Plant-soil Biota Interactions Research Articles

Grazing weakens the linkages between plants and soil biotic communities in the alpine grassland

Livestock grazing alters the diversity and composition of plants and soil biota in grassland ecosystems. However, whether and how grazing affects plant-soil biota interactions are limited. Here, we performed a field investigation on the Tibetan grasslands to determine the relationships between plant community properties (biomass, diversity and richness) and soil biota (abundance, diversity and composition of bacteria, fungi and nematodes) in the long-term yak grazing and ungrazed plots, and responses of plant-soil biota linkages to grazing in alpine meadows and alpine swampy meadows were compared. The results found that grazing did not cause significant changes in plant community properties but increased the soil water content. Further, grazing weakened plant-soil microbes/nematode relationships in alpine meadows. The bacterial and fungal abundances were correlated with plant belowground biomass and Simpson index in the ungrazed plots of alpine meadows, while the correlation was not significant under grazing. Bacterial composition was correlated with plant richness only in the ungrazed meadows. Plant-soil nematode linkages were more sensitive to grazing than plant-microbes linkages. Grazing decoupled the relationships between the abundances of nematode trophic groups and plant aboveground biomass, richness and Simpson index in alpine meadows, while the decoupling phenomenon is less evident in alpine swampy meadows. The SEM results indicate that grazing altered the plant above- and belowground biomass to affect the soil nematode community, while influenced soil microbes only through alterations of plant belowground biomass. The findings highlight the importance of grazing in influencing the interactions between aboveground plant communities and soil biological communities in Tibetan grasslands.

Interspecific interactions between crops influence soil functional groups and networks in a maize/soybean intercropping system

Despite increasing evidence that intercropping systems may increase crop productivity, little is known about whether and how soil biota change under interspecific competition among plants. A field experiment with maize/soybean intercropping and the corresponding monoculture systems was conducted under four nitrogen fertilization regimes to investigate the effects of interspecific plant interactions on grain yield, soil properties (β-glucosidase and water-soluble carbohydrates), and biotic communities (bacteria, fungi, and nematodes). The soils under maize and soybean in the intercropping system were sampled separately to represent intercropped maize and intercropped soybean, respectively. Compared to monocultures, the complexity and robustness of soil networks comprising bacterial, fungal, and nematode communities increased in intercropped maize soils, but densities of plant parasitic nematodes and β-glucosidase activity were reduced. Intercropped soybean soils had lower C availability due to chronic shading by maize, but a significant increase was found in saprophytic fungi, and plant parasitic nematodes compared to soybean monoculture soils. Although intercropped soybean suffered from interspecific competition with maize, the interactions within the fungal community increased for both crop species in the intercropping system. Our study demonstrates that increased carbon uptake in maize due to increased light capture in the intercropping system can facilitate nutrient cycling by altering the abundance of functional groups of soil organisms, such as saprophytic fungi, and enhancing network complexity and stability. We detected a trade-off between productivity and soil nematode diversity in the intercropping system under nitrogen fertilization, the yield of maize increased but soil nematode richness decreased at low nitrogen level, while the yield of soybean decreased but the nematode richness increased at high nitrogen level. These findings show that both trade-offs and benefits occur in intercropping systems and highlight the role of plant-soil biota interactions in such systems.

Plant responses to soil biota depend on precipitation history, plant diversity, and productivity.

Soil biota are critical drivers of plant growth, population dynamics, and community structure and thus have wide-ranging effects on ecosystem function. Interactions between plants and soil biota are complex, however, and can depend on the diversity and productivity of the plant community and environmental conditions. Plant-soil biota interactions may be especially important during stressful periods, such as drought, when plants can gain great benefits from beneficial biota but may be susceptible to antagonists. How soil biota respond to drought is also important and can influence plant growth following drought and leave legacies that affect future plant responses to soil biota and further drought. To explore how drought legacies and plant community context influence plant growth responses to soil biota and further drought, we collected soils from 12 grasslands varying in plant diversity and productivity where precipitation was experimentally reduced. We used these soils as inoculum in a growth chamber experiment testing how precipitation history (ambient or reduced) and soil biota (live or sterile soil inoculum) mediate plant growth and drought responses within an experimental plant community. We also tested whether these responses differed with the diversity and productivity of the community where the soil was collected. Plant growth responses to soil biota were positive when inoculated with soils from less diverse and productive plant communities and became negative as the diversity and productivity of the conditioning community increased. At low diversity, however, positive soil biota effects on plant growth were eliminated if precipitation had been reduced in the field, suggesting that diversity loss may heighten climate change sensitivity. Differences among species within the experimental community in their responses to soil biota and drought suggest that species benefitting from less drought sensitive soil biota may be able to compensate for some of this loss of productivity. Regardless of the plant species and soil origin, further drought eliminated any effects of soil biota on plant growth. Consequently, soil biota may be unable to buffer the effects of drought on primary productivity or other ecosystem functions as extreme events increase in frequency.

