David A. Wardle

EFFECTS OF BIODIVERSITY ON ECOSYSTEM FUNCTIONING: A CONSENSUS OF CURRENT KNOWLEDGE

Humans are altering the composition of biological communities through a variety of activities that increase rates of species invasions and species extinctions, at all scales, from local to global. These changes in components of the Earths biodiversity cause concern for ethical and aesthetic reasons, but they also have a strong potential to alter ecosystem properties and the goods and services they provide to humanity. Ecological experiments, observations, and theoretical developments show that ecosystem properties depend greatly on biodiversity in terms of the functional characteristics of organisms present in the ecosystem and the distribution and abundance of those organisms over space and time. Species effects act in concert with the effects of climate, resource availability, and disturbance regimes in influencing ecosystem properties. Human activities can modify all of the above factors; here we focus on modification of these biotic controls. The scientific community has come to a broad consensus on many aspects of the re- lationship between biodiversity and ecosystem functioning, including many points relevant to management of ecosystems. Further progress will require integration of knowledge about biotic and abiotic controls on ecosystem properties, how ecological communities are struc- tured, and the forces driving species extinctions and invasions. To strengthen links to policy and management, we also need to integrate our ecological knowledge with understanding of the social and economic constraints of potential management practices. Understanding this complexity, while taking strong steps to minimize current losses of species, is necessary for responsible management of Earths ecosystems and the diverse biota they contain.

Biodiversity loss and its impact on humanity

The most unique feature of Earth is the existence of life, and the most extraordinary feature of life is its diversity. Approximately 9 million types of plants, animals, protists and fungi inhabit the Earth. So, too, do 7 billion people. Two decades ago, at the first Earth Summit, the vast majority of the world’s nations declared that human actions were dismantling the Earth’s ecosystems, eliminating genes, species and biological traits at an alarming rate. This observation led to the question of how such loss of biological diversity will alter the functioning of ecosystems and their ability to provide society with the goods and services needed to prosper.

Trophic Downgrading of Planet Earth

Until recently, large apex consumers were ubiquitous across the globe and had been for millions of years. The loss of these animals may be humankind’s most pervasive influence on nature. Although such losses are widely viewed as an ethical and aesthetic problem, recent research reveals extensive cascading effects of their disappearance in marine, terrestrial, and freshwater ecosystems worldwide. This empirical work supports long-standing theory about the role of top-down forcing in ecosystems but also highlights the unanticipated impacts of trophic cascades on processes as diverse as the dynamics of disease, wildfire, carbon sequestration, invasive species, and biogeochemical cycles. These findings emphasize the urgent need for interdisciplinary research to forecast the effects of trophic downgrading on process, function, and resilience in global ecosystems.

Impacts of biological invasions: what's what and the way forward

Study of the impacts of biological invasions, a pervasive component of global change, has generated remarkable understanding of the mechanisms and consequences of the spread of introduced populations. The growing field of invasion science, poised at a crossroads where ecology, social sciences, resource management, and public perception meet, is increasingly exposed to critical scrutiny from several perspectives. Although the rate of biological invasions, elucidation of their consequences, and knowledge about mitigation are growing rapidly, the very need for invasion science is disputed. Here, we highlight recent progress in understanding invasion impacts and management, and discuss the challenges that the discipline faces in its science and interactions with society.

Spatial soil ecology

Although spatial variability in distributions of soil organisms is generally regarded as random noise, this variability often has a predictable spatial structure. Recent studies have provided evidence that a spatially explicit approach to soil ecology can enable identification of factors that drive the spatial heterogeneity of populations and activities of soil organisms, at scales ranging from millimeters to hundreds of meters. Furthermore, there is increasing evidence that spatial soil ecology can yield new insights with regard to understanding the factors that maintain and regulate soil biodiversity, as well as to how the spatial distributions of soil organisms influence both plant growth and plant community structure.

