Tess F. J. van de Voorde

Plant-soil feedbacks: The past, the present and future challenges

Summary Plant–soil feedbacks is becoming an important concept for explaining vegetation dynamics, the invasiveness of introduced exotic species in new habitats and how terrestrial ecosystems respond to global land use and climate change. Using a new conceptual model, we show how critical alterations in plant–soil feedback interactions can change the assemblage of plant communities. We highlight recent advances, define terms and identify future challenges in this area of research and discuss how variations in strengths and directions of plant–soil feedbacks can explain succession, invasion, response to climate warming and diversity-productivity relationships. While there has been a rapid increase in understanding the biological, chemical and physical mechanisms and their interdependencies underlying plant–soil feedback interactions, further progress is to be expected from applying new experimental techniques and technologies, linking empirical studies to modelling and field-based studies that can include plant–soil feedback interactions on longer time scales that also include long-term processes such as litter decomposition and mineralization. Significant progress has also been made in analysing consequences of plant–soil feedbacks for biodiversity-functioning relationships, plant fitness and selection. To further integrate plant–soil feedbacks into ecological theory, it will be important to determine where and how observed patterns may be generalized, and how they may influence evolution. Synthesis. Gaining a greater understanding of plant–soil feedbacks and underlying mechanisms is improving our ability to predict consequences of these interactions for plant community composition and productivity under a variety of conditions. Future research will enable better prediction and mitigation of the consequences of human-induced global changes, improve efforts of restoration and conservation and promote sustainable provision of ecosystem services in a rapidly changing world.

The way forward in biochar research: targeting trade-offs between the potential wins

Biochar application to soil is currently widely advocated for a variety of reasons related to sustainability. Typically, soil amelioration with biochar is presented as a multiple‐‘win’ strategy, although it is also associated with potential risks such as environmental contamination. The most often claimed benefits of biochar (i.e. the ‘wins’) include (i) carbon sequestration; (ii) soil fertility enhancement; (iii) biofuel/bioenergy production; (iv) pollutant immobilization; and (v) waste disposal. However, the vast majority of studies ignore possible trade‐offs between them. For example, there is an obvious trade‐off between maximizing biofuel production and maximizing biochar production. Also, relatively little attention has been paid to mechanisms, as opposed to systems impacts, behind observed biochar effects, often leaving open the question as to whether they reflect truly unique properties of biochar as opposed to being simply the short‐term consequences of a fertilization or liming effect. Here, we provide an outline for the future of soil biochar research. We first identify possible trade‐offs between the potential benefits. Second, to be able to better understand and quantify these trade‐offs, we propose guidelines for robust experimental design and selection of appropriate controls that allow both mechanistic and systems assessment of biochar effects and trade‐offs between the wins. Third, we offer a conceptual framework to guide future experiments and suggest guidelines for the standardized reporting of biochar experiments to allow effective between‐site comparisons to quantify trade‐offs. Such a mechanistic and systems framework is required to allow effective comparisons between experiments, across scales and locations, to guide policy and recommendations concerning biochar application to soil.

Where, when and how plant–soil feedback matters in a changing world

Summary It is increasingly acknowledged that plant–soil feedbacks may play an important role in driving the composition of plant communities and functioning of terrestrial ecosystems. However, the mechanistic understanding of plant–soil feedbacks, as well as their roles in natural ecosystems in proportion to other possible drivers, is still in its infancy. Such knowledge will enhance our capacity to determine the contribution of plant–soil feedback to community and ecosystem responses under global environmental change. Here, we review how plant–soil feedbacks may develop under extreme drought and precipitation events, CO2 and nitrogen enrichment, temperature increase, land use change and plant species loss vs. gain. We present a framework for opening the ‘black box of soil’ considering the responses of the various biotic components (enemies, symbionts and decomposers) of plant–soil feedback to the global environmental changes, and we discuss how to integrate these components to understand and predict the net effects of plant–soil feedbacks under the various scenarios of change. To gain an understanding of how plant–soil feedback plays out in realistic settings, we also use the framework to discuss its interaction with other drivers of plant community composition, including competition, facilitation, herbivory, and soil physical and chemical properties. We conclude that understanding the role that plant–soil feedback plays in shaping the responses of plant community composition and ecosystem processes to global environmental changes requires unravelling the individual contributions of enemies, symbionts and decomposers. These biotic factors may show different response rates and strengths, thereby resulting in different net magnitudes and directions of plant–soil feedbacks under various scenarios of global change. We also need tests of plant–soil feedback under more realistic conditions to determine its contribution to changes in patterns and processes in the field, both at ecologically and evolutionary relevant time-scales.

