Showing papers by "Richard D. Bardgett published in 2008"

The unseen majority: Soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems

Abstract: Microbes are the unseen majority in soil and comprise a large portion of lifes genetic diversity. Despite their abundance, the impact of soil microbes on ecosystem processes is still poorly understood. Here we explore the various roles that soil microbes play in terrestrial ecosystems with special emphasis on their contribution to plant productivity and diversity. Soil microbes are important regulators of plant productivity, especially in nutrient poor ecosystems where plant symbionts are responsible for the acquisition of limiting nutrients. Mycorrhizal fungi and nitrogenfixing bacteria are responsible for c. 5‐20% (grassland and savannah) to 80% (temperate and boreal forests) of all nitrogen, and up to 75% of phosphorus, that is acquired by plants annually. Free-living microbes also strongly regulate plant productivity, through the mineralization of, and competition for, nutrients that sustain plant productivity. Soil microbes, including microbial pathogens, are also important regulators of plant community dynamics and plant diversity, determining plant abundance and, in some cases, facilitating invasion by exotic plants. Conservative estimates suggest that c. 20 000 plant species are completely dependent on microbial symbionts for growth and survival pointing to the importance of soil microbes as regulators of plant species richness on Earth. Overall, this review shows that soil microbes must be considered as important drivers of plant diversity and productivity in terrestrial ecosystems.

Plant functional traits and soil carbon sequestration in contrasting biomes

Abstract: Plant functional traits control a variety of terrestrial ecosystem processes, including soil carbon storage which is a key component of the global carbon cycle. Plant traits regulate net soil carbon storage by controlling carbon assimilation, its transfer and storage in belowground biomass, and its release from soil through respiration, fire and leaching. However, our mechanistic understanding of these processes is incomplete. Here, we present a mechanistic framework, based on the plant traits that drive soil carbon inputs and outputs, for understanding how alteration of vegetation composition will affect soil carbon sequestration under global changes. First, we show direct and indirect plant trait effects on soil carbon input and output through autotrophs and heterotrophs, and through modification of abiotic conditions, which need to be considered to determine the local carbon sequestration potential. Second, we explore how the composition of key plant traits and soil biota related to carbon input, release and storage prevail in different biomes across the globe, and address the biome-specific mechanisms by which plant trait composition may impact on soil carbon sequestration. We propose that a trait-based approach will help to develop strategies to preserve and promote carbon sequestration.

Microbial contributions to climate change through carbon cycle feedbacks.

Abstract: There is considerable interest in understanding the biological mechanisms that regulate carbon exchanges between the land and atmosphere, and how these exchanges respond to climate change. An understanding of soil microbial ecology is central to our ability to assess terrestrial carbon cycle–climate feedbacks, but the complexity of the soil microbial community and the many ways that it can be affected by climate and other global changes hampers our ability to draw firm conclusions on this topic. In this paper, we argue that to understand the potential negative and positive contributions of soil microbes to land–atmosphere carbon exchange and global warming requires explicit consideration of both direct and indirect impacts of climate change on microorganisms. Moreover, we argue that this requires consideration of complex interactions and feedbacks that occur between microbes, plants and their physical environment in the context of climate change, and the influence of other global changes which have the capacity to amplify climate-driven effects on soil microbes. Overall, we emphasize the urgent need for greater understanding of how soil microbial ecology contributes to land–atmosphere carbon exchange in the context of climate change, and identify some challenges for the future. In particular, we highlight the need for a multifactor experimental approach to understand how soil microbes and their activities respond to climate change and consequences for carbon cycle feedbacks.

