G. F. (Ciska) Veen

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.

Vertebrate herbivores influence soil nematodes by modifying plant communities.

Abiotic soil properties, plant community composition, and herbivory all have been reported as important factors influencing the composition of soil communities. However, most studies thus far have considered these factors in isolation, whereas they strongly interact in the field. Here, we study how grazing by vertebrate herbivores influences the soil nematode community composition of a floodplain grassland while we account for effects of grazing on plant community composition and abiotic soil properties. Nematodes are the most ubiquitous invertebrates in the soil. They include a variety of feeding types, ranging from microbial feeders to herbivores and carnivores, and they perform key functions in soil food webs. Our hypothesis was that grazing affects nematode community structure and composition through altering plant community structure and composition. Alternatively, we tested whether the effects of grazing may, directly or indirectly, run via changes in soil abiotic properties. We used a long-term field experiment containing plots with and without vertebrate grazers (cattle and rabbits). We compared plant and nematode community structure and composition, as well as a number of key soil abiotic properties, and we applied structural equation modeling to investigate four possible pathways by which grazing may change nematode community composition. Aboveground grazing increased plant species richness and reduced both plant and nematode community heterogeneity. There was a positive relationship between plant and nematode diversity indices. Grazing decreased the number of bacterial-feeding nematodes, indicating that in these grasslands, top-down control of plant production by grazing leads to bottom-up control in the basal part of the bacterial channel of the soil food web. According to the structural equation model, grazing had a strong effect on soil abiotic properties and plant community composition, whereas plant community composition was the main determinant of nematode community composition. Other pathways, which assumed that grazing influenced nematode community composition by inducing changes in soil abiotic properties, did not significantly explain variation in nematode community composition. We conclude that grazing-induced changes in nematode community composition mainly operated via changes in plant community composition. Influences of vertebrate grazers on soil nematodes through modification of abiotic soil properties were of less importance.

Plant-soil feedbacks and the coexistence of competing plants

Plant–soil feedbacks can have important implications for the interactions among plants. Understanding these effects is a major challenge since it is inherently difficult to measure and manipulate highly diverse soil communities. Mathematical models may advance this understanding by making the interplay of the various processes affecting plant–soil interaction explicit and by quantifying the relative importance of the factors involved. The aim of this paper is to provide a complete analysis of a pioneering plant–soil feedback model developed by Bever and colleagues (J Ecol 85: 561–573, 1997; Ecol Lett 2: 52–62, 1999; New Phytol 157: 465–473, 2003) to fully understand the range of possible impacts of plant–soil feedbacks on plant communities within this framework. We analyze this model by means of a new graphical method that provides a complete classification of the potential effects of soil communities on plant competition. Due to the graphical character of the method, the results are relatively easy to obtain and understand. We show that plant diversity depends crucially on two key parameters that may be viewed as measures of the intensity of plant competition and the direction and strength of plant–soil feedback, respectively. Our analysis provides a formal underpinning of earlier claims that plant–soil feedbacks, especially when they are negative, may enhance the diversity of plant communities. In particular, negative plant–soil feedbacks can enhance the range of plant coexistence by inducing competitive oscillations. However, these oscillations can also destabilize plant coexistence, leading to low population densities and extinctions. In addition, positive feedbacks can allow locally stable forms of plant coexistence by inducing alternative stable states. Our findings highlight that the inclusion of plant–soil interactions may fundamentally alter the predictions on the structure and functioning of above-ground ecosystems. The scenarios presented in this study can be used to formulate hypotheses about the ways soil community effects may influence plant competition that can be tested with empirical studies. This will advance our understanding of the role of plant–soil feedback in ecological communities.

