Temporal carry‐over effects in sequential plant–soil feedbacks

Plant–soil feedbacks (PSF) strongly influence plant performance. However, to what extent these PSF effects are persistent in the soil and how they are altered by species that subsequently condition the soil is unclear. Here we test how conspecific and heterospecific soil‐conditioning effects interact across different soil‐conditioning phases. We conducted a fully factorial glasshouse experiment where six plant species conditioned soils in two consecutive phases and measured the performance of Jacobaea vulgaris. The species that conditioned the soil during the second conditioning phase strongly determined the performance of J. vulgaris, but also the order and combination of species that conditioned the soil in the two phases accounted for a large part of the variance. For shoot biomass this interaction was the dominant variance component. We show that soil conditioning legacies carry‐over and interact with the conditioning effects of succeeding plants. In the field, species replacements at the patch level often appear to be unpredictable and we suggest that sequential feedbacks may explain these apparently unpredictable transitions.     

Intraspecific plant–soil feedback and intraspecific overyielding in Arabidopsis thaliana

Understanding the mechanisms of community coexistence and ecosystem functioning may help to counteract the current biodiversity loss and its potentially harmful consequences. In recent years, plant–soil feedback that can, for example, be caused by below‐ground microorganisms has been suggested to play a role in maintaining plant coexistence and to be a potential driver of the positive relationship between plant diversity and ecosystem functioning. Most of the studies addressing these topics have focused on the species level. However, in addition to interspecific interactions, intraspecific interactions might be important for the structure of natural communities. Here, we examine intraspecific coexistence and intraspecific diversity effects using 10 natural accessions of the model species Arabidopsis thaliana (L.) Heynh. We assessed morphological intraspecific diversity by measuring several above‐ and below‐ground traits. We performed a plant–soil feedback experiment that was based on these trait differences between the accessions in order to determine whether A. thaliana experiences feedback at intraspecific level as a result of trait differences. We also experimentally tested the diversity–productivity relationship at intraspecific level. We found strong differences in above‐ and below‐ground traits between the A. thaliana accessions. Overall, plant–soil feedback occurred at intraspecific level. However, accessions differed in the direction and strength of this feedback: Some accessions grew better on their own soils, some on soils from other accessions. Furthermore, we found positive diversity effects within A. thaliana: Accession mixtures produced a higher total above‐ground biomass than accession monocultures. Differences between accessions in their feedback response could not be explained by morphological traits. Therefore, we suggest that they might have been caused by accession‐specific accumulated soil communities, by root exudates, or by accession‐specific resource use based on genetic differences that are not expressed in morphological traits. Synthesis. Our results provide some of the first evidence for intraspecific plant–soil feedback and intraspecific overyielding. These findings may have wider implications for the maintenance of variation within species and the importance of this variation for ecosystem functioning. Our results highlight the need for an increased focus on intraspecific processes in plant diversity research to fully understand the mechanisms of coexistence and ecosystem functioning.     

Microbial phylotype composition and diversity predicts plant productivity and plant–soil feedbacks

The relationship between ecological variation and microbial genetic composition is critical to understanding microbial influence on community and ecosystem function. In glasshouse trials using nine native legume species and 40 rhizobial strains, we find that bacterial rRNA phylotype accounts for 68% of amoung isolate variability in symbiotic effectiveness and 79% of host specificity in growth response. We also find that rhizobial phylotype diversity and composition of soils collected from a geographical breadth of sites explains the growth responses of two acacia species. Positive soil microbial feedback between the two acacia hosts was largely driven by changes in diversity of rhizobia. Greater rhizobial diversity accumulated in association with the less responsive host species, Acacia salicina, and negatively affected the growth of the more responsive Acacia stenophylla. Together, this work demonstrates correspondence of phylotype with microbial function, and demonstrates that the dynamics of rhizobia on host species can feed back on plant population performance.     