Above‐ and below‐ground herbivory effects on below‐ground plant–fungus interactions and plant–soil feedback responses

1.Feeding by insect herbivores can affect plant growth and the concentration of defense compounds in plant tissues. Since plants provide resources for soil organisms, herbivory can also influence the composition of the soil community via its effects on the plant. Soil organisms, in turn, are important for plant growth. We tested whether insect herbivores, via their effects on the soil microbial community, can influence plant-soil feedbacks. 2.We first examined the effects of above-ground (AG) and below-ground (B) insect herbivory on the composition of pyrrolizidine alkaloids (PAs) in roots and on soil fungi in roots and rhizosphere soil of ragwort (Jacobaea vulgaris). The composition of fungal communities in roots and rhizosphere soil was affected by both AG and BG herbivory, but fungal composition also differed considerably between roots and rhizosphere soil. The composition of PAs in roots was affected only by BG herbivory. 3.Thirteen different fungal species were detected in roots and rhizosphere soil. The presence of the potentially pathogenic fungus Fusarium oxysporum decreased and that of Phoma exigua increased in presence of BG herbivory, but only in soil samples. 4.We then grew new plants in the soils conditioned by plants exposed to the herbivore treatments and in unconditioned soil. A subset of the new plants was exposed to foliar insect herbivory. Plant-soil feedback was strongly negative, but the feedback effect was least negative in soil conditioned by plants that had been exposed to BG herbivory. There was a negative direct effect of foliar herbivory on plant biomass during the feedback phase, but this effect was far less strong when the soil was conditioned by plants exposed to AG herbivory. AG herbivory during the conditioning phase also caused a soil feedback effect on the PA concentration in the foliage of ragwort. 5.Synthesis. Our results illustrate how insect herbivory can affect interactions between plants and soil organisms, and via these effects how herbivory can alter the performance of late-growing plants. Plant-soil feedback is emerging as an important theme in ecology and these results highlight that plant-soil feedback should be considered from a multitrophic AG and BG perspective

Are there evolutionary consequences of plant–soil feedbacks along soil gradients?

1.Both abiotic and biotic gradients exist in soils and several of these gradients have been shown to select for plant traits. Moreover, plants possess a multitude of traits that can lead to strong niche construction (i.e., plant-induced changes to soils). Our objectives in this paper are to outline both empirical and theoretical evidence for the evolutionary consequences of plant-soil linkages and feedbacks on plants along soil heterogeneity gradients. 2.We describe a simple mathematical model of plant evolution to explore the relationship between the sign and magnitude of feedback and the divergence of plant traits. We also constructed an individual-based simulation model to study the conditions under which plant-soil feedbacks occur, niche construction evolves and plant traits diverge. 3.This approach allows us to address specific hypotheses regarding relationships between positive and negative plant-soil feedback with variation in niche construction, the strength of selective gradients and the relative importance of local adaptation vs. feedbacks. 4.The models suggest that feedbacks between soils and plants may commonly result in evolutionary interactions. The simulation model indicates that plant traits can diverge with niche construction and traits can be selected for in response to niche construction. However, the magnitude of feedbacks and how strongly they evolve depends on the amount of gene flow and the strength of selective gradients over time. 5.These results suggest that plant-soil feedback can lead to evolution in plants and reveals new research directions for further inquiry. Questions addressing trade-offs and relationships between positive and negative feedbacks as well as adaptation and maladaptation of plant traits represent important frontiers in plant-soil feedback studies.

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

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

Comparing arbuscular mycorrhizal communities of individual plants in a grassland biodiversity experiment

Plants differ greatly in the soil organisms colonizing their roots. However, how soil organism assemblages of individual plant roots can be influenced by plant community properties remains poorly understood. We determined the composition of arbuscular mycorrhizal fungi (AMF) in Jacobaea vulgaris plants, using terminal restriction fragment length polymorphism (T-RFLP). The plants were collected from an experimental field site with sown and unsown plant communities. Natural colonization was allowed for 10 yr in sown and unsown plots. Unsown plant communities were more diverse and spatially heterogeneous than sown ones. Arbuscular mycorrhizal fungi diversity did not differ between sown and unsown plant communities, but there was higher AMF assemblage dissimilarity between individual plants in the unsown plant communities. When we grew J. vulgaris in field soil that was homogenized after collection in order to rule out spatial variation, no differences in AMF dissimilarity between sown and unsown plots were found. Our study shows that experimental manipulation of plant communities in the field, and hence plant community assembly history, can influence the AMF communities of individual plants growing in those plant communities. This awareness is important when interpreting results from field surveys and experimental ecological studies in relation to plant-symbiont interactions.