Peeking into the black box: a trait‐based approach to predicting plant–soil feedback

Feedbacks between plants and soil communities may be elusive, yet they have far-reaching consequences for plant physiology, competition and community structure. Plant–soil feedbacks (PSFs) are plant-mediated changes to soil properties that ultimately influence the performance of the same or other plants (Van der Putten et al., 2013). These PSFs may be mediated by root-associated organisms (hereafter, root-mediated feedbacks) or saprotrophic organisms and associated litter characteristics (hereafter, litter-mediated feedbacks). However, we know little about the potential mechanistic linkages and relative strengths between these distinct, but connected, processes as root- and litter-mediated feedbacks have generally been studied independently from each other. This is despite the fact that root-associated organisms and saprotrophs can interact through various mechanisms, either directly or as mediated by the plant (e.g. Wardle, 2006). By using a trait-based approach,Ke et al. (in this issue of New Phytologist, pp. 329–341) make an important contribution by integrating root- and litter-mediated PSFs in a nitrogen (N)-based, stage-structured plant population and microbial community model. Their approach allows us to start peeking into the ‘black box’ thereby promoting a better understanding of how PSFs operate interactively. Ke et al. considered various plant traits (e.g. decomposability), but also incorporated trait variation in the physiology, demography and composition of the soil microbial community, and tested their separate and interactive effects on PSF strength in a comprehensive simulation framework. Finally, they used empirical evidence from the literature to support their model predictions.

A test of the hierarchical model of litter decomposition

Our basic understanding of plant litter decomposition informs the assumptions underlying widely applied soil biogeochemical models, including those embedded in Earth system models. Confidence in projected carbon cycle–climate feedbacks therefore depends on accurate knowledge about the controls regulating the rate at which plant biomass is decomposed into products such as CO2. Here we test underlying assumptions of the dominant conceptual model of litter decomposition. The model posits that a primary control on the rate of decomposition at regional to global scales is climate (temperature and moisture), with the controlling effects of decomposers negligible at such broad spatial scales. Using a regional-scale litter decomposition experiment at six sites spanning from northern Sweden to southern France—and capturing both within and among site variation in putative controls—we find that contrary to predictions from the hierarchical model, decomposer (microbial) biomass strongly regulates decomposition at regional scales. Furthermore, the size of the microbial biomass dictates the absolute change in decomposition rates with changing climate variables. Our findings suggest the need for revision of the hierarchical model, with decomposers acting as both local- and broad-scale controls on litter decomposition rates, necessitating their explicit consideration in global biogeochemical models.Accurate understanding of plant litter decomposition is vital to inform Earth system modelling. Here the dominant hierarchical model for plant litter decomposition is found to be wanting, and revisions are suggested.

Effects of root decomposition on plant–soil feedback of early- and mid-successional plant species

Plant-soil feedback (PSF) is an important driver of plant community dynamics. Many studies have emphasized the role of pathogens and symbiotic mutualists in PSFs; however, less is known about the contribution of decomposing litter, especially that of roots. We conducted a PSF experiment, where soils were conditioned by living early- and mid-successional grasses and forbs with and without decomposing roots of conspecific species (conditioning phase). These soils were used to test growth responses of conspecific and heterospecific plant species (feedback phase). The addition of the roots of conspecifics decreased the biomass of both early- and mid-successional plant species in the conditioning phase. In the feedback phase, root addition had positive effects on the biomass of early-successional species and neutral effects on mid-successional species, except when mid-successional grasses were grown in soils conditioned by conspecifics, where effects were negative. Biomass of early- and mid-successional forbs was generally reduced in soils conditioned by conspecifics. We conclude that root decomposition may increase short-term negative PSF effects, but that the effects can become neutral to positive over time, thereby counteracting negative components of PSF. This implies that root decomposition is a key element of PSF and needs to be included in future studies.

Large grazers modify effects of aboveground–belowground interactions on small-scale plant community composition

Aboveground and belowground organisms influence plant community composition by local interactions, and their scale of impact may vary from millimeters belowground to kilometers aboveground. However, it still poorly understood how large grazers that select their forage on large spatial scales interact with small-scale aboveground–belowground interactions on plant community heterogeneity. Here, we investigate how cattle (Bos taurus) modify the effects of interactions between yellow meadow ants (Lasius flavus) and European brown hares (Lepus europaeus) on the formation of small-scale heterogeneity in vegetation composition. In the absence of cattle, hares selectively foraged on ant mounds, while under combined grazing by hares and cattle, vertebrate grazing pressure was similar on and off mounds. Ant mounds that were grazed by only hares had a different plant community composition compared to their surroundings: the cover of the grazing-intolerant grass Elytrigia atherica was reduced on ant mounds, whereas the relative cover of the more grazing-tolerant and palatable grass Festuca rubra was enhanced. Combined grazing by hares and cattle, resulted in homogenization of plant community composition on and off ant mounds, with high overall cover of F. rubra. We conclude that hares can respond to local ant–soil–vegetation interactions, because they are small, selective herbivores that make their foraging decisions on a local scale. This results in small-scale plant patches on mounds of yellow meadow ants. In the presence of cattle, which are less selective aboveground herbivores, local plant community patterns triggered by small-scale aboveground–belowground interactions can disappear. Therefore, cattle modify the consequences of aboveground–belowground interactions for small-scale plant community composition.

