Linking aboveground and belowground diversity

Aboveground and belowground species interactions drive ecosystem properties at the local scale, but it is unclear how these relationships scale-up to regional and global scales. Here, we discuss our current knowledge of aboveground and belowground diversity links from a global to a local scale. Global diversity peaks towards the Equator for large, aboveground organisms, but not for small (mainly belowground) organisms, suggesting that there are size-related biodiversity gradients in global aboveground-belowground linkages. The generalization of aboveground-belowground diversity relationships, and their role in ecosystem functioning, requires surveys at scales that are relevant to the organisms and ecosystem properties. Habitat sizes and diversity gradients can differ significantly between aboveground and belowground organisms and between ecosystems. These gradients in biodiversity and plant community trait perception need to be acknowledged when studying aboveground-belowground biodiversity linkages.     

Comparative impacts of aboveground and belowground enemies on an invasive thistle

Most research examining how herbivores and pathogens affect performance of invasive plants focuses on aboveground interactions. Although important, the role of belowground communities remains poorly understood, and the relative impact of aboveground and belowground interactions is still debated. As well, most studies of belowground interactions have been carried out in controlled environments, so little is known about the role of these interactions under natural conditions or how these relationships may change across a plant's range. Using the invasive plant Cirsium arvense, we performed a reciprocal transplant experiment to test the relative impacts of above‐ and belowground interactions at three sites across a 509‐km latitudinal gradient in its invaded range in Ontario, Canada. At each site, C. arvense seedlings were protected with above‐ and/or belowground exclosures in a factorial design. Plant performance (biomass, height, stem thickness, number of leaves, length of longest leaf, maximum rhizome length) was greatest when both above‐ and belowground exclosures were applied and lowest when no exclosures were applied. When only one type of exclosure was applied, biomass generally improved more with belowground exclosures than with aboveground exclosures. Despite site‐to‐site differences in foliar damage, root damage, and mesofaunal populations, belowground interactions generally had a greater negative impact on performance than aboveground herbivory alone. These results stress the importance of including both aboveground enemy interactions and plant–soil interactions in studies of plant community dynamics and invader performance.     

Differentiating between effects of invasion and diversity: impacts of aboveground plant communities on belowground fungal communities

Exotic plant species can affect soil microbial communities with the potential for community and ecosystem feedbacks. Yet, separating the effects of exotics from confounded changes in plant community diversity still remains a challenge. We focused on how plant diversity and native or exotic life history affected root fungi because of their significant roles in community and ecosystem processes. Specifically, we examined how fungi colonizing plant roots were affected by plant richness (one, two or four species) replicated across a range of plant community mixtures (natives, exotics, native-exotic mixtures). Fungal biomass inside roots was affected independently by plant richness and mixture, while root fungal community composition was affected only by plant richness. Extraradical networks also increased in size with plant richness. By contrast, plant biomass was a function of plant mixture, with natives consistently smaller than exotics and native-exotic mixtures intermediate. Plant invasions may have an impact on the belowground community primarily through their effects on diversity, at least in the short-term. Disentangling the effects of diversity and invasion on belowground microbial communities can help us to understand both the controllers of belowground resilience and mechanisms of successful colonization and spread of exotic plants.     

An ecosystem organization model explaining diversity at an ecosystem level: Coevolution of primary producer and decomposer

Ecological complexity of species interactions and habitat heterogeneity creates and maintains biodiversity at a trophic level in an ecosystem. This biodiversity simultaneously serves as raw material on which selective forces for organizing ecosystems operate. As a result of this organization process, differences in structure and functioning of ecosystems (diversity at ecosystem level) are generated. Although understanding diversity at the ecosystem level has attracted great interest, recent theoretical advances toward this aim have not been fully appreciated yet. Following Higashi et al. (1993), this report presents a theoretical framework that deals with the organization process of an ecosystem as a consequence of the interactions among its biotic components and their modification of ecological traits. Specifically, the ecosystem organization process of a terrestrial ecosystem is analyzed, including primary producers and decomposers. This model sheds new insight into the differences between temperate and tropical forest ecosystems.     

