Wim H. van der Putten

Going back to the roots: the microbial ecology of the rhizosphere

The rhizosphere is the interface between plant roots and soil where interactions among a myriad of microorganisms and invertebrates affect biogeochemical cycling, plant growth and tolerance to biotic and abiotic stress. The rhizosphere is intriguingly complex and dynamic, and understanding its ecology and evolution is key to enhancing plant productivity and ecosystem functioning. Novel insights into key factors and evolutionary processes shaping the rhizosphere microbiome will greatly benefit from integrating reductionist and systems-based approaches in both agricultural and natural ecosystems. Here, we discuss recent developments in rhizosphere research in relation to assessing the contribution of the micro- and macroflora to sustainable agriculture, nature conservation, the development of bio-energy crops and the mitigation of climate change.

Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists

Plants function in a complex multitrophic environment. Most multitrophic studies, however, have almost exclusively focused on aboveground interactions, generally neglecting the fact that above- and belowground organisms interact. The spatial and temporal dynamics of above- and belowground herbivores, plant pathogens, and their antagonists, can differ in space and time. This affects the temporal interaction strengths and impacts of above- and belowground higher trophic level organisms on plants. Combining both above- and belowground compartments in studies of multitrophic interactions throughout the life cycle of plants will improve our understanding of ecology and evolution in the real world.

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.

Belowground biodiversity and ecosystem functioning

Evidence is mounting that the immense diversity of microorganisms and animals that live belowground contributes significantly to shaping aboveground biodiversity and the functioning of terrestrial ecosystems. Our understanding of how this belowground biodiversity is distributed, and how it regulates the structure and functioning of terrestrial ecosystems, is rapidly growing. Evidence also points to soil biodiversity as having a key role in determining the ecological and evolutionary responses of terrestrial ecosystems to current and future environmental change. Here we review recent progress and propose avenues for further research in this field.

Soil invertebrate fauna enhances grassland succession and diversity

One of the most important areas in ecology is to elucidate the factors that drive succession in ecosystems and thus influence the diversity of species in natural vegetation. Significant mechanisms in this process are known to be resource limitation and the effects of aboveground vertebrate herbivores. More recently, symbiotic and pathogenic soil microbes have been shown to exert a profound effect on the composition of vegetation and changes therein. However, the influence of invertebrate soil fauna on succession has so far received little attention. Here we report that invertebrate soil fauna might enhance both secondary succession and local plant species diversity. Soil fauna from a series of secondary grassland succession stages selectively suppress early successional dominant plant species, thereby enhancing the relative abundance of subordinate species and also that of species from later succession stages. Soil fauna from the mid-succession stage had the strongest effect. Our results clearly show that soil fauna strongly affects the composition of natural vegetation and we suggest that this knowledge might improve the restoration and conservation of plant species diversity.

Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels.

Current predictions on species responses to climate change strongly rely on projecting altered environmental conditions on species distributions. However, it is increasingly acknowledged that climate change also influences species interactions. We review and synthesize literature information on biotic interactions and use it to argue that the abundance of species and the direction of selection during climate change vary depending on how their trophic interactions become disrupted. Plant abundance can be controlled by aboveground and belowground multitrophic level interactions with herbivores, pathogens, symbionts and their enemies. We discuss how these interactions may alter during climate change and the resulting species range shifts. We suggest conceptual analogies between species responses to climate warming and exotic species introduced in new ranges. There are also important differences: the herbivores, pathogens and mutualistic symbionts of range-expanding species and their enemies may co-migrate, and the continuous gene flow under climate warming can make adaptation in the expansion zone of range expanders different from that of cross-continental exotic species. We conclude that under climate change, results of altered species interactions may vary, ranging from species becoming rare to disproportionately abundant. Taking these possibilities into account will provide a new perspective on predicting species distribution under climate change.

