Paul Kardol

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.

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.

Soil ecosystem functioning under climate change: plant species and community effects

Feedbacks of terrestrial ecosystems to atmospheric and climate change depend on soil ecosystem dynamics. Soil ecosystems can directly and indirectly respond to climate change. For example, warming directly alters microbial communities by increasing their activity. Climate change may also alter plant community composition, thus indirectly altering the soil communities that depend on their inputs. To better understand how climate change may directly and indirectly alter soil ecosystem functioning, we investigated old-field plant community and soil ecosystem responses to single and combined effects of elevated [CO2], warming, and precipitation in Tennessee (USA). Specifically, we collected soils at the plot level (plant community soils) and beneath dominant plant species (plant-specific soils). We used microbial enzyme activities and soil nematodes as indicators for soil ecosystem functioning. Our study resulted in two main findings: (1) Overall, while there were some interactions, water, relative to increases in [CO2] and warming, had the largest impact on plant community composition, soil enzyme activity, and soil nematodes. Multiple climate-change factors can interact to shape ecosystems, but in our study, those interactions were largely driven by changes in water. (2) Indirect effects of climate change, via changes in plant communities, had a significant impact on soil ecosystem functioning, and this impact was not obvious when looking at plant community soils. Climate-change effects on enzyme activities and soil nematode abundance and community structure strongly differed between plant community soils and plant-specific soils, but also within plant-specific soils. These results indicate that accurate assessments of climate-change impacts on soil ecosystem functioning require incorporating the concurrent changes in plant function and plant community composition. Climate-change-induced shifts in plant community composition will likely modify or counteract the direct impact of atmospheric and climate change on soil ecosystem functioning, and hence, these indirect effects should be taken into account when predicting the manner in which global change will alter ecosystem functioning.

How understanding aboveground–belowground linkages can assist restoration ecology

The topic of aboveground-belowground linkages has seen much recent activity, resulting in several conceptual advances regarding plant-soil feedbacks, multitrophic interactions, and how organisms drive ecosystem processes. Although restoration ecology has been rapidly evolving as a scientific discipline, the principles that have developed regarding aboveground-belowground linkages have yet to be thoroughly integrated into it. In this review, we conceptually integrate the role of aboveground-belowground linkages with the principles of restoration ecology through a framework that transcends multiple levels of ecological organization, and illustrate its application through three examples: restoration of abandoned land, reversal of biological invasions, and restoration of natural disturbances. We conclude that this integration can greatly assist restoration ecology, through aiding identification of effective invention practices and prediction of ecosystem recovery.

Nitrogen deposition weakens plant–microbe interactions in grassland ecosystems

Soil carbon (C) and nitrogen (N) stoichiometry is a main driver of ecosystem functioning. Global N enrichment has greatly changed soil C : N ratios, but how altered resource stoichiometry influences the complexity of direct and indirect interactions among plants, soils, and microbial communities has rarely been explored. Here, we investigated the responses of the plant-soil-microbe system to multi-level N additions and the role of dissolved organic carbon (DOC) and inorganic N stoichiometry in regulating microbial biomass in semiarid grassland in northern China. We documented a significant positive correlation between DOC and inorganic N across the N addition gradient, which contradicts the negative nonlinear correlation between nitrate accrual and DOC availability commonly observed in natural ecosystems. Using hierarchical structural equation modeling, we found that soil acidification resulting from N addition, rather than changes in the plant community, was most closely related to shifts in soil microbial community composition and decline of microbial respiration. These findings indicate a down-regulating effect of high N availability on plant-microbe interactions. That is, with the limiting factor for microbial biomass shifting from resource stoichiometry to soil acidity, N enrichment weakens the bottom-up control of soil microorganisms by plant-derived C sources. These results highlight the importance of integratively studying the plant-soil-microbe system in improving our understanding of ecosystem functioning under conditions of global N enrichment.

Getting Plant–Soil Feedbacks out of the Greenhouse: Experimental and Conceptual Approaches

Plant-soil feedbacks (PSFs) contain two steps: (a) different plant species must create different soils and (b) these different soils must alter subsequent plant growth. Two-phase experiments are used to demonstrate PSF. In Phase I, soils are cultivated by known plants. In Phase II, plants are used as phytometers to measure soil differences created in Phase I. Ideally, a third phase, Phase III, is performed in which soil analyses and inoculation experiments are used to identify mecha- nisms of PSFs. A review of the literature reveals 25 studies that performed phases I and II. Of these 25 studies, 22 used grassland species, 21 were performed in a greenhouse, 19 were published between 2004 and 2006, and 12 used non-native species. Across studies, 271 feedback values were reported. Negative feedbacks represented 147 of the 271 values and produced, on average, a 37% reduction in plant biomass. Positive feedbacks represented 41 tests and produced, on average,

Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands.

