Above-belowground Interactions Research Articles

Warming, nitrogen deposition, and provenance shift above-belowground insect interactions and host compensatory growth.

Above-belowground insect herbivore interactions and plant compensatory growth are crucial for reshaping the fitness of invasive plants, and it is likely that climate warming, nitrogen (N) deposition, and plant provenance influence this interaction and growth in a complex way. We performed an experiment with Solidago canadensis from home and introduced ranges, leaf-chewing Spodoptera litura, and root-feeding Protaetia brevitarsis under climate warming and N deposition, and addressed how these abiotic stressors and plant provenance jointly shaped the reciprocal effects between S. litura and P. brevitarsis and the compensatory growth of S. canadensis after herbivory. Under ambient conditions, S. litura and P. brevitarsis inhibited each other on the basis of growth; warming, N addition or warming plus N addition shifted or even reversed this competition depending on provenance. While the survival-based above-belowground interactions differed from growth-based ones, warming or warming plus N addition also shifted or even reversed the neutralism or amensalism detected under ambient conditions depending on provenance. S. canadensis from its home range was more tolerant of herbivory than from its introduced range under ambient conditions; warming, N addition or warming plus N addition decreased the plant compensatory growth of native S. canadensis, but increased that of invasive S. canadensis relative to ambient conditions. These findings suggest that climate warming and N deposition could enhance positive above-belowground insect interactions, increasing insect pressures on S. canadensis, and that plant provenance might be important in mediating climate change effects on insect interactions and host compensatory growth under plant invasions.

Fungal communities are passengers in community development of dune ecosystems, while bacteria are not.

An increasing number of studies of above-belowground interactions provide a fundamental basis for our understanding of the coexistence between plant and soil communities. However, we lack empirical evidence to understand the directionality of drivers of plant and soil communities under natural conditions: 'Are soil microorganisms driving plant community functioning or do they adapt to the plant community?' In a field experiment in an early successional dune ecosystem, we manipulated soil communities by adding living (i.e., natural microbial communities) and sterile soil inocula, originating from natural ecosystems, and examined the annual responses of soil and plant communities. The experimental manipulations had a persistent effect on the soil microbial community with divergent impacts for living and sterile soil inocula. The plant community was also affected by soil inoculation, but there was no difference between the impacts of living and sterile inocula. We also observed an increasing convergence of plant and soil microbial composition over time. Our results show that alterations in soil abiotic and biotic conditions have long-term effects on the composition of both plant and soil microbial communities. Importantly, our study provides direct evidence that soil microorganisms are not "drivers" of plant community dynamics. We found that soil fungi and bacteria manifest different community assemblies in response to treatments. Soil fungi act as "passengers," that is, soil microorganisms reflect plant community dynamics but do not alter it, whereas soil bacteria are neither "drivers" nor "passengers" of plant community dynamics in early successional ecosystems. These results are critical for understanding the community assembly of plant and soil microbial communities under natural conditions and are directly relevant for ecosystem management and restoration.

Soil arthropod communities collected from agricultural soils influence wheat growth and modify phytohormone responses to aboveground herbivory in a microcosm experiment

Soil arthropods can affect plant growth and aboveground interactions directly via root herbivory and indirectly through nutrient cycling and interactions with soil microorganisms. Research on these effects of soil arthropods has focused on a few taxa within natural systems, largely neglecting agroecosystems and arthropod community-level effects. This study investigated the effects of soil arthropod communities from cereal-based agroecosystems on wheat plant growth and above-belowground interactions. Nutrient cycling and wheat growth were measured in a greenhouse microcosm experiment using field-collected agricultural soils from two rotational schemes with and without their soil arthropod communities. The effects of soil arthropods on aboveground phytohormones and colony growth of an aphid [Metopolophium festucae cerealium (Stroyan)] infesting the plants were measured. Wheat grown in soils with arthropod communities had significantly greater root (+ Arth mean: 0.15 ± 0.01 g; − Arth mean: 0.06 ± 0.01 g; F1,54 = 72.34, p < 0.001) and shoot biomass (+ Arth mean: 0.39 ± 0.03 g; − Arth mean: 0.24 ± 0.03 g; F1,54 = 17.61, p < 0.001), greater soil nitrate concentrations (+ Arth mean: 62.18 ± 4.76 mg NO3− - N kg−1 soil; − Arth mean: 13.06 ± 0.61 mg NO3− - N kg−1 soil; F1,54 = 99.89, p < 0.001), and altered root architecture compared to controls. Soil arthropod communities collected from the two rotational schemes differed significantly in abundance and diversity, but affected wheat growth similarly. Aphid colony growth (+ Arth mean: 30.50 ± 4.06; − Arth mean: 22.13 ± 3.36; χ21,27 = 21.19, p < 0.001), but not plant damage by aphids (+ Arth mean: 2.72 ± 0.17, − Arth mean: 2.69 ± 0.16; F1,27 = 0.02, p > 0.05), was significantly greater on wheat grown in soils with arthropods. Aphids, in turn, modified the effects of soil arthropods on root architecture and increased the abundance of soil arthropods. Wheat grown in soils with arthropods had increased levels of stress- and defense-related phytohormones in response to aphid herbivory, while phytohormones of wheat plants grown in soils without arthropods did not differ with aphid presence. Soil arthropod communities may help plants defend against herbivores aboveground by facilitating phytohormone induction while offsetting costs by increasing soil nutrients and modifying plant growth. By using taxonomically diverse field-collected soil arthropod communities from agroecosystems, this study showed that community-level effects on plant growth are more complex and dynamic than the effects of any single taxon, such as Collembola, illustrating that interactions within communities can produce emergent properties that alter the net effect of soil arthropods on plant growth. The results indicate that community-level effects of soil organisms should be considered as part of sustainable plant production and protection strategies.