HERBIVORE‐MEDIATED LINKAGES BETWEEN ABOVEGROUND AND BELOWGROUND COMMUNITIES

Understanding how terrestrial ecosystems function requires a combined aboveground–belowground approach, because of the importance of feedbacks that occur between herbivores, producers, and the decomposer subsystem. In this paper, we identify several mechanisms by which herbivores can indirectly affect decomposer organisms and soil processes through altering the quantity and quality of resources entering the soil. We show that these mechanisms are broadly similar in nature for both foliar and root herbivory, regardless of whether they operate in the short term as a result of physiological responses of individual plants to herbivore attack or long-term following alteration of plant community structure by herbivores and subsequent changes in the quality of litter inputs to soil. We propose that a variety of possible mechanisms is responsible for the idiosyncratic nature of herbivore effects on soil biota and ecosystem function; positive, negative, or neutral effects of herbivory are possible depending upon the balance of these different mechanisms. However, we predict that positive effects of herbivory on soil biota and soil processes are most common in ecosystems of high soil fertility and high consumption rates, whereas negative effects are most common in unproductive ecosystems with low consumption rates. The significance of multiple-species herbivore communities is also emphasized, and we propose that if resource use complementarity among herbivore species or functional groups leads to greater total consumption of phytomass, and thus greater net herbivory, then both positive and negative consequences of increasing herbivore diversity for belowground properties and processes are theoretically possible. Research priorities are highlighted and include a need for comparative studies of herbivore impacts on above- and belowground processes across ecosystems of varying productivity, as well as a need for experimental testing of the influence of antiherbivore defense compounds on complex multitrophic interactions in the rhizosphere and the significance of multiple herbivore species communities on these plant–soil interactions.

A critique of the microbial metabolic quotient (qCO2) as a bioindicator of disturbance and ecosystem development

Abstract The microbial metabolic quotient (respiration-to-biomass ratio) or qCO2, conceptually based on Odums theory of ecosystem succession, is increasingly being used as an index of ecosystem development (during which it supposedly declines) and disturbance (due to which it supposedly increases). We investigated the suitability of qCO2 as an bioindicator using: (1) data from the Franz Josef Glacier chronosequence, spanning over 22,000 years; and (2) data recalculated from published studies. In the Franz Josef sequence, a detectable decline in qCO2 occurred in the first 250 years in both the L-layer and mineral soil layer. However, in the later phases of the succession there was a sharp increase in qCO2 indicating reduced microbial efficiency, which appeared to be related to stress (independent of disturbance) resulting from steady-state conditions. Calculation of qCO2 from three previous studies on disturbance and ecosystem development indicated that this index responds unpredictably and does not necessarily decline during succession. Plant litter decomposition studies demonstrate that while qCO2 usually declines initially, a significant increase in qCO2 can eventually follow on litter types resistant to decomposition. Correlation analysis of each of 24 previous studies demonstrated that qCO2 often declines with increasing pH, clay content and amounts of microbial biomass; these three soil properties are all indicative of varying stress rather than disturbance levels. Reanalysis of data from 16 previous studies indicated that some disturbances such as fertilization and liming can either increase or decrease qCO2 values depending on whether the disturbance alleviates stress (reducing qCO2)or is more extreme than the stress it alleviates (enhancing qCO2). Although cultivation represents a severe disturbance, qCO2 is not predictably enhanced by this perturbation. While qCO2 undoubtedly provides a useful measure of microbial efficiency, our data suggests it has limitations because it can be insensitive to disturbance and ecosystem development, fails to distinguish between effects of disturbance and stress, and does not decline predictably in response to ecosystem development whenever stress increases along successional gradients.

Biodiversity and plant litter : experimental evidence which does not support the view that enhanced species richness improves ecosystem function

There has been a rapidly increasing recent interest in the effects of biological diversity on ecosystem properties, and while some studies have recently concluded that biodiversity improves ecosystem function, these views are based almost entirely on experiments in which species richness of live plants has been varied over all the species diversity treatments. However, most net ecosystem primary productivity eventually enters the decomposition subsystem as plant litter where it has important afterlife effects. Weconducted a field experiment in which litter from 32 plant species (i.e. effects. We conducted a field experiment in which litter from 32 plant species (i.e. eight species of each of four plant functional groups with contrasting litter quality) was collected and placed into litter-bags so that each litter-bag contained between one and eight species; the species which were included in the multiple (>2) species litter-bags were randomly selected. This litter diversity gradient was created within each functional group and across some functional groups. We found large non-additive effects of mixing litter from different species on litter decomposition rates, litter nitrogen contents, rates of nitrogen release from litter and the active microbial biomass present on the litter. The patterns and directions of these non-additive effects were dependent upon both plant functional group and time of harvest, and these effects could be predicted in some instances by the initial litter nitrogen content and the degree of variability of nitrogen content of the component species in the litter-bag. There was no relationship between litter-bag species richness and any of the response variables that we considered, at least between two and eight species. Within plant functional groups our results provide some support for the species redundancy and idiosyncratic hypotheses about how biodiversity alters ecosystem function, but no support for the ecosystem rivet hypothesis or the view that species richness of plant litter is important for ecosystem function. We suggest that increased species diversity of plant litter is less important than that of live plants for determining ecosystem properties (and provide possible reasons for this) and conclude that perceived relationships between biodiversity and ecosystem function may be of diminished significance when the ecological importance of plant litter is fully appreciated.