物种多样性与人工生态系统稳定性探讨

通过40余年对人工群落的长期研究,探讨了一层一种的传统橡胶及茶树种植园,两层两种的橡胶-茶叶、橡胶-咖啡人工群落,三层三种的橡胶-萝芙木-千年健人工群落以及多层多种(5个层次100余种经济植物)的人工雨林的不同结构．从生物量、生产力及经济生产力,对群落环境(小气候、土壤等)的保护及改善能力和对自然灾害(如寒害、风害等)的抵抗力3个方面,比较了单一结构与复合结构在3个系统功能上的差异．结果表明,随着种类增加,层次复杂加大,系统在生物量及生产力上均有明显增加;小气候中随着结构的复杂化加大,相对湿度也随着增加,最高温度降低,最低温度升高,风速减少,土壤流失明显减少,对低温风害的抵抗力加强,表明人工生态系统结构明显影响了系统稳定性．     

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.     

Crop rotational diversity enhances belowground communities and functions in an agroecosystem

Biodiversity loss, an important consequence of agricultural intensification, can lead to reductions in agroecosystem functions and services. Increasing crop diversity through rotation may alleviate these negative consequences by restoring positive aboveground–belowground interactions. Positive impacts of aboveground biodiversity on belowground communities and processes have primarily been observed in natural systems. Here, we test for the effects of increased diversity in an agroecosystem, where plant diversity is increased over time through crop rotation. As crop diversity increased from one to five species, distinct soil microbial communities were related to increases in soil aggregation, organic carbon, total nitrogen, microbial activity and decreases in the carbon‐to‐nitrogen acquiring enzyme activity ratio. This study indicates positive biodiversity–function relationships in agroecosystems, driven by interactions between rotational and microbial diversity. By increasing the quantity, quality and chemical diversity of residues, high diversity rotations can sustain soil biological communities, with positive effects on soil organic matter and soil fertility.     

The variable effects of soil nitrogen availability and insect herbivory on aboveground and belowground plant biomass in an old-field ecosystem

Nutrient availability and herbivory can regulate primary production in ecosystems, but little is known about how, or whether, they may interact with one another. Here, we investigate how nitrogen availability and insect herbivory interact to alter aboveground and belowground plant community biomass in an old-field ecosystem. In 2004, we established 36 experimental plots in which we manipulated soil nitrogen (N) availability and insect abundance in a completely randomized plot design. In 2009, after 6 years of treatments, we measured aboveground biomass and assessed root production at peak growth. Overall, we found a significant effect of reduced soil N availability on aboveground biomass and belowground plant biomass production. Specifically, responses of aboveground and belowground community biomass to nutrients were driven by reductions in soil N, but not additions, indicating that soil N may not be limiting primary production in this ecosystem. Insects reduced the aboveground biomass of subdominant plant species and decreased coarse root production. We found no statistical interactions between N availability and insect herbivory for any response variable. Overall, the results of 6 years of nutrient manipulations and insect removals suggest strong bottom-up influences on total plant community productivity but more subtle effects of insect herbivores on aspects of aboveground and belowground production.     

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。     

Effect of defoliation intensity on aboveground and belowground relative growth rates

According to a simple growth model, grazed and ungrazed plants may have equal absolute growth rates provided that the relative growth rate (RGR) of grazed plants increases exponentially with grazing intensity (proportion of biomass removed). This paper reports results from an experiment designed to determine whether plants of two grass species subjected to a gradient of defoliation intensities, from 0 to 100% aboveground biomass removal, showed such a response. The relationship between aboveground RGR and defoliation intensity was exponential and closely matched the theoretical relationship of equal absolute growth rate. Thus, plants showed the same aboveground growth regardless of defoliation intensity thanks to an exponential stimulation of RGR by defoliation. Belowground RGR was depressed by defoliation of more than 20% of the above-ground biomass. In spite of the drastic modification imposed by the treatments on the relative proportions of different plant parts, after a 42-day recovery period basic allometric relationships, such as root:shoot and leafarea: weight ratios, were not affected by defoliation intensity. Exponential aboveground compensatory responses represent a key feedback process resulting in constant aboveground growth regardless of defoliation intensity and appear to be a simple consequence of strong commitments to certain allometric relationships.     

Phenotypic diversity and stability of ecosystem processes.