Plant–soil biota interactions explain shifts in plant community composition under global change

Abstract Plant–soil biota interactions play a crucial role in the assembly of plant communities and the maintenance of plant species diversity. However, few studies have tested how the effect of soil biota on plant species and communities depends on environmental context and whether shifts in plant community composition caused by environmental change are associated with variation in plant–soil biota interactions. We combined a field experiment in a Tibetan alpine meadow and a greenhouse experiment with factorial combinations of nitrogen (N) enrichment and warming to examine the role of plant–soil biota interactions in plant community dynamics. The results showed that plant relative abundances were negatively correlated with the net effects of soil biota on plant growth but only under ambient field conditions. Warming and N enrichment alleviated the negative soil biota effects in the greenhouse, and changed plant community composition and reduced species diversity in the field. Importantly, changes in soil biota effects on plant growth were positively correlated with changes in plant relative abundances caused by warming and N enrichment in field. In a parallel field experiment, the diversity of mycorrhizal fungi increased while the diversity of fungal pathogens remained unchanged under warming and N enrichment, indicating that soil biodiversity may play a critical role in plant responses to environmental change. This study empirically demonstrates that altered plant–soil biota interactions explain shifts in plant community composition under global change, providing new insights into the mechanisms of diversity loss in a changing world. A free Plain Language Summary can be found within the Supporting Information of this article.

Conspecific and heterospecific plant–soil biota interactions of Lonicera japonica in its native and introduced range: implications for invasion success

Conspecific and heterospecific plant–soil biota interactions of Lonicera japonica in its native and introduced range: implications for invasion success

Exotic plants accumulate and share herbivores yet dominate communities via rapid growth

Herbivores may facilitate or impede exotic plant invasion, depending on their direct and indirect interactions with exotic plants relative to co-occurring natives. However, previous studies investigating direct effects have mostly used pairwise native-exotic comparisons with few enemies, reached conflicting conclusions, and largely overlooked indirect interactions such as apparent competition. Here, we ask whether native and exotic plants differ in their interactions with invertebrate herbivores. We manipulate and measure plant-herbivore and plant-soil biota interactions in 160 experimental mesocosm communities to test several invasion hypotheses. We find that compared with natives, exotic plants support higher herbivore diversity and biomass, and experience larger proportional biomass reductions from herbivory, regardless of whether specialist soil biota are present. Yet, exotics consistently dominate community biomass, likely due to their fast growth rates rather than strong potential to exert apparent competition on neighbors. We conclude that polyphagous invertebrate herbivores are unlikely to play significant direct or indirect roles in mediating plant invasions, especially for fast-growing exotic plants.

Species abundance fluctuations over 31 years are associated with plant–soil feedback in a species‐rich mountain meadow

Abstract Increasing evidence suggest that plant–soil interactions play an essential role in plant community assembly processes. Empirical investigations show that plant species abundance in the field is often related to plant–soil biota interactions; however, the direction of these relations have yielded inconsistent results. We combined unique 31‐year long field data on species abundances from a species‐rich mountain meadow with single time point plant–soil feedback greenhouse experiments of 24 co‐occurring plant species. We tested whether these relations were dynamic in time, whether coupled increases and decreases in abundance between years were related to plant–soil feedback and whether these changes were underlain by years in which manuring was applied. The prevailingly negative relationship between plant–soil feedback and plant relative abundance in the field was significantly time‐dependent, which may reconcile the contrasting results in literature. Furthermore, significantly coupled oscillations appeared between species relative abundance changes and plant–soil feedback, which were likely moderated by years in which manuring was applied. Our results are consistent with the notion that the more abundant species are stabilised by negative plant–soil feedback, and the less abundant species co‐vary with the fluctuations of these more competitive species. Synthesis. Our results project plant–soil feedback as an important regulatory mechanism in plant communities, operating in conjunction with species' competitive ability and soil nutrient availability. We suggest that negative feedback is particularly prominent in more abundant plant species that profit from more readily available soil nutrients than less abundant species with positive feedback. Negative plant–soil feedback may thus prevent more abundant plant species from out‐competing less abundant plant species, facilitating stable species co‐existence.

Biogeographic differences in plant-soil biota relationships contribute to the exotic range expansion of Verbascum thapsus.

