Towards a mechanistic understanding of the impacts of nitrogen deposition on producer-consumer interactions.

Nitrogen (N) deposition has increased substantially since the second half of the 20th century due to human activities. This increase of reactive N into the biosphere has major implications for ecosystem functioning, including primary production, soil and water chemistry and producer community structure and diversity. Increased N deposition is also linked to the decline of insects observed over recent decades. However, we currently lack a mechanistic understanding of the effects of high N deposition on individual fitness, species richness and community structure of both invertebrate and vertebrate consumers. Here, we review the effects of N deposition on producer-consumer interactions, focusing on five existing ecological frameworks: C:N:P ecological stoichiometry, trace element ecological stoichiometry, nutritional geometry, essential micronutrients and allelochemicals. We link reported N deposition-mediated changes in producer quality to life-history strategies and traits of consumers, to gain a mechanistic understanding of the direction of response in consumers. We conclude that high N deposition influences producer quality via eutrophication and acidification pathways. This makes oligotrophic poorly buffered ecosystems most vulnerable to significant changes in producer quality. Changes in producer quality between the reviewed frameworks are often interlinked, complicating predictions of the effects of high N deposition on producer quality. The degree and direction of fitness responses of consumers to changes in producer quality varies among species but can be explained by differences in life-history traits and strategies, particularly those affecting species nutrient intake regulation, mobility, relative growth rate, host-plant specialisation, ontogeny and physiology. To increase our understanding of the effects of N deposition on these complex mechanisms, the inclusion of life-history traits of consumer species in future study designs is pivotal. Based on the reviewed literature, we formulate five hypotheses on the mechanisms underlying the effects of high N deposition on consumers, by linking effects of nutritional ecological frameworks to life-history strategies. Importantly, we expect that N-deposition-mediated changes in producer quality will result in a net decrease in consumer community as well as functional diversity. Moreover, we anticipate an increased risk of outbreak events of a small subset of generalist species, with concomitant declines in a multitude of specialist species. Overall, linking ecological frameworks with consumer life-history strategies provides a mechanistic understanding of the impacts of high N deposition on producer-consumer interactions, which can inform management towards more effective mitigation strategies.

Initial soil community drives heathland fungal community trajectory over multiple years through altered plant-soil interactions.

Dispersal limitation, biotic interactions, and environmental filters interact to drive plant and fungal community assembly, but their combined effects are rarely investigated. This study examines how different heathland plant and fungal colonization scenarios realized via three biotic treatments - addition of mature heathland-derived sod, addition of hay, and no additions - affect soil fungal community development over 6 yr along a manipulated pH gradient in a large-scale experiment starting from an agricultural, topsoil removed state. Our results show that both biotic and abiotic (pH) treatments had a persistent influence on the development of fungal communities, but that sod additions diminished the effect of abiotic treatments through time. Analysis of correlation networks between soil fungi and plants suggests that the reduced effect of pH in the sod treatment, where both soil and plant propagules were added, might be due to plant-fungal interactions since the sod additions caused stronger, more specific, and more consistent connections compared with the no addition treatment. Based on these results, we suggest that the initial availability of heathland fungal and plant taxa, which reinforce each other, can significantly steer further fungal community development to an alternative configuration, overriding the otherwise prominent effect of abiotic (pH) conditions.

Ecological impacts of atmospheric pollution and interactions with climate change in terrestrial ecosystems of the Mediterranean Basin: Current research and future directions.

Mediterranean Basin ecosystems, their unique biodiversity, and the key services they provide are currently at risk due to air pollution and climate change, yet only a limited number of isolated and geographically-restricted studies have addressed this topic, often with contrasting results. Particularities of air pollution in this region include high O3 levels due to high air temperatures and solar radiation, the stability of air masses, and dominance of dry over wet nitrogen deposition. Moreover, the unique abiotic and biotic factors (e.g., climate, vegetation type, relevance of Saharan dust inputs) modulating the response of Mediterranean ecosystems at various spatiotemporal scales make it difficult to understand, and thus predict, the consequences of human activities that cause air pollution in the Mediterranean Basin. Therefore, there is an urgent need to implement coordinated research and experimental platforms along with wider environmental monitoring networks in the region. In particular, a robust deposition monitoring network in conjunction with modelling estimates is crucial, possibly including a set of common biomonitors (ideally cryptogams, an important component of the Mediterranean vegetation), to help refine pollutant deposition maps. Additionally, increased attention must be paid to functional diversity measures in future air pollution and climate change studies to establish the necessary link between biodiversity and the provision of ecosystem services in Mediterranean ecosystems. Through a coordinated effort, the Mediterranean scientific community can fill the above-mentioned gaps and reach a greater understanding of the mechanisms underlying the combined effects of air pollution and climate change in the Mediterranean Basin.