Drying and rewetting effects on soil microbial community composition and nutrient leaching

Abstract: The effects of a dry-rewetting event (D/RW) on soil microbial properties and nutrient release by leaching from two soils taken from adjacent grasslands with different histories of management intensity were studied. These were a low-productivity grassland, with no history of fertilizer application and a high-productivity grassland with a history of high fertilizer application, referred to as unimproved and improved grassland, respectively. The use of phospholipid fatty acid analysis (PLFA) revealed that the soil of the unimproved grassland had a significantly greater microbial biomass, and a greater abundance of fungi relative to bacteria than did the improved grassland. Soils from both grasslands were maintained at 55% water holding capacity (WHC) or dried to 10% WHC and rewetted to 55% WHC, and then sampled on days 1, 3, 9, 16, 30 and 50 after rewetting. The D/RW stress significantly reduced microbial biomass carbon (C), fungal PLFA and the ratio of fungal-to-bacterial PLFA in both soils. In contrast, D/RW increased microbial activity, but had no effect on total PLFA and bacterial PLFA in either soil. Microbial biomass nitrogen (N) was reduced significantly by D/RW in both soils, but especially in those of the improved grassland. In terms of nutrient leaching, the D/RW stress significantly increased concentrations of dissolved organic C and dissolved organic N in leachates taken from the improved soil only. This treatment increased the concentration of dissolved inorganic N in leachate of both soils, but this effect was most pronounced in the improved soil. Overall, our data show that D/RW stress leads to greater nutrient leaching from improved than from unimproved grassland soils, which have a greater microbial biomass and abundance of fungi relative to bacteria. This finding supports the notion that soils with more fungal-rich communities are better able to retain nutrients under D/RW than are their intensively managed counterparts with lower fungal to bacterial ratios, and that D/RW can enhance nutrient leaching with potential implications for water quality.

Do plant species with different growth strategies vary in their ability to compete with soil microbes for chemical forms of nitrogen

Abstract: We used dual labelled stable isotope (13C and 15N) techniques to examine how grassland plant species with different growth strategies vary in their ability to compete with soil microbes for different chemical forms of nitrogen (N), both inorganic and organic. We also tested whether some plant species might avoid competition by preferentially using different chemical forms of N than microbes. This was tested in a pot experiment where monocultures of five co-existing grassland species, namely the grasses Agrostis capillaris, Anthoxanthum odoratum, Nardus stricta, Deschampsia flexuosa and the herb Rumex acetosella, were grown in field soil from an acid semi-natural temperate grassland. Our data show that grassland plant species with different growth strategies are able to compete effectively with soil microbes for most N forms presented to them, including inorganic N and amino acids of varying complexity. Contrary to what has been found in strongly N limited ecosystems, we did not detect any differential uptake of N on the basis of chemical form, other than that shoot tissue of fast-growing plant species was more enriched in 15N from ammonium-nitrate and glycine, than from more complex amino acids. Shoot tissue of slow-growing species was equally enriched in 15N from all these N forms. However, all species tested, least preferred the most complex amino acid phenylalanine, which was preferentially used by soil microbes. We also found that while fast-growing plants took up more of the added N forms than slow-growing species, this variation was not related to differences in the ability of plants to compete with microbes for N forms, as hypothesised. On the contrary, we detected no difference in microbial biomass or microbial uptake of 15N between fast and slow-growing plant species, suggesting that plant traits that regulate nutrient capture, as opposed to plant species-specific interactions with soil microbes, are the main factor controlling variation in uptake of N by grassland plant species. Overall, our data provide insights into the interactions between plants and soil microbes that influence plant nitrogen use in grassland ecosystems.

Influence of disturbance and nitrogen addition on plant and soil animal diversity in grassland