Soil biota and plant diversity Soil biota, including symbionts such as mycorrhizal fungi and nitrogen-fixing bacteria, as well as fungal and bacterial pathogens, affect terrestrial plant diversity and growth patterns (see the Perspective by van der Putten). Teste et al. monitored growth and survival in Australian shrubland plant species paired with soil biota from plants of the same species and from other plants that use different nutrient acquisition strategies. Plant-soil feedbacks appear to drive local plant diversity through interactions between the different types of plants and their associated soil biota. Bennett et al. studied plant-soil feedbacks in soil and seeds from 550 populations of 55 species of North American trees. Feedbacks ranged from positive to negative, depending on the type of mycorrhizal association, and were related to how densely the same species occurred in natural populations. Science, this issue p. 134, p. 173; see also p. 181 Feedback between plants and soil biota influences diversity in Australian shrublands. Soil biota influence plant performance through plant-soil feedback, but it is unclear whether the strength of such feedback depends on plant traits and whether plant-soil feedback drives local plant diversity. We grew 16 co-occurring plant species with contrasting nutrient-acquisition strategies from hyperdiverse Australian shrublands and exposed them to soil biota from under their own or other plant species. Plant responses to soil biota varied according to their nutrient-acquisition strategy, including positive feedback for ectomycorrhizal plants and negative feedback for nitrogen-fixing and nonmycorrhizal plants. Simulations revealed that such strategy-dependent feedback is sufficient to maintain the high taxonomic and functional diversity characterizing these Mediterranean-climate shrublands. Our study identifies nutrient-acquisition strategy as a key trait explaining how different plant responses to soil biota promote local plant diversity.

Subordinate plant species enhance community resistance against drought in semi‐natural grasslands

According to the insurance hypothesis, more diverse plant communities are more likely to be resistant to drought. Whilst many experiments have been carried out to determine the effects of plant diversity on plant community insurance, the results are still contradictory. Here, we conducted a drought experiment where we tested whether the presence of subordinate species increases plant community insurance. In Swiss Jura grassland, we combined a removal experiment of subordinate species with a summer drought event using rainout shelters. Plant community composition was determined after the drought and based on biomass measurements; we estimated resistance, recovery and resilience of the plant community for each combination of treatments. Moreover, to assess drought impacts on water-use efficiency (WUE), we analysed carbon isotope ratios (13C values) in plant leaves of two dominants and two subordinates collected at the end of the drought period. We showed that subordinate species are more resistant to drought and increased community resistance by enhancing their above-ground biomass production during the imposed drought. These patterns were associated with decreased competitiveness of dominant species whose biomass decreased during drought. Significant increase in 13C values in plant tissue under drought indicated a better WUE for the measured species. Interestingly, the WUE was significantly higher in plots where subordinates were removed. Recovery and resilience were not affected by the summer drought, but the absence of subordinates reduced overall above-ground biomass in both watered and drought plots. Synthesis. We demonstrated that, independent of plant diversity, the presence of drought-resistant subordinate species increases plant community insurance against drought and, hence, is important for the functioning of grassland ecosystems.

Global patterns and substrate-based mechanisms of the terrestrial nitrogen cycle

Nitrogen (N) deposition is impacting the services that ecosystems provide to humanity. However, the mechanisms determining impacts on the N cycle are not fully understood. To explore the mechanistic underpinnings of N impacts on N cycle processes, we reviewed and synthesised recent progress in ecosystem N research through empirical studies, conceptual analysis and model simulations. Experimental and observational studies have revealed that the stimulation of plant N uptake and soil retention generally diminishes as N loading increases, while dissolved and gaseous losses of N occur at low N availability but increase exponentially and become the dominant fate of N at high loading rates. The original N saturation hypothesis emphasises sequential N saturation from plant uptake to soil retention before N losses occur. However, biogeochemical models that simulate simultaneous competition for soil N substrates by multiple processes match the observed patterns of N losses better than models based on sequential competition. To enable better prediction of terrestrial N cycle responses to N loading, we recommend that future research identifies the response functions of different N processes to substrate availability using manipulative experiments, and incorporates the measured N saturation response functions into conceptual, theoretical and quantitative analyses.

Emissions of ammonia and greenhouse gases during combined pre-composting and vermicomposting of duck manure

Combined pre-composting and vermicomposting has shown potential for reclamation of solid wastes, which is a significant source of ammonia (NH3), and greenhouse gases (GHG), including nitrous oxide (N2O), methane (CH4), and carbon dioxide (CO2). Earthworms and amendments may both affect physico-chemical characteristics that control gas-producing processes, and thus affect NH3 and GHG emissions. Here, we used two-way ANOVA to test the effects of addition of reed straw and combined addition of reed straw and zeolite on NH3 and GHG emissions during pre-composting of duck manure, either with or without a follow-up phase of vermicomposting. Results showed that cumulative N2O, CH4, and CO2 emissions during pre-composting and vermicomposting ranged from 92.8, 5.8, and 260.6 mg kg(-)(1) DM to 274.2, 30.4, and 314.0 mg kg(-1) DM, respectively. Earthworms and amendments significantly decreased N2O and CH4 emissions. Emission of CO2 was not affected by earthworms, but increased in responses to addition of reed straw. Cumulative NH3 emission ranged from 3.0 to 8.1 g kg(-1) DM, and was significantly decreased by reed straw and zeolite addition. In conclusion, combined pre-composting and vermicomposting with reed straw and zeolite addition would be strongly recommended in mitigating emissions of N2O, CH4, and NH3 from duck manure. Moreover, this method also provides nutrient-rich products that can be used as a fertilizer.