The resistance of an ecosystem to perturbations and the speed at which it recovers after the perturbations, which is called resilience, are two important components of ecosystem stability. It has been suggested that biodiversity increases the resilience and resistance of aggregated ecosystem processes. We test this hypothesis using a theoretical model of a nutrient-limited ecosystem in a heterogeneous environment. We investigate the stability properties of the model for its simplest possible configuration, i.e. , a system consisting of two plant species and their associated detritus and local resource depletion zones. Phenotypic diversity within the plant community is described by differences in the nutrient uptake and mortality rates of the two species. The usual measure of resilience characterizes the system as a whole and thus also applies to aggregated ecosystem processes. As a rule this decreases with increased diversity, though under certain conditions it is maximum for an intermediate value of diversity. Resistance is a property that characterizes each system component and process separately. The resistance of the inorganic nutrient pools, hence of nutrient retention in the ecosystem, decreases with increased diversity. The resistance of both total plant biomass and productivity either monotonically decreases or increases over part of the parameter range with increased diversity. Furthermore, it is very sensitive to parameter values. These results support the view that there is no simple relationship between diversity and stability in equilibrium deterministic systems, whether at the level of populations or aggregated ecosystem processes. We discuss these results in relation to recent experiments.     

A temporal approach to linking aboveground and belowground ecology

Ecologists are becoming increasingly aware of the role of aboveground-belowground relationships in controlling ecosystem processes and properties. Here, we review recent studies that show that relationships between aboveground and belowground communities operate over a hierarchy of temporal scales, ranging from days to seasons, to millennia, with differing consequences for ecosystem structure and function. We propose that a temporal framework is crucial to our understanding of the nature and ecological significance of relationships between aboveground and belowground communities.     

Linking aboveground and belowground interactions via induced plant defenses

Plants have a variety of chemical defenses that often increase in concentration following attack by herbivores. Such induced plant responses can occur aboveground, in the leaves, and also belowground in the roots. We show here that belowground organisms can also induce defense responses aboveground and vice versa. Indirect defenses are particularly sensitive to interference by induced feeding activities in the other compartment, and this can disrupt multitrophic interactions. Unravelling the involvement of induced plant responses in the interactions between aboveground and belowground communities associated with plants is likely to benefit from comprehensive metabolomic analyses. Such analyses are likely to contribute to a better understanding of the costs and benefits involved in the selection for induced responses in plants.     

Effects of plant evolution on nutrient cycling couple aboveground and belowground processes

Plant strategies for nutrient acquisition and recycling are key components of ecosystem functioning. How the evolution of such strategies modifies ecosystem functioning and services is still not well understood. In the present work, we aim at understanding how the evolution of different phenotypic traits link aboveground and belowground processes, thereby affecting the functioning of the ecosystem at different scales and in different realms. Using a simple model, we follow the dynamics of a limiting nutrient inside an ecosystem. Considering trade-offs between aboveground and belowground functional traits, we study the effects of the evolution of such strategies on ecosystem properties (amount of mineral nutrient, total plant biomass, dead organic matter, and primary productivity) and whether such properties are maximized. Our results show that when evolution leads to a stable outcome, it minimizes the quantity of nutrient available (following Tilman’s R* rule). We also show that considering the evolution of aboveground and belowground functional traits simultaneously, total plant biomass and primary productivity are not necessarily maximized through evolution. The coupling of aboveground and belowground processes through evolution may largely diminish predicted standing biomass and productivity (extinction may even occur) and impact the evolutionary resilience (i.e., the return time to previous phenotypic states) of the ecosystem in the face of external disturbances. We show that changes in plant biomass and their effects on evolutionary change can be understood by accounting for the links between nutrient uptake and mineralization, and for indirect effects of nutrient uptake on the amount of detritus in the system.     

Effects of aboveground herbivory on plants with long-term belowground biomass storage

Plant tolerance to herbivory is contingent on multiple traits and adaptive mechanisms, which makes it a complex response with ecological implications. In plants with long-term belowground storage, allocation of biomass to inaccessible parts belowground in response to folivory is a well-recognized tolerance mechanism. In temperate regions, spring growth from buried rootstock is common among winter deciduous plants and is often followed by regrowth after defoliation, both of which draws resources from the stored reserves. We developed a mathematical model to analyze this tolerance response in a winter deciduous plant with long-term belowground biomass when it is defoliated by a specialist insect folivore. The model explores how three closely associated traits—(1) belowground biomass allocation to roots, (2) spring utilization of stored reserves, and (3) post-defoliation regrowth capacity—modulate the persistence and dynamics of the plant and herbivore populations. Model results show that allocation to belowground storage is not only a critical component of tolerance but also influences the herbivore population dynamics in ways that depend on how and when plant biomass is allocated and used. Low belowground biomass allocation and high storage utilization combined with poor photosynthetic growth caused extirpation of the plant population by the defoliating insects. Stable coexistence of the plant at low biomass along with its specialist insect required a moderate amount of post-herbivory belowground allocation. High values of belowground biomass allocation, storage utilization, and photosynthetic growth resulted in sustained cycles of the herbivore and plant populations. Interestingly, utilization of stored reserves had conflicting influence on above and belowground biomass, and strongly affected herbivore population dynamics. Our model thus highlights the complexity of tolerance response when it involves multiple traits and mechanisms as evinced by winter deciduous plants. We close by discussing the implications of our findings for the contributions of defoliating insects to biocontrol programs.     

