Legacy effects of aboveground-belowground interactions

Root herbivory can greatly affect the performance of aboveground insects via changes in plant chemistry. These interactions have been studied extensively in experiments where aboveground and belowground insects were feeding on the same plant. However, little is known about how aboveground and belowground organisms interact when they feed on plant individuals that grow after each other in the same soil. We show that feeding by aboveground and belowground insect herbivores on ragwort (Jacobaea vulgaris) plants exert unique soil legacy effects, via herbivore-induced changes in the composition of soil fungi. These changes in the soil biota induced by aboveground and belowground herbivores of preceding plants greatly influenced the pyrrolizidine alkaloid content, biomass and aboveground multitrophic interactions of succeeding plants. We conclude that plant-mediated interactions between aboveground and belowground insects are also important when they do not feed simultaneously on the same plant.     

Bidirectional plant‐mediated interactions between rhizobacteria and shoot‐feeding herbivorous insects: a community ecology perspective

1. Plants interact with various organisms, aboveground as well as belowground. Such interactions result in changes in plant traits with consequences for members of the plant‐associated community at different trophic levels. Research thus far focussed on interactions of plants with individual species. However, studying such interactions in a community context is needed to gain a better understanding.
2. Members of the aboveground insect community induce defences that systemically influence plant interactions with herbivorous as well as carnivorous insects. Plant roots are associated with a community of plant‐growth promoting rhizobacteria (PGPR). This PGPR community modulates insect‐induced defences of plants. Thus, PGPR and insects interact indirectly via plant‐mediated interactions.
3. Such plant‐mediated interactions between belowground PGPR and aboveground insects have usually been addressed unidirectionally from belowground to aboveground. Here, we take a bidirectional approach to these cross‐compartment plant‐mediated interactions.
4. Recent studies show that upon aboveground attack by insect herbivores, plants may recruit rhizobacteria that enhance plant defence against the attackers. This rearranging of the PGPR community in the rhizosphere has consequences for members of the aboveground insect community. This review focusses on the bidirectional nature of plant‐mediated interactions between the PGPR and insect communities associated with plants, including (a) effects of beneficial rhizobacteria via modification of plant defence traits on insects and (b) effects of plant defence against insects on the PGPR community in the rhizosphere. We discuss how such knowledge can be used in the development of sustainable crop‐protection strategies.

     

Effects of soil organisms on aboveground multitrophic interactions are consistent between plant genotypes mediating the interaction

Belowground communities can affect interactions between plants and aboveground insect communities. Such belowground–aboveground interactions are known to depend on the composition of belowground communities, as well as on the plant species that mediates these interactions. However, it is largely unknown whether the effect of belowground communities on aboveground plant–insect interactions also depends on genotypic variation within the plant species that mediates the interaction. To assess whether the outcome of belowground–aboveground interactions can be affected by plant genotype, we selected two white cabbage cultivars [Brassica oleracea L. var. capitata (Brassicaceae)]. From previous studies, it is known that these cultivars differ in their chemistry and belowground and aboveground multitrophic interactions. Belowground, we inoculated soils of the cultivars with either nematodes or microorganisms and included a sterilized soil as a control treatment. Aboveground, we quantified aphid [Brevicoryne brassicae (L.) (Hemiptera: Aphididae)] population development and parasitoid [Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae)] fitness parameters. The cultivar that sustained highest aphid numbers also had the best parasitoid performance. Soil treatment affected aphid population sizes: microorganisms increased aphid population growth. Soil treatments did not affect parasitoid performance. Cultivars differed in their amino acid concentration, leaf relative growth rate, and root, shoot, and phloem glucosinolate composition but showed similar responses of these traits to soil treatments. Consistent with this observation, no interactions were found between cultivar and soil treatment for aphid population growth or parasitoid performance. Overall, the aboveground community was more affected by cultivar, which was associated with glucosinolate profiles, than by soil community.     