Dynamics of soil bio-physicochemical properties under different disturbance regimes in sal forests in western Himalaya, India

Disturbance is a key factor in controlling vegetation diversity, nutrient influx rate, and biochemical cycling in terrestrial forest ecosystems. Limited studies are available on changes in tree diversity, soil nutrients and enzyme activities in response to different intensities of land disturbances in the Himalayan forests. Present study investigated the impact of varying intensities of disturbances on tree diversity and their relationship with soil physical and bio-chemical properties in sal forests, Western Himalayas. Sites were categorized into four different classes of disturbances, namely, No disturbance (ND), Low disturbance (LD), Moderate disturbance (MD), and High disturbance (HD). Composite samples were collected at two depths (0–15 and 15–30 cm) in each plot to investigate soil physical and biochemical properties. Multivariate analyses were conducted to find relationship between tree vegetation and soil physical and biochemical properties. Soil organic carbon (Corg), total nitrogen (Nttl), available phosphorous (Pavl), microbial biomass carbon (Cmic), nitrogen (Nmic), phosphorous (Pmic), and enzymes (dehydrogenase (DHA), Urease, acid and alkaline phosphatase) followed the order: MD > ND > LD > HD. Across disturbances, soil physical and biochemical characteristics significantly (p < 0.05) decreased with increasing soil depths. Across the sites, positive correlation was observed among soil microbial biomass, enzymes, Corg, clay, and moisture. Redundancy analysis (RDA) results revealed that species distribution is essential regulator in the variation of prominent soil variables, viz., nutrients (Nttl and Pavl), Cmic, and DHA across disturbance categories and soil depths. Moreover, variance partitioning analysis (VPA) showed that changes in vegetation composition across disturbance levels explain 13.12 % of the variation in soil biochemical subset higher than soil physicochemical subset. The result illustrated that moderate disturbance increases species composition, soil nutrient properties and microbial activity. These findings would help understand microbial activity and its relationship with disturbances, suggesting site-specific measurements for soil nutrient availability and above-below ground interactions.

Above-belowground interactions in alpine ecosystems on the roof of the world

Above-belowground interactions in alpine ecosystems on the roof of the world

Modulation of above-belowground plant-herbivore interactions by entomopathogenic nematodes

Plants indirectly mediate above-belowground interactions between root- and shoot- herbivores via changes in primary and secondary metabolism. Such effects can cascade up to affect higher trophic level organisms such as predators, however, to what extent predators can in turn influence plant-mediated above-belowground interactions needs to be further elucidated. In this study, we examined the effect of entomopathogenic nematodes (EPNs) (Heterorhabditis bacteriophora and Steinernema carpocapsae) on the interactions between a belowground herbivore, the root-knot nematode (RKN) Meloidogyne arenaria, and an aboveground herbivore, the green-peach aphid Myzus persicae on tobacco (Nicotiana tabacum) plants. We found that the effect of RKNs on aphid population growth and reproduction was negative only when EPNs were inoculated near the rhizosphere. We also observed that the addition of EPNs in the rhizosphere annihilated the positive effect of the aphids on the RKNs feeding on tobacco roots. While aphids and RKNs feeding, respectively, reduced the root and shoot biomass independently of EPNs presence in the rhizosphere, the concentration of glucose and nicotine in tobacco leaves was modified by the presence of EPNs in a species-dependent manner. Our study reveals that tobacco plants detect the presence of EPNs in the rhizosphere and in turn they respond by modifying their interactions with the above- and belowground herbivores. Therefore, soil-dwelling organisms that are not directly associated with the plants can also have community-wide effects that are mediated by changes in plant primary and secondary chemistry.