Negative plant‐phyllosphere feedbacks in native Asteraceae hosts – a novel extension of the plant‐soil feedback framework

Over the past 25 years, the plant‐soil feedback (PSF) framework has catalyzed our understanding of how belowground microbiota impact plant fitness and species coexistence. Here, we apply a novel extension of this framework to microbiota associated with aboveground tissues, termed ‘plant‐phyllosphere feedback (PPFs)’. In parallel greenhouse experiments, rhizosphere and phyllosphere microbiota of con‐ and heterospecific hosts from four species were independently manipulated. In a third experiment, we tested the combined effects of soil and phyllosphere feedback under field conditions. We found that three of four species experienced weak negative PSF whereas, in contrast, all four species experienced strong negative PPFs. Field‐based feedback estimates were highly negative for all four species, though variable in magnitude. Our results suggest that phyllosphere microbiota, like rhizosphere microbiota, can potentially mediate plant species coexistence via negative feedbacks. Extension of the PSF framework to the phyllosphere is needed to more fully elucidate plant‐microbiota interactions.     

Community‐level plant–soil feedbacks explain landscape distribution of native and non‐native plants

Plant–soil feedbacks (PSFs) have gained attention for their potential role in explaining plant growth and invasion. While promising, most PSF research has measured plant monoculture growth on different soils in short‐term, greenhouse experiments. Here, five soil types were conditioned by growing one native species, three non‐native species, or a mixed plant community in different plots in a common‐garden experiment. After 4 years, plants were removed and one native and one non‐native plant community were planted into replicate plots of each soil type. After three additional years, the percentage cover of each of the three target species in each community was measured. These data were used to parameterize a plant community growth model. Model predictions were compared to native and non‐native abundance on the landscape. Native community cover was lowest on soil conditioned by the dominant non‐native, Centaurea diffusa, and non‐native community cover was lowest on soil cultivated by the dominant native, Pseudoroegneria spicata. Consistent with plant growth on the landscape, the plant growth model predicted that the positive PSFs observed in the common‐garden experiment would result in two distinct communities on the landscape: a native plant community on native soils and a non‐native plant community on non‐native soils. In contrast, when PSF effects were removed, the model predicted that non‐native plants would dominate all soils, which was not consistent with plant growth on the landscape. Results provide an example where PSF effects were large enough to change the rank‐order abundance of native and non‐native plant communities and to explain plant distributions on the landscape. The positive PSFs that contributed to this effect reflected the ability of the two dominant plant species to suppress each other's growth. Results suggest that plant dominance, at least in this system, reflects the ability of a species to suppress the growth of dominant competitors through soil‐mediated effects.     

Native and non‐native grasses generate common types of plant–soil feedbacks by altering soil nutrients and microbial communities

Soil conditioning occurs when plants alter features of their soil environment. When these alterations affect subsequent plant growth, it is a plant soil feedback. Plant–soil feedbacks are an important and understudied aspect of aboveground–belowground linkages in plant ecology that influence plant coexistence, invasion and restoration. Here, we examine plant–soil feedback dynamics of seven co‐occurring native and non‐native grass species to address the questions of how plants modify their soil environment, do those modifications inhibit or favor their own species relative to other species, and do non‐natives exhibit different plant–soil feedback dynamics than natives. We used a two‐phase design, wherein a first generation of plants was grown to induce species‐specific changes in the soil and a second generation of plants was used as a bioassay to determine the effects of those changes. We also used path‐analysis to examine the potential chain of effects of the first generation on soil nutrients and soil microbial composition and on bioassay plant performance. Our findings show species‐specific (rather than consistent within groups of natives and non‐natives) soil conditioning effects on both soil nutrients and the soil microbial community by plants. Additionally, native species produced plant–soil feedback types that benefit other species more than themselves and non‐native invasive species tended to produce plant–soil feedback types that benefit themselves more than other species. These results, coupled with previous field observations, support hypotheses that plant–soil feedbacks may be a mechanism by which some non‐native species increase their invasive potential and plant–soil feedbacks may influence the vulnerability of a site to invasion.     

Predators in the plant–soil feedback loop: aboveground plant‐associated predators may alter the outcome of plant–soil interactions

Plant–soil feedback (PSF) can structure plant communities, promoting coexistence (negative PSF) or monodominance (positive PSF). At higher trophic levels, predators can alter plant community structure by re‐allocating resources within habitats. When predator and plant species are spatially associated, predators may alter the outcome of PSF. Here, I explore the influence of plant‐associated predators on PSF using a generalised cellular automaton model that tracks nutrients, plants, herbivores and predators. I explore key contingencies in plant–predator associations such as whether predators associate with live vs. senesced vegetation. Results indicate that plant‐associated predators shift PSF to favour the host plant when predators colonise live vegetation, but the outcome of PSF will depend upon plant dispersal distance when predators colonise dead vegetation. I apply the model to two spider‐associated invasive plants, finding that spider predators should shift PSF dynamics in a way that inhibits invasion by one forest invader, but exacerbates invasion by another.     