First insights into specificity of belowground tritrophic interactions

Tritrophic interactions involving plants, herbivores and parasites have been only recently documented for belowground systems, where entomopathogenic nematodes can exploit root herbivore induced volatile compounds to locate their hosts. Little is known, however, about whether the specificity of such interactions rivals that of the remarkable interactions found in aboveground studies. Using a belowground six-arm olfactometer that allows recording of nematode attraction, specificity of nine economically important species of different trophic levels, including plants, root feeders and entomopathogenic nematodes, was tested. We found that belowground tritrophic interactions are variable at the level of plant volatiles that are induced, elicitation by herbivores, as well as behavior of nematodes. We argue that studies on specificity and variability of belowground responses should be included in plant defense theories and in efforts to exploit tritrophic interactions to improve biological control practices.     

Belowground interactions shift the relative importance of direct and indirect genetic effects

Intraspecific genetic variation can affect decomposition, nutrient cycling, and interactions between plants and their associated belowground communities. However, the effects of genetic variation on ecosystems can also be indirect, meaning that genes in a focal plant may affect ecosystems by altering the phenotype of interacting (i.e., neighboring) individuals. We manipulated genotype identity, species identity, and the possibility of belowground interactions between neighboring Solidago plants. We hypothesized that, because our plants were nitrogen (N) limited, the most important interactions between focal and neighbor plants would occur belowground. More specifically, we hypothesized that the genotypic identity of a plant's neighbor would have a larger effect on belowground biomass than on aboveground biomass, but only when neighboring plants were allowed to interact belowground. We detected species‐ and genotype‐level variation for aboveground biomass and ramet production. We also found that belowground biomass and ramet production depended on the interaction of neighbor genotype identity and the presence or absence of belowground interactions. Additionally, we found that interspecific indirect genetic effects (IIGEs; changes in focal plant traits due to the genotype identity of a heterospecific neighbor) had a greater effect size on belowground biomass than did focal genotype; however, this effect only held in pots that allowed belowground interactions. These results expand the types of natural processes that can be attributed to genotypes by showing that, under certain conditions, a plant's phenotype can be strongly determined by the expression of genes in its neighbor. By showing that IIGEs are dependent upon plants being able to interact belowground, our results also provide a first step for thinking about how genotype‐based, belowground interactions influence the evolutionary outcomes of plant‐neighbor interactions.     

Sequential effects of root and foliar herbivory on aboveground and belowground induced plant defense responses and insect performance

Plants are often simultaneously or sequentially attacked by multiple herbivores and changes in host plants induced by one herbivore can influence the performance of other herbivores. We examined how sequential feeding on the plant Plantago lanceolata by the aboveground herbivore Spodoptera exigua and the belowground herbivore Agriotes lineatus influences plant defense and the performance of both insects. Belowground herbivory caused a reduction in the food consumption by the aboveground herbivore independent of whether it was initiated before, at the same time, or after that of the aboveground herbivore. By contrast, aboveground herbivory did not significantly affect belowground herbivore performance, but significantly reduced the performance of later arriving aboveground conspecifics. Interestingly, belowground herbivores negated negative effects of aboveground herbivores on consumption efficiency of their later arriving conspecifics, but only if the belowground herbivores were introduced simultaneously with the early arriving aboveground herbivores. Aboveground–belowground interactions could only partly be explained by induced changes in an important class of defense compounds, iridoid glycosides (IGs). Belowground herbivory caused a reduction in IGs in roots without affecting shoot levels, while aboveground herbivory increased IG levels in roots in the short term (4 days) but only in the shoots in the longer term (17 days). We conclude that the sequence of aboveground and belowground herbivory is important in interactions between aboveground and belowground herbivores and that knowledge on the timing of exposure is essential to predict outcomes of aboveground–belowground interactions.     

Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea

Plants respond to herbivore attack by rapidly inducing defenses that are mainly regulated by jasmonic acid (JA). Due to the systemic nature of induced defenses, attack by root herbivores can also result in a shoot response and vice versa, causing interactions between above- and belowground herbivores. However, little is known about the molecular mechanisms underlying these interactions. We investigated whether plants respond differently when roots or shoots are induced. We mimicked herbivore attack by applying JA to the roots or shoots of Brassica oleracea and analyzed molecular and chemical responses in both organs. In shoots, an immediate and massive change in primary and secondary metabolism was observed. In roots, the JA-induced response was less extensive and qualitatively different from that in the shoots. Strikingly, in both roots and shoots we also observed differential responses in primary metabolism, development as well as defense specific traits depending on whether the JA induction had been below- or aboveground. We conclude that the JA response is not only tissue-specific but also dependent on the organ that was induced. Already very early in the JA signaling pathway the differential response was observed. This indicates that both organs have a different JA signaling cascade, and that the signal eliciting systemic responses contains information about the site of induction, thus providing plants with a mechanism to tailor their responses specifically to the organ that is damaged.     

Soil legacy effects of plants and drought on aboveground insects in native and range-expanding plant communities

Soils contain biotic and abiotic legacies of previous conditions that may influence plant community biomass and associated aboveground biodiversity. However, little is known about the relative strengths and interactions of the various belowground legacies on aboveground plant–insect interactions. We used an outdoor mesocosm experiment to investigate the belowground legacy effects of range-expanding versus native plants, extreme drought and their interactions on plants, aphids and pollinators. We show that plant biomass was influenced more strongly by the previous plant community than by the previous summer drought. Plant communities consisted of four congeneric pairs of natives and range expanders, and their responses were not unanimous. Legacy effects affected the abundance of aphids more strongly than pollinators. We conclude that legacies can be contained as soil ‘memories’ that influence aboveground plant community interactions in the next growing season. These soil-borne ‘memories’ can be altered by climate warming-induced plant range shifts and extreme drought.     

Putting the ‘upstairs–downstairs’ into ecosystem service: What can aboveground–belowground ecology tell us?

Interactions between spatially-separated aboveground and belowground biota exert important influences on the functioning of terrestrial ecosystems. Plant root exudates and litter inputs affect root-associated and decomposer sub-communities, which, in turn, regulate nutrient availability and plant growth. Ecosystem services theoretically attributed to specific functional components of aboveground or belowground biota are, therefore, influenced by indirect (plant-mediated) interactions with the wider community. Some recent studies have considered aboveground–belowground interactions in a climate change context, with implications for altered ecosystem service provision. This review is a conceptual discussion of the mechanisms by which aboveground–belowground interactions affect specific ecosystem services: control of herbivores by natural enemies, insect pollination and nutrient mineralization by soil decomposers. While some mechanisms are well-characterized, others are poorly understood. Reducing root and shoot herbivory, in addition to the direct plant benefit, indirectly promotes antagonism of the spatially-separate herbivore by its natural enemies. Soil decomposers and mycorrhizal fungi can increase shoot herbivore performance such that control by natural enemies is weakened, or initiate bottom-up trophic cascades which strengthen antagonism of shoot herbivores. Aboveground herbivory generally stimulates nutrient cycling by decomposers. Root herbivory and mycorrhizal association both appear to increase floral attractiveness to insect pollinators. Mechanisms reflect alterations to plant growth, nutritional quality and chemical defenses. Climate change has considerable potential to alter aboveground–belowground interactions, with largely unexplored implications for biological control, pollination and soil nutrient cycling.     