Applying the Aboveground-Belowground Interaction Concept in Agriculture: Spatio-Temporal Scales Matter

Interactions between aboveground and belowground organisms are important drivers of plant growth and performance in natural ecosystems. Making practical use of such above-belowground biotic interactions offers important opportunities for enhancing the sustainability of agriculture, as it could favor crop growth, nutrient supply, and defense against biotic and abiotic stresses. However, the operation of above-and belowground organisms at different spatial and temporal scales provides important challenges for application in agriculture. Aboveground organisms, such as herbivores and pollinators, operate at spatial scales that exceed individual fields and are highly variable in abundance within growing seasons. In contrast, pathogenic, symbiotic, and decomposer soil biota operate at more localized spatial scales from individual plants to patches of square meters, however, they generate legacy effects on plant performance that may last from single to multiple years. The challenge is to promote pollinators and suppress pests at the landscape and field scale, while creating positive legacy effects of local plant-soil interactions for next generations of plants. Here, we explore the possibilities to improve utilization of above-belowground interactions in agro-ecosystems by considering spatio-temporal scales at which aboveground and belowground organisms operate. We identified that successful integration of above-belowground biotic interactions initially requires developing crop rotations and intercropping systems that create positive local soil legacy effects for neighboring as well subsequent crops. These configurations may then be used as building blocks to design landscapes that accommodate beneficial aboveground communities with respect to their required resources. For successful adoption of above-belowground interactions in agriculture there is a need for context-specific solutions, as well as sound socio-economic embedding.

Plant and soil communities are associated with the response of soil water repellency to environmental stress

A warming climate and expected changes in average and extreme rainfall emphasise the importance of understanding how the land surface routes and stores surface water. The availability and movement of water within an ecosystem is a fundamental control on biological and geophysical activity, and influences many climatic feedbacks. A key phenomenon influencing water infiltration into the land surface is soil hydrophobicity, or water repellency. Despite repellency dictating the speed, volume and pattern of water infiltration, there is still major uncertainty over whether this critical hydrological process is biologically or physicochemically controlled. Here we show that soil water repellency is likely driven by changes in the plant and soil microbial communities in response to environmental stressors. We carried out a field survey in the summers of 2013 to 2016 in a variety of temperate habitats ranging across arable, grassland, forest and bog sites. We found that moderate to extreme repellency occurs in 68% of soils at a national scale in temperate ecosystems, with 92% showing some repellency. Taking a systems approach, we show that a wetter climate and low nutrient availability alter plant, bacterial and fungal community structure, which in turn are associated with increased soil water repellency across a large-scale gradient of soil, vegetation and land-use. The stress tolerance of the plant community and associated changes in soil microbial communities were more closely linked to changes in repellency than soil physicochemical properties. Our results indicate that there are consistent responses to diverse ecosystem stresses that will impact plant and microbial community composition, soil properties, and hydrological behaviour. We suggest that the ability of a biological community to induce such hydrological responses will influence the resilience of the whole ecosystem to environmental stress. This highlights the crucial role of above-belowground interactions in mediating climatic feedbacks and dictating ecosystem health.

Successional trajectories of soil bacterial communities in mine tailings: The role of plant functional traits

Plant species identity is assumed to be a major driver of belowground microbial diversity and composition. However, diagnosing which plant functional traits are responsible for shaping microbial communities remains elusive. Primary succession on barren metalliferous mining substrates was selected as the framework to study above-belowground interactions, and plant functional traits that lead the successional trajectories of soil bacterial communities were identified. The impact of the plant functional group (i.e. trees, shrubs, dwarf shrubs, perennial grasses), a trait integrating the life span and morphological structure, on the bacterial primary succession was monitored. Bacterial diversity and composition was estimated along plant size gradients including over 90 scattered patches ranging from seedlings to mature multispecific patches. Soil bacterial diversity was affected by heavy metals levels and increased towards higher resource availability underneath mature patches, with stress-tolerant heterotrophs and phototrophs being replaced by competitive heterotrophs. The plant functional group modulated these general patterns and shrubs had the greatest impact belowground by inducing the largest increase in soil fertility. Functional traits related to leaf decomposability and root architecture further determined the composition and structure of bacterial communities. These results underline the importance of plant functional traits in the assembly of soil bacterial communities, and can help guiding restoration of degraded lands.