Globally,plant‐soil feedbacks are weak predictors of plant abundance

Plant‐soil feedbacks (PSFs) have been shown to strongly affect plant performance under controlled conditions, and PSFs are thought to have far reaching consequences for plant population dynamics and the structuring of plant communities. However, thus far the relationship between PSF and plant species abundance in the field is not consistent. Here, we synthesize PSF experiments from tropical forests to semiarid grasslands, and test for a positive relationship between plant abundance in the field and PSFs estimated from controlled bioassays. We meta‐analyzed results from 22 PSF experiments and found an overall positive correlation (0.12 ≤ r¯ ≤ 0.32) between plant abundance in the field and PSFs across plant functional types (herbaceous and woody plants) but also variation by plant functional type. Thus, our analysis provides quantitative support that plant abundance has a general albeit weak positive relationship with PSFs across ecosystems. Overall, our results suggest that harmful soil biota tend to accumulate around and disproportionately impact species that are rare. However, data for the herbaceous species, which are most common in the literature, had no significant abundance‐PSFs relationship. Therefore, we conclude that further work is needed within and across biomes, succession stages and plant types, both under controlled and field conditions, while separating PSF effects from other drivers (e.g., herbivory, competition, disturbance) of plant abundance to tease apart the role of soil biota in causing patterns of plant rarity versus commonness.     

Genetic by environment interactions affect plant–soil linkages

The role of plant intraspecific variation in plant–soil linkages is poorly understood, especially in the context of natural environmental variation, but has important implications in evolutionary ecology. We utilized three 18‐ to 21‐year‐old common gardens across an elevational gradient, planted with replicates of five Populus angustifolia genotypes each, to address the hypothesis that tree genotype (G), environment (E), and G × E interactions would affect soil carbon and nitrogen dynamics beneath individual trees. We found that soil nitrogen and carbon varied by over 50% and 62%, respectively, across all common garden environments. We found that plant leaf litter (but not root) traits vary by genotype and environment while soil nutrient pools demonstrated genotype, environment, and sometimes G × E interactions, while process rates (net N mineralization and net nitrification) demonstrated G × E interactions. Plasticity in tree growth and litter chemistry was significantly related to the variation in soil nutrient pools and processes across environments, reflecting tight plant–soil linkages. These data overall suggest that plant genetic variation can have differential affects on carbon storage and nitrogen cycling, with implications for understanding the role of genetic variation in plant–soil feedback as well as management plans for conservation and restoration of forest habitats with a changing climate.     

Intraspecific variation in herbivore‐induced plant volatiles influences the spatial range of plant–parasitoid interactions

Chemical information influences the behaviour of many animals, thus affecting species interactions. Many animals forage for resources that are heterogeneously distributed in space and time, and have evolved foraging behaviour that utilizes information related to these resources. Herbivore‐induced plant volatiles (HIPVs), emitted by plants upon herbivore attack, provide information on herbivory to various animal species, including parasitoids. Little is known about the spatial scale at which plants attract parasitoids via HIPVs under field conditions and how intraspecific variation in HIPV emission affects this spatial scale. Here, we investigated the spatial scale of parasitoid attraction to two cabbage accessions that differ in relative preference of the parasitoid Cotesia glomerata when plants were damaged by Pieris brassicae caterpillars. Parasitoids were released in a field experiment with plants at distances of up to 60 m from the release site using intervals between plants of 10 or 20 m to assess parasitism rates over time and distance. Additionally, we observed host‐location behaviour of parasitoids in detail in a semi‐field tent experiment with plant spacing up to 8 m. Plant accession strongly affected successful host location in field set‐ups with 10 or 20 m intervals between plants. In the semi‐field set‐up, plant finding success by parasitoids decreased with increasing plant spacing, differed between plant accessions, and was higher for host‐infested plants than for uninfested plants. We demonstrate that parasitoids can be attracted to herbivore‐infested plants over large distances (10 m or 20 m) in the field, and that stronger plant attractiveness via HIPVs increases this distance (up to at least 20 m). Our study indicates that variation in plant traits can affect attraction distance, movement patterns of parasitoids, and ultimately spatial patterns of plant–insect interactions. It is therefore important to consider plant‐trait variation in HIPVs when studying animal foraging behaviour and multi‐trophic interactions in a spatial context.     