Abstract: Two key determinants of biological diversity that have been examined in aboveground and aquatic systems are productivity, or resource supply, and physical disturbance. In this study, we examined how these factors interact under field conditions to determine belowground diversity using microarthropods (mites and Collembola) as our test community. To do this, we established a field manipulation experiment consisting of crossed, continuous gradients of nitrogenous (N) fertilizer addition (up to 240 kg N ha−1) and disturbance (imitated trampling by cattle) to produce a gradient of soil nutrient availability and disturbance. Due to the relatively short-term nature of our study (i.e. 2 years), we only detected minimal changes in plant diversity due to the experimental manipulations; in the longer term we would expect to detect changes in plant diversity that could potentially impact on soil fauna. However, disturbance reduced, and additions of N increased, aboveground biomass, reflecting the potential effects of these manipulations on resource availability for soil fauna. We found that disturbance strongly reduced the abundance, diversity, and species richness of oribatid mites and Collembola, but had little effect on predatory mites (Mesostigmata). In contrast, N addition, and therefore resource availability, had little effect on microarthropod community structure, but did increase mesostigmatan mite richness and collembolan abundance at high levels of disturbance. Oribatid community structure was mostly influenced by disturbance, whereas collembolan and mesostigmatan diversity were responsive to N addition, suggesting bottom-up control. That maximal species richness of microarthropod groups overall occurred in undisturbed plots, suggests that the microarthropod community was negatively affected by disturbance. We found no change in microarthropod species richness with high N additions, where plant productivity was greatest, indicating that soil biotic communities are unlikely to be strongly regulated by competition. We conclude that the diversity of soil animals is best explained as a combination of their many varied life history tactics, phenology and the heterogeneity of soils that enable so many species to co-exist.

Direct and indirect effects of nitrogen deposition on litter decomposition

Abstract: Elevated nitrogen (N) deposition can affect litter decomposition directly, by raising soil N availability and the quantity and quality of litter inputs, and indirectly by altering plant community composition. We investigated the importance of these controls on litter decomposition using litter bags placed in annual herb based microcosm ecosystems that had been subject to two rates of N deposition (which raised soil inorganic N availability and stimulated litter inputs) and two planting regimes, namely the plant species compositions of low and high N deposition environments. In each microcosm, we harvested litter bags of 10 annual plant species, over an 8-week period, to determine mass loss from decomposition. Our data showed that species differed greatly in their decomposability, but that these differences were unlikely to affect decomposition at the ecosystem level because there was no correlation between a species’ decomposability and its response to N deposition (measured as population seed production under high N, relative to low N, deposition). Litter mass loss was 2% greater in high N deposition microcosms. Using a comprehensive set of measurements of the microcosm soil environments, we found that the most statistically likely explanation for this effect was increased soil enzyme activity (cellobiosidase, β-glucosidase and β-xylosidase), which appears to have occurred in response to a combination of raised soil inorganic N availability and stimulated litter inputs. Our data indicate that direct effects of N deposition on litter input and soil N availability significantly affected decomposition but indirect effects did not. We argue that indirect effects of changes to plant species composition could be stronger in natural ecosystems, which often contain a greater diversity of plant functional types than those considered here.

Nitrogen enrichment modifies plant community structure via changes to plant–soil feedback

Abstract: We tested the hypothesis that N enrichment modifies plant-soil feedback relationships, resulting in changes to plant community composition. This was done in a two-phase glasshouse experiment. In the first phase, we grew eight annual plant species in monoculture at two levels of N addition. Plants were harvested at senescence and the effect of each species on a range of soil properties was measured. In the second phase, the eight plant species were grown in multi-species mixtures in the eight soils conditioned by the species in the first phase, at both levels of N addition. At senescence, species performance was measured as aboveground biomass. We found that in the first phase, plant species identity strongly influenced several soil properties, including microbial and protist biomass, soil moisture content and the availability of several soil nutrients. Species effects on the soil were mostly independent of N addition and several were strongly correlated with plant biomass. In the second phase, both the performance of individual species and overall community structure were influenced by the interacting effects of the species identity of the previous soil occupant and the rate of N addition. This indicates that N enrichment modified plant-soil feedback. The performance of two species correlated with differences in soil N availability that were generated by the species formerly occupying the soil. However, negative feedback (poorer performance on the soil of conspecifics relative to that of heterospecifics) was only observed for one species. In conclusion, we provide evidence that N enrichment modifies plant-soil feedback relationships and that these modifications may affect plant community composition. Field testing and further investigations into which mechanisms dominate feedback are required before we fully understand how and when feedback processes determine plant community responses to N enrichment.