Nitrogen pools and cycles in Tibetan Kobresia pastures depending on grazing

Kobresia grasslands on the Tibetan Plateau comprise the world’s largest pastoral alpine ecosystem. Overgrazing-driven degradation strongly proceeded on this vulnerable grassland, but the mechanisms behind are still unclear. Plants must balance the costs of releasing C to soil against the benefits of accelerated microbial nutrient mineralization, which increases their availability for root uptake. To achieve the effect of grazing on this C-N exchange mechanism, a 15NH4+ field labeling experiment was implemented at grazed and ungrazed sites, with additional treatments of clipping and shading to reduce belowground C input by manipulating photosynthesis. Grazing reduced gross N mineralization rates by 18.7%, similar to shading and clipping. This indicates that shoot removal by grazing decreased belowground C input, thereby suppressing microbial N mining and overall soil N availability. Nevertheless, NH4+ uptake rate by plants at the grazed site was 1.4 times higher than at the ungrazed site, because plants increased N acquisition to meet the high N demands of shoot regrowth (compensatory growth: grazed > ungrazed). To enable efficient N uptake and regrowth, Kobresia plants have developed specific traits (i.e., efficient above-belowground interactions). These traits reflect important mechanisms of resilience and ecosystem stability under long-term moderate grazing in an N-limited environment. However, excessive (over)grazing might imbalance such C-N exchange and amplify plant N limitation, hampering productivity and pasture recovery over the long term. In this context, a reduction in grazing pressure provides a sustainable way to maintain soil fertility, C sequestration, efficient nutrient recycling, and overall ecosystem stability.

(Re)appreciating the role of life history in eco‐evolutionary dynamics

(Re)appreciating the role of life history in eco‐evolutionary dynamics

Editorial: Above-belowground interactions involving plants, microbes and insects

1 Laboratory of Entomology, Wageningen University, Wageningen, Netherlands, Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, Netherlands, 3 R&D Microbiology, Koppert Biological Systems, Berkel en Rodenrijs, Netherlands, Department of Soil Microbiology and Symbiotic Systems, Estacion Experimental del Zaidin, CSIC, Granada, Spain, 5 Laboratory of Functional Ecology, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland, 6 Laboratory of Fundamental and Applied Research in Chemical Ecology, Institute of Biology, University of

Above-belowground interactions govern the course and impact of biological invasions.

Introduction of exotic organisms that subsequently become invasive is considered a serious threat to global biodiversity, and both scientists and nature-conservationists attempt to find explanations and means to meet this challenge. This requires a thorough analysis of the invasion phenomenon in an evolutionary and ecological context; in the case of invasive plants, we must have a major focus on above-belowground interactions. Thus, we discuss different theories that have been proposed to explain the course of invasions through interactions between plants and soil organisms. Further, a thorough analysis of invasion must include a temporal context. Invasions will typically include an initial acute phase, where the invader expands its territory and a later chronic phase where equilibrium is re-established. Many studies fail to make this distinction, which is unfortunate as it makes it impossible to thoroughly understand the invasion of focus. Thus, we claim that invasions fall into two broad categories. Some invasions irreversibly change pools and pathways of matter and energy in the invaded system; even if the abundance of the invader is reduced or it is completely removed, the system will not return to its former state. We use earthworm invasion in North America as a particular conspicuous example of invasive species that irreversibly change ecosystems. However, invasions may also be reversible, where the exotic organism dominates the system for a period, but in the longer term it either disappears, declines or its negative impact decreases. If the fundamental ecosystem structure and flows of energy and matter have not been changed, the system will return to a state not principally different from the original.

Aspects of soil lichen biodiversity and aggregation interact to influence subsurface microbial function

Background and aims Many previous studies have evaluated aboveground–heterotrophic belowground interactions such as plant-soil feedbacks, plant-mycorrhizal fungi associations or plant-actinorhizal symbioses. However, few studies have used biocrusts, which are specialized soil communities of autotrophic cyanobacteria, mosses, lichens and non-photosynthetic fungi and bacteria that are prevalent in drylands worldwide. These communities largely influence ecosystem functioning, and can be used as a model system for studying above-belowground interactions. In this study, we evaluated how biocrusts affect the functional diversity and biomass of microbial diversities beneath biocrusts.

Plant-mediated links between detritivores and aboveground herbivores.