Linking aboveground and belowground communities: the indirect influence of aphid species identity and diversity on a three trophic level soil food web

There has been a growing recent interest in how foliar herbivory may indirectly affect the belowground sub-system, but little is known about the belowground consequences of the identity, species composition or diversity of foliar herbivores. We performed an experiment, utilising model grassland communities containing three plant species, in which treatments consisted of addition of each of eight aphid species in single and in two- four- and eight-species combinations, as well as an aphid-free treatment. While aphid species treatments did not affect total plant biomass or productivity, aphid species identity had important effects on the relative abundance of the three plant species. This in turn affected the abundances of each of three groups of secondary consumers in the soil food web (bacterial- and fungal-feeding nematodes, and enchytraeids) but not primary consumers (microbes, herbivorous nematodes) or tertiary consumers (predatory nematodes). The fact that some trophic levels responded to treatments while others did not is consistent with trophic dynamic theory. Aphid species treatments also affected the community composition within each of the herbivorous, microbe-feeding and top predatory nematode groups, as well as diversity within the first two of these groups. However, aphid species diversity per se had few effects. There were specific instances in which specific aboveground and belowground response variables in two aphid species combinations differed significantly from those in both of the corresponding single aphid species treatments (apparently as a consequence of resource use complementarity between coexisting aphid species), but no instance in which increasing aphid diversity beyond two species had any effect. Our results provide evidence that the identity of aboveground consumers can have effects that propagate through multiple trophic levels in soil food webs in terms of consumer abundance, and composition and diversity within trophic levels.     

Trophic interactions and the relationship between species diversity and ecosystem stability

Several theoretical studies propose that biodiversity buffers ecosystem functioning against environmental fluctuations, but virtually all of these studies concern a single trophic level, the primary producers. Changes in biodiversity also affect ecosystem processes through trophic interactions. Therefore, it is important to understand how trophic interactions affect the relationship between biodiversity and the stability of ecosystem processes. Here we present two models to investigate this issue in ecosystems with two trophic levels. The first is an analytically tractable symmetrical plant-herbivore model under random environmental fluctuations, while the second is a mechanistic ecosystem model under periodic environmental fluctuations. Our analysis shows that when diversity affects net species interaction strength, species interactions--both competition among plants and plant-herbivore interactions--have a strong impact on the relationships between diversity and the temporal variability of total biomass of the various trophic levels. More intense plant competition leads to a stronger decrease or a lower increase in variability of total plant biomass, but plant-herbivore interactions always have a destabilizing effect on total plant biomass. Despite the complexity generated by trophic interactions, biodiversity should still act as biological insurance for ecosystem processes, except when mean trophic interaction strength increases strongly with diversity.     

Rare taxa maintain the stability of crop mycobiomes and ecosystem functions

Plants harbour highly diverse mycobiomes which sustain essential functions for host health and productivity. However, ecological processes that govern the plant–mycobiome assembly, interactions and their impact on ecosystem functions remain poorly known. Here we characterized the ecological role and community assembly of both abundant and rare fungal taxa along the soil–plant continuums (rhizosphere, phyllosphere and endosphere) in the maize–wheat/barley rotation system under different fertilization practices at two contrasting sites. Our results indicate that mycobiome assembly is shaped predominantly by compartment niche and host species rather than by environmental factors. Moreover, crop-associated fungal communities are dominated by few abundant taxa mainly belonging to Sordariomycetes and Dothideomycetes, while the majority of diversity within mycobiomes are represented by rare taxa. For plant compartments, the abundant sub-community is mainly determined by stochastic processes. In contrast, the rare sub-community is more sensitive to host selection and mainly governed by deterministic processes. Furthermore, our results demonstrate that rare taxa play an important role in fungal co-occurrence network and ecosystem functioning like crop yield and soil enzyme activities. These results significantly advance our understanding of crop mycobiome assembly and highlight the key role of rare taxa in sustaining the stability of crop mycobiomes and ecosystem functions.