The response of plant diversity to ecosystem retrogression: evidence from contrasting long‐term chronosequences

Abstract: Following catastrophic disturbances, succession and vegetation development occur, but in the prolonged absence of these disturbances a decline (retrogressive) phase follows in which nutrient availability and tree biomass declines considerably. We measured plant diversity across six long-term chronosequences that each included retrogressive stages in Australia, New Zealand, Alaska, Hawaii and Sweden. In contrast to theories predicting negative or hump-shaped responses of tree diversity to biomass or soil fertility, tree species richness often peaked coincidentally with tree basal area (a surrogate of tree biomass), and declined during retrogression. Similar patterns were found regardless of whether or not species richness estimates were rarefraction-adjusted to correct for variation in stem densities across plots. The Shannon-Weiner diversity index sometimes showed the same pattern, but in two chronosequences was least when tree basal area peaked; this was driven by the domination of total basal area by single tree species in both cases. The decline in tree diversity during retrogression was often associated with reduced relative amounts of total phosphorus in soil. In contrast, total vascular plant species richness often increased during retrogression. These results demonstrate that forests with high tree diversity and biomass do not persist indefinitely in the long-term absence of catastrophic disturbance, and that similar patterns occur across the boreal, temperate and subtropical zones.

Long‐term change in vegetation and soil microbial communities during the phased restoration of traditional meadow grassland

Abstract: 1. Restoration of high plant species diversity to sites where it has been reduced by intensive grassland management requires identification of appropriate management regimes. Understanding the combinatorial effects of management on above-ground vegetation and below-ground microbial communities will inform management prescriptions on how best to increase plant diversity, restore rare vegetation types and achieve agri-environmental objectives. 2. Changes in vegetation and soil microbial community structure are described from the second phase of a 1990-2004 field trial that investigated the interacting effects of fertilizer and farmyard manure (FYM) treatments imposed after 1998, in the context of previous hay-cut date and seed-addition treatments. 3. Hay-cut date was the main factor influencing plant species composition in phase 1, whereas FYM was the dominant factor in phase 2. 4. Poa trivialis and Lolium perenne increased in abundance with FYM application, particularly in combination with mineral fertilizer, and particularly in 2002 after the 2001 foot and mouth epidemic. The lowest Ellenberg fertility scores were associated with absence of FYM and mineral fertilizer but with addition of seed. 5. The highest plant species diversity in phase 2 was associated with seed addition and the absence of mineral fertilizer, an effect that had probably persisted from phase 1. Progressive development of the target traditional meadow vegetation occurred through phase 2. 6. Fungal:bacterial (F:B) ratios, a measure of changes in the relative abundance of fungi and bacteria in the microbial community, generally increased from 1996 to 2004, and were particularly high in the seed-addition treatments and in the absence of fertilizer. Here the high F:B ratios were associated with species (including legumes) typical of traditionally managed mesotrophic grassland in northern England. 7. Synthesis and applications. These results demonstrate that biodiversity goals for upland meadows need to plan beyond the typical 5-10-year management agreement period of agri-environment schemes. Combination treatments, in which seed addition is vital, alongside appropriate fertilizer, FYM, hay-cut date and grazing regimes, are needed for grassland restoration. However, even after 14 years the most effective treatment combinations had still not restored the target species composition and diversity. The demonstrated change in soil microbial communities, linked to the growth of legumes, might be important to facilitate future increases in plant diversity.

The effect of transgenic nematode resistance on non-target organisms in the potato rhizosphere