Exotic plant species can evolve adaptations to environmental conditions in the exotic range. Furthermore, soil biota can foster exotic spread in the absence of negative soil pathogen–plant interactions or because of increased positive soil biota–plant feedbacks in the exotic range. Little is known, however, about the evolutionary dimension of plant–soil biota interactions when comparing native and introduced ranges.To assess the role of soil microbes for rapid evolution in plant invasion, we subjected Verbascum thapsus, a species native to Europe, to a reciprocal transplant experiment with soil and seed material originating from Germany (native) and New Zealand (exotic). Soil samples were treated with biocides to distinguish between effects of soil fungi and bacteria. Seedlings from each of five native and exotic populations were transplanted into soil biota communities originating from all populations and subjected to treatments of soil biota reduction: application of (a) fungicide, (b) biocide, (c) a combination of the two, and (d) control.For most of the investigated traits, native populations showed higher performance than exotic populations; there was no effect of soil biota origin. However, plants developed longer leaves and larger rosettes when treated with their respective home soil communities, indicating that native and exotic plant populations differed in their interaction with soil biota origin. The absence of fungi and bacteria resulted in a higher specific root length, suggesting that V. thapsus may compensate the absence of mutualistic microbes by increasing its root–soil surface contact. Synthesis. Introduced plants can evolve adaptations to soil biota in their new distribution range. This demonstrates the importance of biogeographic differences in plant–soil biota relationships and suggests that future studies addressing evolutionary divergence should account for differential effects of soil biota from the home and exotic range on native and exotic populations of successful plant invaders.

Plant–soil feedbacks mediate shrub expansion in declining forests, but only in the right light

Abstract Contemporary global change, including the widespread mortality of foundation tree species, is altering ecosystems and plant communities at unprecedented rates. Plant–soil interactions drive myriad community dynamics, and we hypothesized that such interactions may be an important driver of succession following the loss of foundation tree species. We examined whether plant–soil biota interactions, in the context of a putatively important light gradient associated with foundation tree decline, mediate the expansion of Rhododendron maximum in southeastern US forests where Tsuga canadensis (eastern hemlock), a dominant foundation tree species, is in decline. Using an 11‐month, controlled inoculation experiment paired with Illumina sequencing, we tested the following hypotheses: (1) Relative to conspecific (R. maximum‐conditioned) soils, R. maximum seedlings have higher performance in soils conditioned by T. canadensis and lower performance in interspace soils (conditioned by neither T. canadensis nor R. maximum) due to variation in soil fungal biota, and (2) seedling performance is greater in high‐light vs. low‐light environments (matching environments under infested vs. uninfested T. canadensis crowns, respectively). In partial support of the first hypothesis, we found that R. maximum seedling performance was highest in T. canadensis‐conditioned and R. maximum‐conditioned soils and lowest in interspace soils. Mechanistically, soils conditioned by T. canadensis and R. maximum had more ericoid and ectomycorrhizal fungi, less saprotrophic fungi, and were less species‐rich than interspace soils, and variation in these community traits predicted substantial variation in R. maximum seedling biomass. However, in support of our second hypothesis, soil effects on plant performance were evident in high light only; in low light, soil inoculation did not affect plant performance and plants performed worse on average. Synthesis. Our findings suggest that interactions with soil biota act synergistically with altered abiotic environments to mediate species responses to widespread foundation tree mortality, providing evidence for a novel mechanism of plant response to large‐scale disturbance. Examining plant–soil interactions in the context of relevant abiotic gradients can, therefore, enhance our understanding, predictions and management of community development processes following forest disturbance.

Modularity reveals the tendency of arbuscular mycorrhizal fungi to interact differently with generalist and specialist plant species in gypsum soils.

Patterns in plant-soil biota interactions could be influenced by the spatial distribution of species due to soil conditions or by the functional traits of species. Gypsum environments usually constitute a mosaic of heterogeneous soils where gypsum and nongypsum soils are imbricated at a local scale. A case study of the interactions of plants with arbuscular mycorrhizal fungi (AMF) in gypsum environments can be illustrative of patterns in biotic interactions. We hypothesized that (i) soil characteristics might affect the AMF community and (ii) there are differences between the AMF communities (modules) associated with plants exclusive to gypsum soils (gypsophytes) and those associated with plants that show facultative behavior on gypsum and/or marly-limestone soils (gypsovags). We used indicator species and network analyses to test for differences between the AMF communities harbored in gypsophyte and gypsovag plants. We recorded 46 operational taxonomic units (OTUs) belonging to nine genera of Glomeromycota. The indicator species analysis showed two OTUs preferentially associating with gypsum soils and three OTUs preferentially associating with marly-limestone soils. Modularity analysis revealed that soil type can be a major factor shaping AMF communities, and some AMF groups showed a tendency to interact differently with plants that had distinct ecological strategies (gypsophytes and gypsovags). Characterization of ecological networks can be a valuable tool for ascertaining the potential influence of above- and below-ground biotic interactions (plant-AMF) on plant community composition.