Effects of decomposers and herbivores on plant performance and aboveground plant-insect interactions

Most ecologists acknowledge that plants are subject to complex interactions between both below- and aboveground dwelling animals. However, these complex interactions are seldomly investigated simultaneously. In a factorial common garden experiment we tested single and combined effects of decomposers, root herbivores and leaf herbivores on the growth, flower visitation, and abundance of naturally colonizing aphids and parasitoids on wild mustard ( Sinapis arvensis ). We found that the individual presence of either root herbivores or decomposers resulted in increased aphid abundance, demonstrating that the same aboveground plant–insect interaction can be released by different belowground processes. Enhanced aphid densities caused higher numbers of parasitoids. Furthermore, decomposers increased plant growth and plant fitness (measured as the number of seeds produced), indicating that mustard may benefit from nutrients provided by decomposers, regardless whether plants are attacked by root herbivores or leaf herbivores, or both simultaneously. More flower visits were observed in plants attacked by root herbivores but without leaf herbivores than in plants with both herbivores, suggesting that root herbivory can modify flower attractivity to pollinators. Our results suggest that patterns in plant–insect interactions above the ground are not only affected by aboveground factors but also by a wealth of different belowground processes mediated by the plant.     

Effects of a belowground mutualism on an aboveground mutualism

Studies of multitrophic interactions between below‐ and aboveground communities have generally focused on soil organisms and antagonists of plant shoots and leaves (herbivores). Despite the widespread occurrence of plant mutualists below‐ and aboveground which can occur on the same host plant, the potential for interactions between them has not been considered. Here we demonstrate that aboveground plant mutualists, insect pollinators, are strongly influenced by belowground plant mutualists, arbuscular mycorrhizal fungi. The presence of arbuscular mycorrhizal fungi in the roots of Chamerion angustifolium increased pollinator visitation and per cent seed set of this plant in the field by up to two times compared with non‐mycorrhizal plants. We propose that interactions between belowground and aboveground mutualisms are widespread and may play important functional roles in populations and communities.     

Belowground ABA boosts aboveground production of DIMBOA and primes induction of chlorogenic acid in maize

Plants are important mediators between above- and belowground herbivores. Consequently, interactions between root and shoot defenses can have far-reaching impacts on entire food webs. We recently reported that infestation of maize roots by larvae of the beetle Diabrotica virgifera virgifera induced shoot resistance against herbivores and pathogens. Root herbivory also enhanced aboveground DIMBOA and primed for enhanced induction of chlorogenic acid, two secondary metabolites that have been associated with plant stress resistance. Interestingly, the plant hormone abscisic acid (ABA) emerged as a putative long-distance signal in the regulation of these systemic defenses. In this addendum, we have investigated the role of root-derived ABA in aboveground regulation of DIMBOA and the phenolic compounds chlorogenic acid, caffeic and ferulic acid. Furthermore, we discuss the relevance of ABA in relation to defense against the leaf herbivore Spodoptera littoralis. Soil-drench treatment with ABA mimicked root herbivore-induced accumulation of DIMBOA in the leaves. Similarly, ABA mimicked aboveground priming of chlorogenic acid production, causing augmented induction of this compound after subsequent shoot attack by S. littoralis caterpillars. These findings confirm our notion that ABA acts as an important signal in the regulation of aboveground defenses during belowground herbivory. However, based on our previous finding that ABA alone is not sufficient to trigger aboveground resistance against S. littoralis caterpillars, our results also suggest that the ABA-inducible effects on DIMBOA and chlorogenic acid are not solely responsible for root herbivore-induced resistance against S. littoralis.Key words: induced resistance, Spodoptera littoralis, Zea mays, Diabrotica virgifera, DIMBOA, chlorogenic acid, absisic acid, priming     

Developing X-ray Computed Tomography to non-invasively image 3-D root systems architecture in soil

Background

The positive relationship between biodiversity and ecosystem functioning (BEF) is due mainly to complementarity between species. Most BEF studies primarily focused on plant interactions; however, plants are embedded in a dense network of multitrophic interactions above and below the ground, which are likely to play a crucial role in BEF relationships.