Abstract: 1. Plant-parasitic nematodes are important pests of agriculture and transgenic plants with potential for nematode control are currently being developed. The expression of cysteine proteinase inhibitors (cystatins) in potato confers partial resistance to potato-cyst nematode (PCN). Here, we used field studies to test for effects of cystatin-expressing potato on non-target soil organisms. 2. Microbial community structure, soil microarthropods and litter decomposition were studied during two growing seasons. In the second year, nematode control options of cystatin-expressing plants and an oxime carbamate nematicide application were compared for their non-target effects. 3. In the first year, the transgenic lines had no effect on the abundance, evenness or metabolic activity of the soil microbial community as determined by ester-linked phospholipid fatty acid analysis (PLFA). However, one transgenic line (D6/7) influenced the structure of the soil microbial community. PLFA suggested it favoured fungal growth relative to bacterial growth during the latter parts of the growing season. A second transgenic line (D5/13) was more effective against PCN. It reduced the abundance of the fungal fatty acid 18:2omega6 in late season, suggesting a suppression of fungal growth. 4. In the second year PLFA analysis suggested microbial abundance was reduced by 15% and 23% in the nematicide and transgenic treatments, respectively, relative to the control. Nematicidal treatment reduced the bacterial fraction of the microbial community, whereas the transgenic plants suppressed both the bacterial and fungal community components. 5. The observed changes in soil microbial community structure did not result in changes in the rate of leaf litter decomposition. 6. The transgenic lines had no significant effect on the abundance of soil microarthropods or free-living nematodes. 7. The study is the first stage of a risk assessment of the impact of transgenic nematode resistance on non-target soil organisms. It has highlighted the importance of including currently used management options when studying the effect of transgenic plants on non-target organisms. Both nematicide use and the transgenic plants affected components of the soil microbial community. However, the changes brought about by the two treatments were not sufficient to affect soil functioning, as measured by rates of litter decomposition.

Impacts of Grazing and Browsing by Large Herbivores on Soils and Soil Biological Properties

Abstract: Herbivores can have a wide range of effects on terrestrial ecosystems. Some of these effects are direct, such as the removal and consumption of herbage—which can vary some 100-fold across terrestrial ecosystems from less than 1% to greater than 60% (McNaughton et al. 1989)—treading on soil and vegetation, and the return of excreta (Floate 1981). Herbivores also have important indirect effects on ecosystems, altering rates of nutrient cycling and changing nutrient availability to plants (Bardgett and Wardle 2003; Bardgett 2005). These indirect effects of herbivores on ecosystems are mediated by feedbacks that occur between plants and below-ground decomposer communities, and especially soil microbes, which play a central role regulating nutrient availability to plants. This chapter examines some of the many ways that above-ground herbivores might indirectly influence ecosystem properties through their influence on below-ground organisms and processes. We also examine how these changes in soil biological properties may in turn feed back to affect above-ground primary production in both positive and negative ways. The chapter will highlight the different mechanisms by which herbivores affect decomposer organisms and their activities over various temporal and spatial scales, ranging from short-term responses at the individual plant level, to longterm responses at the level of the plant community. The effects of different types of herbivory, namely grazing and browsing, on soil biological properties will also be discussed. The mechanisms highlighted will be illustrated with specific examples from a range of different ecosystems, thereby providing a global perspective on herbivore effects on soils.

Large old trees influence patterns of δ13C and δ15N in forests

Abstract: Large old trees are the dominant primary producers of native pine forest, but their influence on spatial patterns of soil properties and potential feedback to tree regeneration in their neighbourhood is poorly understood. We measured stable isotopes of carbon (13C) and nitrogen (15N) in soil and litter taken from three zones of influence (inner, middle and outer zone) around the trunk of freestanding old Scots pine (Pinus sylvestris L.) trees, to determine the trees' influence on below-ground properties. We also measured 15N and 13C in wood cores extracted from the old trees and from regenerating trees growing within their three zones of influence. We found a significant and positive gradient in soil 15N from the inner zone, nearest to the tree centre, to the outer zone beyond the tree crown. This was probably caused by the higher input of 15N-depleted litter below the tree crown. In contrast, the soil 13C did not change along the gradient of tree influence. Distance-related trends, although weak, were visible in the wood 15N and 13C of regenerating trees. Moreover, the wood 15N of small trees showed a weak negative relationship with soil N content in the relevant zone of influence. Our results indicate that large old trees control below-ground conditions in their immediate surroundings, and that stable isotopes might act as markers for the spatial and temporal extent of these below-ground effects.