Interactions with soil biota shift from negative to positive when a tree species is moved outside its native range

Studies evaluating plant-soil biota interactions in both native and introduced plant ranges are rare, and thus far have lacked robust experimental designs to account for several potential confounding factors. Here, we investigated the effects of soil biota on growth of Pinus contorta, which has been introduced from Canada to Sweden. Using Swedish and Canadian soils, we conducted two glasshouse experiments. The first experiment utilized unsterilized soil from each country, with a full-factorial cross of soil origin, tree provenance, and fertilizer addition. The second experiment utilized gamma-irradiated sterile soil from each country, with a full-factorial cross of soil origin, soil biota inoculation treatments, tree provenance, and fertilizer addition. The first experiment showed higher seedling growth on Swedish soil relative to Canadian soil. The second experiment showed this effect was due to differences in soil biotic communities between the two countries, and occurred independently of all other experimental factors. Our results provide strong evidence that plant interactions with soil biota can shift from negative to positive following introduction to a new region, and are relevant for understanding the success of some exotic forest plantations, and invasive and range-expanding native species.

Plant–soil biota interactions of an invasive species in its native and introduced ranges: Implications for invasion success

Biotic interactions of exotic plant species in their introduced ranges may differ from those of co-occurring plant species and from interactions in their native range. Interactions less negative (Enemy Release Hypothesis) or more positive (Enhanced Mutualist Hypothesis) compared to native plants may enhance invasive success and change exotic plant traits. We investigated plant–soil interactions of Chinese tallow (Triadica sebifera) from China (native range) and US (invasive range) populations along with US and China species within four co-occurring genera (Liquidambar, Ulmus, Celtis, and Platanus) grown in both ranges. Treatments included sterilized, home, away, active mix, and fungicide treated soils. The net effect of soil biota on Triadica performance was generally negative or had no effect in its native range but was always positive in its invasive range. In China, Triadica had higher survival and biomass in “away” (heterospecific) soils than in “home” (conspecific) soil, but in the US, only biomass was higher. The pattern of performance in home and away soils suggests a stronger negative effect of specific pathogens for Triadica in China (Enemy Release Hypothesis). No other species had a significant feedback in either range. Triadica mycorrhizal colonization was higher in the US than in China supporting the Enhanced Mutualist Hypothesis. On average, Triadica performance was similar for native and invasive populations. However, invasive populations had greater biomass in active mix than in sterilized or fungicide-treated soil and native populations had higher mycorrhizal colonization in home than in away soils or active mix. These population origin results suggest genetic differences in strength or specificity of mycorrhizal interactions. Overall, our results support both ecological and evolutionary variation in interactions with the soil community that may influence the invasion success of exotic plants.

Conspecific Plant-Soil Feedbacks of Temperate Tree Species in the Southern Appalachians, USA

Many tree species have seedling recruitment patterns suggesting that they are affected by non-competitive distance-dependent sources of mortality. We conducted an experiment, with landscape-level replication, to identify cases of negative distance-dependent effects and whether variation in these effects corresponded with tree recruitment patterns in the southern Appalachian Mountains region. Specifically, soil was collected from 14 sites and used as inocula in a 62 day growth chamber experiment determining whether tree seedling growth was less when interacting with soil from conspecific (like) than heterospecific (other) tree species. Tests were performed on six tree species. Three of the tree species had been previously described as having greater recruitment around conspecifics (i.e. facilitator species group) compared to the other half (i.e. inhibitor species group). We were then able to determine whether variation in negative distance-dependent effects corresponded with recruitment patterns in the field. Across the six species, none were negatively affected by soil inocula from conspecific relative to heterospecific sources. Most species (four of six) were unaffected by soil source. Two species (Prunus serotina and Tsuga canadensis) had enhanced growth in pots inoculated with soil from conspecific trees vs. heterospecifics. Species varied in their susceptibility to soil pathogens, but trends across all species revealed that species classified as inhibitors were not more negatively affected by conspecific than heterospecific soil inocula or more susceptible to pathogenic effects than facilitators. Although plant-soil biota interactions may be important for individual species and sites, it may be difficult to scale these interactions over space or levels of ecological organization. Generalizing the importance of plant-soil feedbacks or other factors across regional scales may be especially problematic for hyperdiverse temperate forests where interactions may be spatially variable.