Evidence for differential effects of reduced and oxidised nitrogen deposition on vegetation independent of nitrogen load.

Nitrogen (N) deposition impacts natural and semi-natural ecosystems globally. The responses of vegetation to N deposition may, however, differ strongly between habitats and may be mediated by the form of N. Although much attention has been focused on the impact of total N deposition, the effects of reduced and oxidised N, independent of the total N deposition, have received less attention. In this paper, we present new analyses of national monitoring data in the UK to provide an extensive evaluation of whether there are differences in the effects of reduced and oxidised N deposition across eight habitat types (acid, calcareous and mesotrophic grasslands, upland and lowland heaths, bogs and mires, base-rich mires, woodlands). We analysed data from 6860 plots in the British Countryside Survey 2007 for effects of total N deposition and N form on species richness, Ellenberg N values and grass:forb ratio. Our results provide clear evidence that N deposition affects species richness in all habitats except base-rich mires, after factoring out correlated explanatory variables (climate and sulphur deposition). In addition, the form of N in deposition appears important for the biodiversity of grasslands and woodlands but not mires and heaths. Ellenberg N increased more in relation to NHx deposition than NOy deposition in all but one habitat type. Relationships between species richness and N form were habitat-specific: acid and mesotrophic grasslands appear more sensitive to NHx deposition while calcareous grasslands and woodlands appeared more responsive to NOy deposition. These relationships are likely driven by the preferences of the component plant species for oxidised or reduced forms of N, rather than by soil acidification.

Soil phosphorus constrains biodiversity across European grasslands.

Nutrient pollution presents a serious threat to biodiversity conservation. In terrestrial ecosystems, the deleterious effects of nitrogen pollution are increasingly understood and several mitigating environmental policies have been developed. Compared to nitrogen, the effects of increased phosphorus have received far less attention, although some studies have indicated that phosphorus pollution may be detrimental for biodiversity as well. On the basis of a dataset covering 501 grassland plots throughout Europe, we demonstrate that, independent of the level of atmospheric nitrogen deposition and soil acidity, plant species richness was consistently negatively related to soil phosphorus. We also identified thresholds in soil phosphorus above which biodiversity appears to remain at a constant low level. Our results indicate that nutrient management policies biased toward reducing nitrogen pollution will fail to preserve biodiversity. As soil phosphorus is known to be extremely persistent and we found no evidence for a critical threshold below which no environmental harm is expected, we suggest that agro-environmental schemes should include grasslands that are permanently free from phosphorus fertilization.

Ammonium as a driving force of plant diversity and ecosystem functioning: observations based on 5 years' manipulation of N dose and form in a Mediterranean ecosystem.

Enhanced nitrogen (N) availability is one of the main drivers of biodiversity loss and degradation of ecosystem functions. However, in very nutrient-poor ecosystems, enhanced N input can, in the short-term, promote diversity. Mediterranean Basin ecosystems are nutrient-limited biodiversity hotspots, but no information is available on their medium- or long-term responses to enhanced N input. Since 2007, we have been manipulating the form and dose of available N in a Mediterranean Basin maquis in south-western Europe that has low ambient N deposition (<4 kg N ha(-1) yr(-1)) and low soil N content (0.1%). N availability was modified by the addition of 40 kg N ha(-1) yr(-1) as a 1∶1 NH4Cl to (NH4)2SO4 mixture, and 40 and 80 kg N ha(-1) yr(-1) as NH4NO3. Over the following 5 years, the impacts on plant composition and diversity (richness and evenness) and some ecosystem characteristics (soil extractable N and organic matter, aboveground biomass and % of bare soil) were assessed. Plant species richness increased with enhanced N input and was more related to ammonium than to nitrate. Exposure to 40 kg NH4+-N ha(-1) yr(-1) (alone and with nitrate) enhanced plant richness, but did not increase aboveground biomass; soil extractable N even increased under 80 kg NH4NO3-N ha(-1) yr(-1) and the % of bare soil increased under 40 kg NH4+-N ha(-1) yr(-1). The treatment containing less ammonium, 40 kg NH4NO3-N ha(-1) yr(-1), did not enhance plant diversity but promoted aboveground biomass and reduced the % of bare soil. Data suggest that enhanced NHy availability affects the structure of the maquis, which may promote soil erosion and N leakage, whereas enhanced NOx availability leads to biomass accumulation which may increase the fire risk. These observations are relevant for land use management in biodiverse and fragmented ecosystems such as the maquis, especially in conservation areas.