Linking above-ground and below-ground interactions: How plant responses to foliar herbivory influence soil organisms

Abstract Studies of the effects of above-ground herbivory on soil organisms and decomposer food webs, as well as the processes that they regulate, have largely concentrated on the effects of non-living inputs into the soil, such as dung, urine, body parts and litter. However, there is an increasing body of information which points to the importance of plant physiological responses to herbivory in regulating soil organisms and therefore, implicitly, key soil processes such as decomposition and nutrient mineralisation. In this review we identify the mechanisms by which foliar herbivory may indirectly affect the soil biota and associated below-ground processes through affecting plants, so as to better understand the nature of interactions which exist between above-ground and below-ground biota. We consider two broad pathways by which above-ground foliar herbivory may affect soil biotic communities. The first of these occurs through herbivore effects on patterns of root exudation and carbon allocation. These effects manifest themselves either as short-term changes in plant C allocation and root exudation or as long-term changes in root biomass and morphology. Evidence suggests that these mechanisms positively influence the size and activity of the soil biotic community and may alter the supply of nutrients in the rhizosphere for plant uptake and regrowth. The second of these involves herbivores influencing soil organisms through altering the quality of input of plant litter. Possible mechanisms by which this occurs are through herbivory enhancing nitrogen contents of root litter, through herbivory affecting production of secondary metabolites and concentrations of nutrients in foliage and thus in leaf litter and through selective foliar feeding causing shifts in plant community structure and thus the nature of litter input to the soil. While the effects of herbivory on soil organisms via plant responses may be extremely important, the directions of these effects are often unpredictable because several mechanisms are often involved and because of the inherently complex nature of soil food-web interactions; this creates obvious difficulties in developing general principles about how herbivory affects soil food-webs. Finally, it is apparent that very little is understood on how responses of soil organisms to herbivory affect those ecosystem-level processes regulated by the soil food-web (e.g. decomposition, nutrient mineralisation) and that such information is essential in developing a balanced understanding about how herbivory affects ecosystem function.

Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest

Forest Fungi Boreal forest is one of the worlds major biomes, dominating the subarctic northern latitudes of Europe, Asia, and America. The soils of boreal forest function as a net sink in the global carbon cycle and, hitherto, it has been thought that organic matter in this sink primarily accumulates in the form of plant remains. Clemmensen et al. (p. 1615; see the Perspective by Treseder and Holden) now show that most of the stored carbon in boreal forested islands in Sweden is in fact derived from mycorrhizal mycelium rather than from plant litter. Biochemical and sequencing studies show that carbon sequestration is regulated by functional and phylogenetic shifts in the mycorrhizal fungal community. The results will need to be explicitly considered in models of the role of the boreal forest in the global carbon cycle. Reservoirs of carbon in boreal forest soils are revisited in an island chronosequence, using modeling and molecular approaches. [Also see Perspective by Treseder and Holden] Boreal forest soils function as a terrestrial net sink in the global carbon cycle. The prevailing dogma has focused on aboveground plant litter as a principal source of soil organic matter. Using 14C bomb-carbon modeling, we show that 50 to 70% of stored carbon in a chronosequence of boreal forested islands derives from roots and root-associated microorganisms. Fungal biomarkers indicate impaired degradation and preservation of fungal residues in late successional forests. Furthermore, 454 pyrosequencing of molecular barcodes, in conjunction with stable isotope analyses, highlights root-associated fungi as important regulators of ecosystem carbon dynamics. Our results suggest an alternative mechanism for the accumulation of organic matter in boreal forests during succession in the long-term absence of disturbance.