MICROBE-MEDIATED PLANT-SOIL FEEDBACK CAUSES HISTORICAL CONTINGENCY EFFECTS IN PLANT COMMUNITY ASSEMBLY

Plant-soil feedback affects performance and competitive ability of individual plants. However, the importance of plant-soil feedback in historical contingency processes and plant community dynamics is largely unknown. In microcosms, we tested how six early- successional plant species of secondary succession on ex-arable land induced plant-specific changes in soil community composition. Following one growth cycle of conditioning the soil community, soil feedback effects were assessed as plant performance in soil of their own as compared to soil from a mixture of the other five early-successional species. Performance was tested in monocultures and in mixed communities with heterospecific competition from mid- successional species. The role of soil microorganisms was determined by isolating the microbial component from the soil community, re-inoculating microorganisms into sterilized substrate, and analyzing plant biomass responses of the early- and mid-successional species. Plant-soil feedback responses of the early-successional species were negative and significantly increased when the plants were grown in a competitive environment with heterospecifics. In monocultures, three early-successional species experienced negative feedback in soil with a history of conspecifics, while all early-successional species experienced negative feedback when grown with interspecific competition. Interestingly, the nonnative forb Conyza canadensis showed the weakest soil feedback effect. Biomass production of the early- successional plant species was profoundly reduced by the microbial inocula, most strongly when exposed to inocula of conspecific origin. Molecular characterization of the fungal and bacterial rhizosphere communities revealed a relationship between plant biomass production and the composition of the dominant fungal species. Furthermore, our results show that, in early secondary succession, the early-successional plant species induce changes in the soil microbial community composition that cause historical contingency effects in dominance patterns of mid-succession plant communities. We conclude that feedback between early-successional plant species and soil microorgan- isms can play a crucial role in breaking dominance of early-successional plant communities. Moreover the influences on soil microorganism community composition influenced plant community dynamics in the mid-successional plant communities. These results shed new light on how feedback effects between plants and soil organisms in one successional stage result in a biotic legacy effect, which influences plant community processes in subsequent successional stages.

Terrestrial Ecosystem Responses to Species Gains and Losses

Ecosystems worldwide are losing some species and gaining others, resulting in an interchange of species that is having profound impacts on how these ecosystems function. However, research on the effects of species gains and losses has developed largely independently of one another. Recent conceptual advances regarding effects of species gain have arisen from studies that have unraveled the mechanistic basis of how invading species with novel traits alter biotic interactions and ecosystem processes. In contrast, studies on traits associated with species loss are fewer, and much remains unknown about how traits that predispose species to extinction affect ecological processes. Species gains and losses are both consequences and drivers of global change; thus, explicit integration of research on how both processes simultaneously affect ecosystem functioning is key to determining the response of the Earth system to current and future human activities.

Biodiversity Increases the Resistance of Ecosystem Productivity to Climate Extremes

It remains unclear whether biodiversity buffers ecosystems against climate extremes, which are becoming increasingly frequent worldwide. Early results suggested that the ecosystem productivity of diverse grassland plant communities was more resistant, changing less during drought, and more resilient, recovering more quickly after drought, than that of depauperate communities. However, subsequent experimental tests produced mixed results. Here we use data from 46 experiments that manipulated grassland plant diversity to test whether biodiversity provides resistance during and resilience after climate events. We show that biodiversity increased ecosystem resistance for a broad range of climate events, including wet or dry, moderate or extreme, and brief or prolonged events. Across all studies and climate events, the productivity of low-diversity communities with one or two species changed by approximately 50% during climate events, whereas that of high-diversity communities with 16–32 species was more resistant, changing by only approximately 25%. By a year after each climate event, ecosystem productivity had often fully recovered, or overshot, normal levels of productivity in both high- and low-diversity communities, leading to no detectable dependence of ecosystem resilience on biodiversity. Our results suggest that biodiversity mainly stabilizes ecosystem productivity, and productivity-dependent ecosystem services, by increasing resistance to climate events. Anthropogenic environmental changes that drive biodiversity loss thus seem likely to decrease ecosystem stability, and restoration of biodiversity to increase it, mainly by changing the resistance of ecosystem productivity to climate events.

Soil food web properties explain ecosystem services across European land use systems

Intensive land use reduces the diversity and abundance of many soil biota, with consequences for the processes that they govern and the ecosystem services that these processes underpin. Relationships between soil biota and ecosystem processes have mostly been found in laboratory experiments and rarely are found in the field. Here, we quantified, across four countries of contrasting climatic and soil conditions in Europe, how differences in soil food web composition resulting from land use systems (intensive wheat rotation, extensive rotation, and permanent grassland) influence the functioning of soils and the ecosystem services that they deliver. Intensive wheat rotation consistently reduced the biomass of all components of the soil food web across all countries. Soil food web properties strongly and consistently predicted processes of C and N cycling across land use systems and geographic locations, and they were a better predictor of these processes than land use. Processes of carbon loss increased with soil food web properties that correlated with soil C content, such as earthworm biomass and fungal/bacterial energy channel ratio, and were greatest in permanent grassland. In contrast, processes of N cycling were explained by soil food web properties independent of land use, such as arbuscular mycorrhizal fungi and bacterial channel biomass. Our quantification of the contribution of soil organisms to processes of C and N cycling across land use systems and geographic locations shows that soil biota need to be included in C and N cycling models and highlights the need to map and conserve soil biodiversity across the world.