Global assessment of the effects of terrestrial acidification on plant species richness.

This study estimates the potential losses of vascular plant species richness due to terrestrial acidification for different world's biomes. We used empirical occurrence data of 2409 species from 140 studies and estimated the relative species richness - pH response curves using logistic regressions. The regressions were then used to quantify the fraction of species that are potentially lost due to soil pH changes. Although we found considerable variability within biomes, out results show that the pH at which species richness was maximized was found to be the lowest in (sub)tropical forests (pH = 4.1) and the highest in deserts (pH = 7.4). We also found that (sub)tropical moist forests are highly sensitive to decreases of in soil pH below 4.1. This study can be coupled with existing atmospheric deposition models to quantify the risk of species richness loss following soil acidification.

Ecosystem responses to reduced and oxidised nitrogen inputs in European terrestrial habitats.

While it is well established that ecosystems display strong responses to elevated nitrogen deposition, the importance of the ratio between the dominant forms of deposited nitrogen (NH(x) and NO(y)) in determining ecosystem response is poorly understood. As large changes in the ratio of oxidised and reduced nitrogen inputs are occurring, this oversight requires attention. One reason for this knowledge gap is that plants experience a different NH(x):NO(y) ratio in soil to that seen in atmospheric deposits because atmospheric inputs are modified by soil transformations, mediated by soil pH. Consequently species of neutral and alkaline habitats are less likely to encounter high NH(4)(+) concentrations than species from acid soils. We suggest that the response of vascular plant species to changing ratios of NH(x):NO(y) deposits will be driven primarily by a combination of soil pH and nitrification rates. Testing this hypothesis requires a combination of experimental and survey work in a range of systems.

The impact of nitrogen deposition on acid grasslands in the Atlantic region of Europe.

A survey of 153 acid grasslands from the Atlantic biogeographic region of Europe indicates that chronic nitrogen deposition is changing plant species composition and soil and plant-tissue chemistry. Across the deposition gradient (2-44 kg N ha(-1) yr(-1)) grass richness as a proportion of total species richness increased whereas forb richness decreased. Soil C:N ratio increased, but soil extractable nitrate and ammonium concentrations did not show any relationship with nitrogen deposition. The above-ground tissue nitrogen contents of three plant species were examined: Agrostis capillaris (grass), Galium saxatile (forb) and Rhytidiadelphus squarrosus (bryophyte). The tissue nitrogen content of neither vascular plant species showed any relationship with nitrogen deposition, but there was a weak positive relationship between R. squarrosus nitrogen content and nitrogen deposition. None of the species showed strong relationships between above-ground tissue N:P or C:N and nitrogen deposition, indicating that they are not good indicators of deposition rate.

Nitrogen deposition threatens species richness of grasslands across Europe.

Evidence from an international survey in the Atlantic biogeographic region of Europe indicates that chronic nitrogen deposition is reducing plant species richness in acid grasslands. Across the deposition gradient in this region (2-44 kg N ha(-1) yr(-1)) species richness showed a curvilinear response, with greatest reductions in species richness when deposition increased from low levels. This has important implications for conservation policies, suggesting that to protect the most sensitive grasslands resources should be focussed where deposition is currently low. Soil pH is also an important driver of species richness indicating that the acidifying effect of nitrogen deposition may be contributing to species richness reductions. The results of this survey suggest that the impacts of nitrogen deposition can be observed over a large geographical range.

Effects of nitrogen enrichment on coastal dune grassland: a mesocosm study.

Mesocosms filled with dune sand were planted with graminoid (Calamagrostis epigejos, Carex arenaria) and herbaceous species (Carlina vulgaris, Galium verum). Strong effects of nitrogen addition on the vegetation were found within two to three years. The above-ground biomass of C. epigejos and C. arenaria increased at deposition rates between 10 and 80 kg N ha(-1) yr(-1). Both grasses were limited by N. In latter stages P limitation was suggested for C. arenaria. At high N-levels, C. epigejos dominated the vegetation within two years. C. vulgaris and G. verum declined drastically as a result of increased competition for light by the highly competitive grass C. epigejos. It is concluded that increased (ambient) N inputs are of major importance for the increased dominance of tall grasses in stable dune grasslands.