Moderate plant–soil feedbacks have small effects on the biodiversity–productivity relationship: A field experiment

Plant–soil feedback (PSF) has gained attention as a mechanism promoting plant growth and coexistence. However, most PSF research has measured monoculture growth in greenhouse conditions. Translating PSFs into effects on plant growth in field communities remains an important frontier for PSF research. Using a 4‐year, factorial field experiment in Jena, Germany, we measured the growth of nine grassland species on soils conditioned by each of the target species (i.e., 72 PSFs). Plant community models were parameterized with or without these PSF effects, and model predictions were compared to plant biomass production in diversity–productivity experiments. Plants created soils that changed subsequent plant biomass by 40%. However, because they were both positive and negative, the average PSF effect was 14% less growth on “home” than on “away” soils. Nine‐species plant communities produced 29 to 37% more biomass for polycultures than for monocultures due primarily to selection effects. With or without PSF, plant community models predicted 28%–29% more biomass for polycultures than for monocultures, again due primarily to selection effects. Synthesis: Despite causing 40% changes in plant biomass, PSFs had little effect on model predictions of plant community biomass across a range of species richness. While somewhat surprising, a lack of a PSF effect was appropriate in this site because species richness effects in this study were caused by selection effects and not complementarity effects (PSFs are a complementarity mechanism). Our plant community models helped us describe several reasons that even large PSF may not affect plant productivity. Notably, we found that dominant species demonstrated small PSF, suggesting there may be selective pressure for plants to create neutral PSF. Broadly, testing PSFs in plant communities in field conditions provided a more realistic understanding of how PSFs affect plant growth in communities in the context of other species traits.     

Grazing‐induced changes in plant–soil feedback alter plant biomass allocation

Large vertebrate herbivores, as well as plant–soil feedback interactions are important drivers of plant performance, plant community composition and vegetation dynamics in terrestrial ecosystems. However, it is poorly understood whether and how large vertebrate herbivores and plant–soil feedback effects interact. Here, we study the response of grassland plant species to grazing‐induced legacy effects in the soil and we explore whether these plant responses can help us to understand long‐term vegetation dynamics in the field. In a greenhouse experiment we tested the response of four grassland plant species, Agrostis capillaris, Festuca rubra, Holcus lanatus and Rumex acetosa, to field‐conditioned soils from grazed and ungrazed grassland. We relate these responses to long‐term vegetation data from a grassland exclosure experiment in the field. In the greenhouse experiment, we found that total biomass production and biomass allocation to roots was higher in soils from grazed than from ungrazed plots. There were only few relationships between plant production in the greenhouse and the abundance of conspecifics in the field. Spatiotemporal patterns in plant community composition were more stable in grazed than ungrazed grassland plots, but were not related to plant–soil feedbacks effects and biomass allocation patterns. We conclude that grazing‐induced soil legacy effects mainly influenced plant biomass allocation patterns, but could not explain altered vegetation dynamics in grazed grasslands. Consequently, the direct effects of grazing on plant community composition (e.g. through modifying light competition or differences in grazing tolerance) appear to overrule indirect effects through changes in plant–soil feedback.     

Individual‐level differences in generalist caterpillar responses to a plant–plant cue

1. Plant–plant communication has been found to affect interactions between herbivores and plants in several model systems. In these systems, herbivore‐induced volatile chemical cues are emitted and perceived by other plants (receivers), which subsequently change their defensive phenotypes. Most studies have focused on how the effects of volatile cues affect plant damage, whereas herbivore performance has rarely been examined. 2. In this study, it is shown that plant–plant communication between willows reduced the growth rate, feeding rate, and conversion efficiency of some individuals but not others of a generalist caterpillar, Orgyia vetusta. 3. Using a paired, no‐choice trial design, there was substantial variation between caterpillar individuals in their response to willows that had been induced with a volatile plant–plant cue. This variation was explained by feeding parameters of the individual herbivores. Individuals behaved similarly when fed induced and non‐induced willow leaves. Specifically, growth rates of caterpillars that grew rapidly on non‐induced willow leaves were negatively affected by plant–plant cues, but growth rates of caterpillars that grew slowly on non‐induced willow leaves were not affected by the responses to volatiles from neighbouring willows. 4. Induction by volatile plant–plant cues reduced the growth rates of those individual herbivores that caused the greatest damage to willow, but had little effect on weak growers.     