Herbivores Enforce Sharp Boundaries Between Terrestrial and Aquatic Ecosystems

The transitions between ecosystems (ecotones) are often biodiversity hotspots, but we know little about the forces that shape them. Today, often sharp boundaries with low diversity are found between terrestrial and aquatic ecosystems. This has been attributed to environmental factors that hamper succession. However, ecosystem properties are often controlled by both bottom-up and top-down forces, but their relative importance in shaping riparian boundaries is not known. We hypothesize that (1) herbivores may enforce sharp transitions between terrestrial and aquatic ecosystems by inhibiting emergent vegetation expansion and reducing the width of the transition zone and (2) the vegetation expansion, diversity, and species turnover are related to abiotic factors in the absence of herbivores, but not in their presence. We tested these hypotheses in 50 paired grazed and ungrazed plots spread over ten wetlands, during two years. Excluding grazers increased vegetation expansion, cover, biomass, and species richness. In ungrazed plots, vegetation cover was negatively related to water depth, whereas plant species richness was negatively related to the vegetation N:P ratio. The presence of (mainly aquatic) herbivores overruled the effect of water depth on vegetation cover increase but did not interact with vegetation N:P ratio. Increased local extinction in the presence of herbivores explained the negative effect of herbivores on species richness, as local colonization rates were unaffected by grazing. We conclude that (aquatic) herbivores can strongly inhibit expansion of the riparian vegetation and reduce vegetation diversity over a range of environmental conditions. Consequently, herbivores enforce sharp boundaries between terrestrial and aquatic ecosystems.

The stoichiometry of nutrient release by terrestrial herbivores and its ecosystem consequences

It is widely recognized that the release of nutrients by herbivores via their waste products strongly impacts nutrient availability for autotrophs. The ratios of nitrogen (N) and phosphorus (P) recycled through herbivore release (i.e., waste N:P) are mainly determined by the stoichiometric composition of the herbivore’s food (food N:P) and its body nutrient content (body N:P). Waste N:P can in turn impact autotroph nutrient limitation and productivity. Herbivore-driven nutrient recycling based on stoichiometric principles is dominated by theoretical and experimental research in freshwater systems, in particular interactions between algae and invertebrate herbivores. In terrestrial ecosystems, the impact of herbivores on nutrient cycling and availability is often limited to studying carbon (C ):N and C:P ratios, while the role of terrestrial herbivores in mediating N:P ratios is also likely to influence herbivore-driven nutrient recycling. In this review, we use rules and predictions on the stoichiometry of nutrient release originating from algal-based aquatic systems to identify the factors that determine the stoichiometry of nutrient release by herbivores. We then explore how these rules can be used to understand the stoichiometry of nutrient release by terrestrial herbivores, ranging from invertebrates to mammals, and its impact on plant nutrient limitation and productivity. Future studies should focus on measuring both N and P when investigating herbivore-driven nutrient recycling in terrestrial ecosystems, while also taking the form of waste product (urine or feces) and other pathways by which herbivores change nutrients into account, to be able to quantify the impact of waste stoichiometry on plant communities.

Plant–Soil Feedback: Bridging Natural and Agricultural Sciences

In agricultural and natural systems researchers have demonstrated large effects of plant-soil feedback (PSF) on plant growth. However, the concepts and approaches used in these two types of systems have developed, for the most part, independently. Here, we present a conceptual framework that integrates knowledge and approaches from these two contrasting systems. We use this integrated framework to demonstrate (i) how knowledge from complex natural systems can be used to increase agricultural resource-use efficiency and productivity and (ii) how research in agricultural systems can be used to test hypotheses and approaches developed in natural systems. Using this framework, we discuss avenues for new research toward an ecologically sustainable and climate-smart future.