Scope

In the present review I point out the relevance of aboveground–belowground interactions as a source of complementarity effects in grassland biodiversity experiments. A review of the current knowledge on the role of decomposers, arbuscular mycorrhizal fungi, rhizobia, plant growth promoting rhizobacteria, invertebrate ecosystem engineers, herbivores, pathogens and predators in biodiversity experiments, indicates that soil biota can drive both positive and negative complementarity between plant species via a multitude of mechanisms.

Conclusions

I pose four main processes by which aboveground–belowground interactions determine positive complementarity effects: enlarging biotope space, mediating legume effects, increasing plant community resistance, and maintaining plant diversity. By contrast, soil biota may also reinforce negative complementarity effects by competing with plants for nutrients or by exerting herbivore or pathogen pressure, thereby reducing community productivity. Thus, considering aboveground–belowground interactions as well as interactions between antagonistic and mutualistic consumers may improve the mechanistic understanding of complementarity effects in plant diversity–ecosystem functioning experiments and should inspire future research.     

Chemical defense,mycorrhizal colonization and growth responses in <Emphasis Type="Italic">Plantago lanceolata</Emphasis> L.

Allelochemicals defend plants against herbivore and pathogen attack aboveground and belowground. Whether such plant defenses incur ecological costs by reducing benefits from plant mutualistic symbionts is largely unknown. We explored a potential trade-off between inherent plant chemical defense and belowground mutualism with arbuscular mycorrhizal fungi (AMF) in Plantago lanceolata L., using plant genotypes from lines selected for low and high constitutive levels of the iridoid glycosides (IG) aucubin and catalpol. As selection was based on IG concentrations in leaves, we first examined whether IG concentrations covaried in roots. Root and leaf IG concentrations were strongly positively correlated among genotypes, indicating genetic interdependence of leaf and root defense. We then found that root AMF arbuscule colonization was negatively correlated with root aucubin concentration. This negative correlation was observed both in plants grown with monocultures of Glomus intraradices and in plants colonized from whole-field soil inoculum. Overall, AMF did not affect total biomass of plants; an enhancement of initial shoot biomass was offset by a lower root biomass and reduced regrowth after defoliation. Although the precise effects of AMF on plant biomass varied among genotypes, plants with high IG levels and low AMF arbuscule colonization in roots did not produce less biomass than plants with low IG and high AMF arbuscule colonization. Therefore, although an apparent trade-off was observed between high root chemical defense and AMF arbuscule colonization, this did not negatively affect the growth responses of the plants to AMF. Interestingly, AMF induced an increase in root aucubin concentration in the high root IG genotype of P. lanceolata. We conclude that AMF does not necessarily stimulate plant growth, that direct plant defense by secondary metabolites does not necessarily reduce potential benefits from AMF, and that AMF can enhance concentrations of root chemical defenses, but that these responses are plant genotype-dependent.     

Root and shoot jasmonic acid induced plants differently affect the performance of Bemisia tabaci and its parasitoid Encarsia formosa

Plants employ both direct and indirect defenses to protect themselves from attacks by herbivores and pathogens. To date most aboveground and belowground interaction studies have focused on interactions between plants and leaf-chewing herbivores, while the plant defence on the performance of phloem-feeding insects, induced by above- and belowground interaction, has been less explored. Here, jasmonic acid (JA) was used to mimic herbivore-induced responses in Chinese broccoli (Brassica oleracea var. alboglabra) roots (RJA) and shoots (SJA). The effects of JA-induced plant defenses on the performance of the phloem-feeding whitefly, Bemisia tabaci, and its aphelinid parasitoid Encarsia formosa were investigated. The results indicated that SJA induction has a much larger negative effect on B. tabaci than RJA: nymphs develop slower and have a lower survivorship. Also, females live shorter and have a lower fecundity on SJA plants compared to those on RJA and untreated control (CON) plants. The intrinsic rate of increase (r_m) of B. tabaci on SJA plants was 0.089, which was significantly lower than those on CON and RJA plants (0.115 and 0.104, respectively). The parasitoid E. formosa, on the other hand, shows a significantly faster development when parasitizing whitefly hosts feeding on SJA plants, whereas parasitism rate, longevity and fecundity were similar to those on RJA and CON plants. The current study reveals that plants induced with exogenous JA vary in both their resistance to whitefly and suitability for parasitoids, depending on the organ to which the JA was applied. Root and shoot JA applications also have contrasting effects on the phloem-feeding insect B. tabaci and its parasitoid, that is, SJA induction leads to more negative effects on whitefly performance than RJA induction, but its parasitoid performs better on hosts reared on SJA plants. These results show that top-down and bottom-up processes governing herbivore populations on Chinese broccoli are working in concert to increase plant resistance when plants are induced by SJA application.     

Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals

It is widely reported that plants emit volatile compounds when they are attacked by herbivorous insects, which may be used by parasitoids and predators to locate their host or prey. The study of herbivore-induced plant volatiles and their role in mediating interactions between plants, herbivores and their natural enemies have been primarily based on aboveground systems, generally ignoring the potential interactions between above and belowground infochemical- and food webs. This study examines whether herbivory by Delia radicum feeding on roots of Brassica nigra (black mustard) affects the behaviour of Cotesia glomerata , a parasitoid of the leaf herbivore Pieris brassicae , mediated by changes in plant volatiles. In a semi-field experiment with root-damaged and root-undamaged plants C. glomerata prefers to oviposit in hosts feeding on root-undamaged plants. In addition, in a flight-cage experiment the parasitoid also prefers to search for hosts on plants without root herbivores. Plants exposed to root herbivory were shown to emit a volatile blend characterized by high levels of specific sulphur volatile compounds, which are reported to be highly toxic for insects, combined with low levels of several compounds, i.e. beta-farnesene, reported to act as attractants for herbivorous and carnivorous insects. Our results provide evidence that the foraging behaviour of a parasitoid of an aboveground herbivore can be influenced by belowground herbivores through changes in the plant volatile blend. Such indirect interactions may have profound consequences for the evolution of host selection behaviour in parasitoids, and may play an important role in the structuring and functioning of communities.     

植物地上部与地下部的诱导防御反应研究综述

地球上大多数植物对病虫害的侵袭具有诱导防御反应。植物地上部与地下部之间存在着密切的生理生态关系,因此,地上部处理是否影响地下部的防御反应以及地下部处理是否影响地上部的防御反应,进而分别影响到地下部和地上部生物的行为成为当前研究的热点。本文系统地综述了地上部机械损伤、害虫取食、信号物质处理对植物地下部防御反应及生物行为影响以及地下部机械损伤、害虫取食、信号物质处理对植物地上部防御反应及生物行为影响的研究进展,并在此基础上提出了未来该领域值得进一步研究的方向,以期为深入研究植物地上部与地下部诱导防御间的相互关系提供科学依据。     

Interrelated effects of mycorrhiza and free‐living nitrogen fixers cascade up to aboveground herbivores