Geographic mosaics of plant–soil microbe interactions in a global plant invasion

Aim Our aim in this study was to document the global biogeographic variation in the effects of soil microbes on the growth of Centaurea solstitialis (yellow starthistle; Asteraceae), a species that has been introduced throughout the world, but has become highly invasive only in some introduced regions. Location  To assess biogeographic variation in plant–soil microbe interactions, we collected seeds and soils from native Eurasian C. solstitialis populations and introduced populations in California, Argentina and Chile. Methods To test whether escape from soil‐borne natural enemies may contribute to the success of C. solstitialis, we compared the performance of plants using seeds and soils collected from each of the biogeographic regions in greenhouse inoculation/sterilization experiments. Results  We found that soil microbes had pervasive negative effects on plants from all regions, but these negative effects were significantly weaker in soils from non‐native ranges in Chile and California than in those from the non‐native range in Argentina and the native range in Eurasia. Main conclusions The biogeographic differences in negative effects of microbes in this study conformed to the enemy‐release hypothesis (ERH) overall, but the strong negative effect of soil biota in Argentina, where C. solstitialis is invasive, and weaker effects in Chile where it is not, indicated that different factors influencing invasion are likely to occur in large scale biogeographic mosaics of interaction strengths.     

Using generalized autoregressive error models to understand fire–vegetation–soil feedbacks in a mulga–spinifex landscape mosaic

Aim To develop a new modelling approach for spatially autocorrelated non‐normal data, and apply it to a case study of the role that fire–vegetation–soil feedbacks play in maintaining boundaries between fire‐sensitive and fire‐promoted plant communities. Location A mulga (Acacia aneura) shrubland–spinifex (Triodia spp.) grassland mosaic, central Australia. Methods Autoregressive error models were extended to non‐normal data by incorporating neighbourhood values of the response and predictor variables into generalized nonlinear models. These models were used to examine the environmental correlates of three response variables: mulga cover; fire frequency in areas free of mulga; and the presence of mulga banding. Mulga cover and mulga banding were assessed visually by overlaying 4477 × 1 km² grid cells on both Landsat 7 ETM+ and very high resolution imagery. Fire frequency was estimated from an existing fire history for central Australia, based on remotely sensed fire scars. Results The autoregressive error models explained 27%, 47% and 57% of the null deviance of mulga cover, fire frequency and mulga banding, respectively, with 12%, 15% and 24% of the null deviance being explained by environmental variables alone. These models accounted for virtually all residual spatial autocorrelation. While there was a clear negative relationship between mulga cover and fire frequency, there was little evidence that mulga was being restricted to parts of the landscape with inherently low fire frequencies. Mulga was most abundant at very low slope angles and on red earths, both of which are likely to reflect high site productivity, while fire frequency was not clearly affected by slope angle and was also relatively high on red earths. Main conclusions The modelling approach we have developed provides a much needed way of analysing spatially autocorrelated non‐normal data and can be easily incorporated into an information‐theoretic modelling framework. Using this approach, we provide evidence that mulga and spinifex have a highly antagonistic relationship. In more productive parts of the landscape, mulga suppresses spinifex and fire, while in less productive parts of the landscape, fire and spinifex suppress mulga, leading to the remarkable abruptness of mulga–spinifex boundaries that are maintained via fire–vegetation–soil feedbacks.     

Sexual differences in flower defense and correlated male‐biased florivory in a plant–florivore system

Male‐biased florivory is a prominent phenomenon in the interaction between plants and florivores, and is potentially related to the evolution of flower traits and sex expression; however, its adaptive significance is not well understood. We studied florivory in the geometrid moth Chloroclystis excisa utilizing flower buds of a sexually polymorphic shrub, Eurya japonica, to reveal relationships between flower sex and moth oviposition preference, moth larval performance, and plant phenolics composition. In the field, C. excisa exploited flower buds on male and hermaphrodite trees but never those on female trees. In the laboratory, moths showed a strong oviposition preference for male over female flower buds, and larvae did not survive on female buds. Mortality was caused solely by feeding on the calyx covering the female bud. Female calyces contained higher concentrations of total phenolics and condensed tannins than did male calyces. These results suggest that substantial sexual differences in defense against florivory may have evolved in association with the differentiation of flower sexes and that a strong preference for the weakly defended flower sex may have evolved in florivores as a counter‐adaptation.