects. As components of diversity we defined the number of species (1-16), number of functional groups (1-4), presence of functional groups (legumes, tall herbs, small herbs, and grasses) and proportional abundance of functional groups. Using linear models, replacement series on the level of functional groups, and additive partitioning on the level of species, we explored whether the observed biodiversity effects originated from disproportionate effects of single functional groups or species or from positive interactions between them. Aboveground community biomass was positively related to the number of species measured across functional groups as well as to the number of functional groups measured across different levels of species richness. Furthermore, increasing the number of species within functional groups increased aboveground community biomass, indicating that species within functional groups were not redundant with respect to biomass production. A positive relationship between the number of functional groups and aboveground community biomass within a particular level of species richness suggested that complementarity was larger between species belonging to different rather than to the same functional groups. The presence of legumes or tall herbs had a strong positive impact on aboveground community biomass whereas the presence of small herbs or grasses had on average no significant effect. Two- and three-way interactions between functional group presences were weak, suggesting that their main effects were largely additive. Replacement series analyses on the level of functional groups revealed strong transgressive overyielding and relative yields >1, indicating facilitation. On the species level, we found strong complementarity effects that increased over time while selection effects due to disproportionate contributions of particular species decreased over time. We conclude that transgressive overyielding between functional groups and species richness effects within functional groups caused the positive biodiversity effects on aboveground community biomass in our experiment.

Aboveground overyielding in grassland mixtures is associated with reduced biomass partitioning to belowground organs.

We investigated effects of plant species richness in experimental grassland plots on annual above- and belowground biomass production estimated from repeated harvests and ingrowth cores, respectively. Aboveground and total biomass production increased with increasing plant species richness while belowground production remained constant. Root to shoot biomass production ratios (R/S) in mixtures were lower than expected from monoculture performance of the species present in the mixtures, showing that interactions among species led to reduced biomass partitioning to belowground organs. This change in partitioning to belowground organs was not confined to mixtures with legumes, but also measured in mixtures without legumes, and correlated with aboveground overyielding in mixtures. It is suggested that species-rich communities invest less in belowground biomass than do monocultures to extract soil resources, thus leading to increased investment into aboveground organs and overyielding.

Tomato plants rather than fertilizers drive microbial community structure in horticultural growing media.

Synthetic fertilizer production is associated with a high environmental footprint, as compounds typically dissolve rapidly leaching emissions to the atmosphere or surface waters. We tested two recovered nutrients with slower release patterns, as promising alternatives for synthetic fertilizers: struvite and a commercially available organic fertilizer. Using these fertilizers as nitrogen source, we conducted a rhizotron experiment to test their effect on plant performance and nutrient recovery in juvenile tomato plants. Plant performance was significantly improved when organic fertilizer was provided, promoting higher shoot biomass. Since the microbial community influences plant nitrogen availability, we characterized the root-associated microbial community structure and functionality. Analyses revealed distinct root microbial community structure when different fertilizers were supplied. However, plant presence significantly increased the similarity of the microbial community over time, regardless of fertilization. Additionally, the presence of the plant significantly reduced the potential ammonia oxidation rates, implying a possible role of the rhizosheath microbiome or nitrification inhibition by the plant. Our results indicate that nitrifying community members are impacted by the type of fertilizer used, while tomato plants influenced the potential ammonia-oxidizing activity of nitrogen-related rhizospheric microbial communities. These novel insights on interactions between recovered fertilizers, plant and associated microbes can contribute to develop sustainable crop production systems.

Comment on "The global tree restoration potential".

Bastin et al's estimate (Reports, 5 July 2019, p. 76) that tree planting for climate change mitigation could sequester 205 gigatonnes of carbon is approximately five times too large. Their analysis inflated soil organic carbon gains, failed to safeguard against warming from trees at high latitudes and elevations, and considered afforestation of savannas, grasslands, and shrublands to be restoration.

Legume Intercropping With the Bioenergy Crop Sida hermaphrodita on Marginal Soil.

The cultivation of perennial biomass plants on marginal soils can serve as a sustainable alternative to conventional biomass production via annual cultures on fertile soils. Sida hermaphrodita is a promising species to be cultivated in an extensive cropping system on marginal soils in combination with organic fertilization using biogas digestates. In order to enrich this cropping system with nitrogen (N) and to increase overall soil fertility of the production system, we tested the potential of intercropping with leguminous species. In a 3-year outdoor mesocosm study, we intercropped established S. hermaphrodita plants with the perennial legume species Trifolium pratense, T. repens, Melilotus albus, and Medicago sativa individually to study their effects on plant biomass yields, soil N, and above ground biomass N. As a control for intercropping, we used a commercial grass mixture without N2-fixing species as well as a no-intercropping treatment. Results indicate that intercropping in all intercropping treatments increased the total biomass yield, however, grass species competed with S. hermaphrodita for N more strongly than legumes. Legumes enriched the cropping system with fixed atmospheric nitrogen (N2) and legume facilitation effects varied between the legume species. T. pratense increased the biomass yield of S. hermaphrodita and increased the total biomass yield per mesocosm by 300%. Further, the total above ground biomass of S. hermaphrodita and T. pratense contained seven times more N compared to the mono-cropped S. hermaphrodita. T. repens also contributed highly to N facilitation. We conclude that intercropping of legumes, especially T. pratense and T. repens can stimulate the yield of S. hermaphrodita on marginal soils for sustainable plant biomass production.