Disturbance influences the outcome of plant-soil biota interactions in the invasive Acacia longifolia and in native species

Interrelated causes of plant invasion have been gaining increasing recognition. However, research on this subject has mainly focused around conceptual models. Here we explore whether plant–soil biota feedbacks and disturbance, two major factors capable of facilitating invasive plants in introduced ranges, interact to preferentially benefit exotics compared to native plants. We investigated the influence of fire disturbance on plant–soil biota interactions for the invasive Acacia longifolia and two dominant natives (Cytisus striatus and Pinus pinaster) in Portuguese dune systems. In the first experiment, we grew exotic and native plants in soil inoculated with soil biota from unburned or recently burned soils collected in an area with small invasion intensity by A. longifolia. Soil biota effects on the exotic legume A. longifolia changed from neutral to positive after fire, whereas the opposite outcome was observed in the native legume C. striatus, and a change from negative to neutral effects after fire occurred in the native P. pinaster. Fire reduced mycorrhizal colonization in all species and rhizobial colonization in C. striatus but not in A. longifolia. In the second experiment, we grew the exotic and native plants with conspecific and heterospecific soil biota from undisturbed soils (area with low invasion intensity by A. longifolia), and from post-fire soils (area affected by a fire ∼12 years ago and currently heavily invaded by A. longifolia). The exotic benefited more from post-fire than from undisturbed soil biota, particularly from those associated with natives. Natives did not experience detrimental effects with invasive-associated soil biota. Our results show that fire disturbance affected the functional interactions between soil biota and plants that may benefit more the exotic than some native species. Disturbance may open a window of opportunity that promotes invader success by altering soil enemy and mutualistic impacts.

Population variation of invasive Spartina alterniflora can differentiate bacterial diversity in its rhizosphere

While several studies have documented that invasive plants can change the microbial communities, little is known about how soil microbial communities respond to population variation of invasive plants. Here, nine populations of Spartina alterniflora were selected from the east coast of China along latitudinal gradient to compare bacterial diversity of rhizospheres among these populations. The bacterial diversity in S. alterniflora rhizospheres was valued by denaturing gradient gel electrophoresis (DGGE) analysis. Shannon–Weaver diversity index (H′) and number of DGGE bands showed that rhizosphere bacterial diversity of S. alterniflora populations increased along a latitudinal gradient when all the populations were grown in a common garden. These findings suggest that population variation of S. alterniflora can differentiate the rhizosphere bacterial diversity, and the latitudinal gradient can shape the specific plant–bacterial diversity relationship. Our results adding to the recent literature suggest that invasive plant–soil biota interactions would have clinal variation with environmental gradients and improve our understanding of the mechanisms and processes of plant invasions.

Soil biota and invasive plants

Interactions between plants and soil biota resist invasion by some nonnative plants and facilitate others. In this review, we organize research and ideas about the role of soil biota as drivers of invasion by nonnative plants and how soil biota may fit into hypotheses proposed for invasive success. For example, some invasive species benefit from being introduced into regions of the world where they encounter fewer soil-borne enemies than in their native ranges. Other invasives encounter novel but strong soil mutualists which enhance their invasive success. Leaving below-ground natural enemies behind or encountering strong mutualists can enhance invasions, but indigenous enemies in soils or the absence of key soil mutualists can help native communities resist invasions. Furthermore, inhibitory and beneficial effects of soil biota on plants can accelerate or decelerate over time depending on the net effect of accumulating pathogenic and mutualistic soil organisms. These 'feedback' relationships may alter plant-soil biota interactions in ways that may facilitate invasion and inhibit re-establishment by native species. Although soil biota affect nonnative plant invasions in many different ways, research on the topic is broadening our understanding of why invasive plants can be so astoundingly successful and expanding our perspectives on the drivers of natural community organization.

Plant–soil biota interactions and spatial distribution of black cherry in its native and invasive ranges

AbstractOne explanation for the higher abundance of invasive species in their non‐native than native ranges is the escape from natural enemies. But there are few experimental studies comparing the parallel impact of enemies (or competitors and mutualists) on a plant species in its native and invaded ranges, and release from soil pathogens has been rarely investigated. Here we present evidence showing that the invasion of black cherry (Prunus serotina) into north‐western Europe is facilitated by the soil community. In the native range in the USA, the soil community that develops near black cherry inhibits the establishment of neighbouring conspecifics and reduces seedling performance in the greenhouse. In contrast, in the non‐native range, black cherry readily establishes in close proximity to conspecifics, and the soil community enhances the growth of its seedlings. Understanding the effects of soil organisms on plant abundance will improve our ability to predict and counteract plant invasions.