Aboveground plant performance is strongly influenced by belowground microorganisms, some of which are pathogenic and have negative effects, while others, such as nitrogen‐fixing bacteria and arbuscular mycorrhizal fungi, usually have positive effects. Recent research revealed that belowground interactions between plants and functionally distinct groups of microorganisms cascade up to aboveground plant associates such as herbivores and their natural enemies. However, while functionally distinct belowground microorganisms commonly co‐occur in the rhizosphere, their combined effects, and relative contributions, respectively, on performance of aboveground plant‐associated organisms are virtually unexplored. Here, we scrutinized and disentangled the effects of free‐living nitrogen‐fixing (diazotrophic) bacteria Azotobacter chroococcum (DB) and arbuscular mycorrhizal fungi Glomus mosseae (AMF) on host plant choice and reproduction of the herbivorous two‐spotted spider mite Tetranychus urticae on common bean plants Phaseolus vulgaris. Additionally, we assessed plant growth, and AMF and DB occurrence and density as affected by each other. Both AMF alone and DB alone increased spider mite reproduction to similar levels, as compared to the control, and exerted additive effects under co‐occurrence. These effects were similarly apparent in host plant choice, that is, the mites preferred leaves from plants with both AMF and DB to plants with AMF or DB to plants grown without AMF and DB. DB, which also act as AMF helper bacteria, enhanced root colonization by AMF, whereas AMF did not affect DB abundance. AMF but not DB increased growth of reproductive plant tissue and seed production, respectively. Both AMF and DB increased the biomass of vegetative aboveground plant tissue. Our study breaks new ground in multitrophic belowground–aboveground research by providing first insights into the fitness implications of plant‐mediated interactions between interrelated belowground fungi–bacteria and aboveground herbivores.     

Above‐ and belowground herbivory jointly impact defense and seed dispersal traits in Taraxacum officinale

Plants are able to cope with herbivores by inducing defensive traits or growth responses that allow them to reduce or avoid the impact of herbivores. Since above‐ and belowground herbivores differ substantially in life‐history traits, for example feeding types, and their spatial distribution, it is likely that they induce different responses in plants. Moreover, strong interactive effects on defense and plant growth are expected when above‐ and belowground herbivores are jointly present. The strengths and directions of these responses have been scarcely addressed in the literature. Using Taraxacum officinale, the root‐feeding nematode Meloidogyne hapla and the locust Schistocerca gregaria as a model species, we examined to what degree above‐ and belowground herbivory affect (1) plant growth responses, (2) the induction of plant defensive traits, that is, leaf trichomes, and (3) changes in dispersal‐related seed traits and seed germination. We compared the performance of plants originating from different populations to address whether plant responses are conserved across putative different genotypes. Overall, aboveground herbivory resulted in increased plant biomass. Root herbivory had no effect on plant growth. Plants exposed to the two herbivores showed fewer leaf trichomes than plants challenged only by one herbivore and consequently experienced greater aboveground herbivory. In addition, herbivory had effects that reached beyond the individual plant by modifying seed morphology, producing seeds with longer pappus, and germination success.     

Empirical and theoretical challenges in aboveground–belowground ecology

A growing body of evidence shows that aboveground and belowground communities and processes are intrinsically linked, and that feedbacks between these subsystems have important implications for community structure and ecosystem functioning. Almost all studies on this topic have been carried out from an empirical perspective and in specific ecological settings or contexts. Belowground interactions operate at different spatial and temporal scales. Due to the relatively low mobility and high survival of organisms in the soil, plants have longer lasting legacy effects belowground than aboveground. Our current challenge is to understand how aboveground–belowground biotic interactions operate across spatial and temporal scales, and how they depend on, as well as influence, the abiotic environment. Because empirical capacities are too limited to explore all possible combinations of interactions and environmental settings, we explore where and how they can be supported by theoretical approaches to develop testable predictions and to generalise empirical results. We review four key areas where a combined aboveground–belowground approach offers perspectives for enhancing ecological understanding, namely succession, agro-ecosystems, biological invasions and global change impacts on ecosystems. In plant succession, differences in scales between aboveground and belowground biota, as well as between species interactions and ecosystem processes, have important implications for the rate and direction of community change. Aboveground as well as belowground interactions either enhance or reduce rates of plant species replacement. Moreover, the outcomes of the interactions depend on abiotic conditions and plant life history characteristics, which may vary with successional position. We exemplify where translation of the current conceptual succession models into more predictive models can help targeting empirical studies and generalising their results. Then, we discuss how understanding succession may help to enhance managing arable crops, grasslands and invasive plants, as well as provide insights into the effects of global change on community re-organisation and ecosystem processes.