Most studies on plant-mediated above-belowground interactions focus on soil biota with direct trophic links to plant roots such as root herbivores, pathogens, and symbionts. Detritivorous soil fauna, though ubiquitous and present in high abundances and biomasses in soil, are under-represented in those studies. Understanding of their impact on plants is mainly restricted to growth and nutrient uptake parameters. Detritivores have been shown to affect secondary metabolites and defense gene expression in aboveground parts of plants, with potential impacts on aboveground plant-herbivore interactions. The proposed mechanisms range from nutrient mobilization effects and impacts on soil microorganisms to defense induction by passive or active ingestion of roots. Since their negative effects (disruption or direct feeding of roots) may be counterbalanced by their overall beneficial effects (nutrient mobilization), detritivores may not harm, but rather enable plants to respond to aboveground herbivore attacks in a more efficient way. Both more mechanistic and holistic approaches are needed to better understand the involvement of detritivores in plant-mediated above-belowground interactions and their potential for sustainable agriculture.

How can we exploit above-belowground interactions to assist in addressing the challenges of food security?

Can above–belowground interactions help address issues of food security? We address this question in this manuscript, and review the intersection of above–belowground interactions and food security. We propose that above–belowground interactions could address two strategies identified by Godfray etal. (2010): reducing the Yield Gap, and Increasing Production Limits. In particular, to minimize the difference between potential and realized production (The Yield Gap) above–belowground interactions could be manipulated to reduce losses to pests and increase crop growth (and therefore yields). To Increase Production Limits we propose two mechanisms: utilizing intercropping (which uses multiple aspects of above–belowground interactions) and breeding for traits that promote beneficial above–belowground interactions, as well as breeding mutualistic organisms to improve their provided benefit. As a result, if they are managed correctly, there is great potential for above–belowground interactions to contribute to food security.

Root herbivore effects on aboveground multitrophic interactions: patterns, processes and mechanisms.

In terrestrial food webs, the study of multitrophic interactions traditionally has focused on organisms that share a common domain, mainly above ground. In the last two decades, it has become clear that to further understand multitrophic interactions, the barrier between the belowground and aboveground domains has to be crossed. Belowground organisms that are intimately associated with the roots of terrestrial plants can influence the levels of primary and secondary chemistry and biomass of aboveground plant parts. These changes, in turn, influence the growth, development, and survival of aboveground insect herbivores. The discovery that soil organisms, which are usually out of sight and out of mind, can affect plant-herbivore interactions aboveground raised the question if and how higher trophic level organisms, such as carnivores, could be influenced. At present, the study of above-belowground interactions is evolving from interactions between organisms directly associated with the plant roots and shoots (e.g., root feeders - plant - foliar herbivores) to interactions involving members of higher trophic levels (e.g., parasitoids), as well as non-herbivorous organisms (e.g., decomposers, symbiotic plant mutualists, and pollinators). This multitrophic approach linking above- and belowground food webs aims at addressing interactions between plants, herbivores, and carnivores in a more realistic community setting. The ultimate goal is to understand the ecology and evolution of species in communities and, ultimately how community interactions contribute to the functioning of terrestrial ecosystems. Here, we summarize studies on the effects of root feeders on aboveground insect herbivores and parasitoids and discuss if there are common trends. We discuss the mechanisms that have been reported to mediate these effects, from changes in concentrations of plant nutritional quality and secondary chemistry to defense signaling. Finally, we discuss how the traditional framework of fixed paired combinations of root- and shoot-related organisms feeding on a common plant can be transformed into a more dynamic and realistic framework that incorporates community variation in species, densities, space and time, in order to gain further insight in this exciting and rapidly developing field.

Longer days in spring than in autumn accelerate migration speed of passerine birds

Above- and belowground herbivores promote plant diversity when selectively feeding on dominant plant species, but little is known about their combined effects. Using a model system, we show that neutral effects of an aboveground herbivore and positive effects of a belowground herbivore on plant diversity became profoundly negative when adding these herbivores in combination. The non-additive effects were explained by differences in plant preference between the aboveground- and the belowground herbivores and their consequences for indirect interactions among plant species. Simultaneous exposure to aboveground- and belowground herbivores led to plant communities being dominated by a few highly abundant species. As above- and belowground invertebrate herbivores generally differ in their mobility and local distribution patterns, our results strongly suggest that abovegroundbelowground interactions contribute to local spatial heterogeneity of diversity patterns within plant communities. [KEYWORDS: Abovebelowground interactions ; indirect effects ; insect herbivores ; nematodes ; plant diversity]