Decline of acid-sensitive plant species in heathland can be attributed to ammonium toxicity in combination with low pH.

The effects of increasing ammonium concentrations in combination with different pH levels were studied on five heathland plant species to determine whether their occurrence and decline could be attributed to ammonium toxicity and/or pH levels. Plants were grown in growth media amended with four different ammonium concentrations (10, 100, 500 and 1000 micromol l(-1)) and two pH levels resembling acidified (pH 3.5 or 4) and weakly buffered (pH 5 or 5.5) situations. Survival of Antennaria dioica and Succisa pratensis was reduced by low pH in combination with high ammonium concentrations. Biomass decreased with increased ammonium concentrations and decreasing pH levels. Internal pH of the plants decreased with increasing ammonium concentrations. Survival of Calluna vulgaris, Deschampsia flexuosa and Gentiana pneumonanthe was not affected by ammonium. Moreover, biomass increased with increasing ammonium concentrations. Biomass production of G. pneumonanthe reduced at low pH levels. A decline of acid-sensitive species in heathlands was attributed to ammonium toxicity effects in combination with a low pH.

Nitrous oxide emission and denitrification in chronically nitrate-loaded riparian buffer zones.

Riparian buffer zones are known to reduce diffuse N pollution of streams by removing and modifying N from agricultural runoff. Denitrification, often identified as the key N removal process, is also considered as a major source of the greenhouse gas nitrous oxide (N2O). The risks of high N2O emissions during nitrate mitigation and the environmental controls of emissions have been examined in relatively few riparian zones and the interactions between controls and emissions are still poorly understood. Our objectives were to assess the rates of N2O emission from riparian buffer zones that receive large loads of nitrate, and to evaluate various factors that are purported to control N emissions. Denitrification, nitrification, and N2O emissions were measured seasonally in grassland and forested buffer zones along first-order streams in The Netherlands. Lateral nitrate loading rates were high, up to 470 g N m(-2) yr(-1). Nitrogen process rates were determined using flux chamber measurements and incubation experiments. Nitrous oxide emissions were found to be significantly higher in the forested (20 kg N ha(-1) yr(-1)) compared with the grassland buffer zone (2-4 kg N ha(-1) yr(-1)), whereas denitrification rates were not significantly different. Higher rates of N2O emissions in the forested buffer zone were associated with higher nitrate concentrations in the ground water. We conclude that N transformation by nitrate-loaded buffer zones results in a significant increase of greenhouse gas emission. Considerable N2O fluxes measured in this study indicate that Intergovernmental Panel on Climate Change methodologies for quantifying indirect N2O emissions have to distinguish between agricultural uplands and riparian buffer zones in landscapes receiving large N inputs.

A comparative study on nutrient cycling in wet heathland ecosystems : II. Litter decomposition and nutrient mineralization.

The concept of the relative nutrient requirement (L n) that was introduced in the first paper of this series is used to analyse the effects of the dominant plant population on nutrient cycling and nutrient mineralization in wet heathland ecosystems. A distinction is made between the effect that the dominant plant species has on (1) the distribution of nutrients over the plant biomass and the soil compartment of the ecosystem and (2) the recirculation rate of nutrients. The first effect of the dominant plant species can be calculated on the basis of the δ/k ratio (which is the ratio of the relative mortality to the decomposition constant). The second effect can be analysed using the relative nutrient requirement (L n). The mass loss and the changes in the amounts of N and P in decomposing above-ground and below-ground litter produced by Erica tetralix and Molinia caerulea were measured over three years. The rates of mass loss from both above-ground and below-ground litter of Molinia were higher than those from Erica litter. After an initial leaching phase, litter showed either a net release or a net immobilization of nitrogen or phosphorus that depended on the initial concentrations of these nutrients. At the same sites, mineralization of nitrogen and phosphorus were measured for two years both in communities dominated by Molinia and in communities dominated by Erica. There were no clear differences in the nitrogen mineralization, but in one of the two years, phosphate mineralization in the Molinia-community was significantly higher. On the basis of the theory that was developed, mineralization rates and ratios between amounts of nutrients in plant biomass and in the soil were calculated on the basis of parameters that were independently measured. There was a reasonable agreement between predicted and measured values in the Erica-communities. In the Molinia-communities there were large differences between calculated and measured values, which was explained by the observation that the soil organic matter in these ecosystems still predominantly consisted of Erica-remains.