Linda H. Pardo

Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis

Atmospheric nitrogen (N) deposition is a recognized threat to plant diversity in temperate and northern parts of Europe and North America. This paper assesses evidence from field experiments for N deposition effects and thresholds for terrestrial plant diversity protection across a latitudinal range of main categories of ecosystems, from arctic and boreal systems to tropical forests. Current thinking on the mechanisms of N deposition effects on plant diversity, the global distribution of G200 ecoregions, and current and future (2030) estimates of atmospheric N-deposition rates are then used to identify the risks to plant diversity in all major ecosystem types now and in the future. This synthesis paper clearly shows that N accumulation is the main driver of changes to species composition across the whole range of different ecosystem types by driving the competitive interactions that lead to composition change and/or making conditions unfavorable for some species. Other effects such as direct toxicity of nitrogen gases and aerosols, long-term negative effects of increased ammonium and ammonia availability, soil-mediated effects of acidification, and secondary stress and disturbance are more ecosystem- and site-specific and often play a supporting role. N deposition effects in mediterranean ecosystems have now been identified, leading to a first estimate of an effect threshold. Importantly, ecosystems thought of as not N limited, such as tropical and subtropical systems, may be more vulnerable in the regeneration phase, in situations where heterogeneity in N availability is reduced by atmospheric N deposition, on sandy soils, or in montane areas. Critical loads are effect thresholds for N deposition, and the critical load concept has helped European governments make progress toward reducing N loads on sensitive ecosystems. More needs to be done in Europe and North America, especially for the more sensitive ecosystem types, including several ecosystems of high conservation importance. The results of this assessment show that the vulnerable regions outside Europe and North America which have not received enough attention are ecoregions in eastern and southern Asia (China, India), an important part of the mediterranean ecoregion (California, southern Europe), and in the coming decades several subtropical and tropical parts of Latin America and Africa. Reductions in plant diversity by increased atmospheric N deposition may be more widespread than first thought, and more targeted studies are required in low background areas, especially in the G200 ecoregions.

Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability.

Ratios of nitrogen (N) isotopes in leaves could elucidate underlying patterns of N cycling across ecological gradients. To better understand global-scale patterns of N cycling, we compiled data on foliar N isotope ratios (delta(15)N), foliar N concentrations, mycorrhizal type and climate for over 11,000 plants worldwide. Arbuscular mycorrhizal, ectomycorrhizal, and ericoid mycorrhizal plants were depleted in foliar delta(15)N by 2 per thousand, 3.2 per thousand, 5.9 per thousand, respectively, relative to nonmycorrhizal plants. Foliar delta(15)N increased with decreasing mean annual precipitation and with increasing mean annual temperature (MAT) across sites with MAT >or= -0.5 degrees C, but was invariant with MAT across sites with MAT < -0.5 degrees C. In independent landscape-level to regional-level studies, foliar delta(15)N increased with increasing N availability; at the global scale, foliar delta(15)N increased with increasing foliar N concentrations and decreasing foliar phosphorus (P) concentrations. Together, these results suggest that warm, dry ecosystems have the highest N availability, while plants with high N concentrations, on average, occupy sites with higher N availability than plants with low N concentrations. Global-scale comparisons of other components of the N cycle are still required for better mechanistic understanding of the determinants of variation in foliar delta(15)N and ultimately global patterns in N cycling.

Effects of nitrogen deposition and empirical nitrogen critical loads for ecoregions of the United States

Human activity in the last century has led to a significant increase in nitrogen (N) emissions and atmospheric deposition. This N deposition has reached a level that has caused or is likely to cause alterations to the structure and function of many ecosystems across the United States. One approach for quantifying the deposition of pollution that would be harmful to ecosystems is the determination of critical loads. A critical load is defined as the input of a pollutant below which no detrimental ecological effects occur over the long-term according to present knowledge. The objectives of this project were to synthesize current research relating atmospheric N deposition to effects on terrestrial and freshwater ecosystems in the United States, and to estimate associated empirical N critical loads. The receptors considered included freshwater diatoms, mycorrhizal fungi, lichens, bryophytes, herbaceous plants, shrubs, and trees. Ecosystem impacts included: (1) biogeochemical responses and (2) individual species, population, and community responses. Biogeochemical responses included increased N mineralization and nitrification (and N availability for plant and microbial uptake), increased gaseous N losses (ammonia volatilization, nitric and nitrous oxide from nitrification and denitrification), and increased N leaching. Individual species, population, and community responses included increased tissue N, physiological and nutrient imbalances, increased growth, altered root : shoot ratios, increased susceptibility to secondary stresses, altered fire regime, shifts in competitive interactions and community composition, changes in species richness and other measures of biodiversity, and increases in invasive species.

Long-Term Integrated Studies Show Complex and Surprising Effects of Climate Change in the Northern Hardwood Forest

Evaluations of the local effects of global change are often confounded by the interactions of natural and anthropogenic factors that overshadow the effects of climate changes on ecosystems. Long-term watershed and natural elevation gradient studies at the Hubbard Brook Experimental Forest and in the surrounding region show surprising results demonstrating the effects of climate change on hydrologic variables (e.g., evapotranspiration, streamflow, soil moisture); the importance of changes in phenology on water, carbon, and nitrogen fluxes during critical seasonal transition periods; winter climate change effects on plant and animal community composition and ecosystem services; and the effects of anthropogenic disturbances and land-use history on plant community composition. These studies highlight the value of long-term integrated research for assessments of the subtle effects of changing climate on complex ecosystems.

Critical loads as a policy tool for protecting ecosystems from the effects of air pollutants

Framing the effects of air pollutants on ecosystems in terms of a “critical load” provides a meaningful approach for research scientists to communicate policy-relevant science to air-quality policy makers and natural resource managers. A critical-loads approach has been widely used to shape air-pollutant control policy in Europe since the 1980s, yet has only rarely been applied in the US. Recently, however, interest in applying a critical-loads approach to managing sulfur and nitrogen air pollutants in the US has been growing, as evidenced by several recent conferences, a new critical-loads sub-committee within the National Atmospheric Deposition Program, and nascent efforts by several federal agencies to apply critical loads to land management. Here, we describe the critical-loads concept, including some of its limitations, and indicate how critical loads can better inform future air-pollutant control policy in the US.

Using Nitrogen Isotope Ratios to Assess Terrestrial Ecosystems at Regional and Global Scales

Advances in technology have made extensive surveys of 15N natural abundances in terrestrial ecosystems feasible at the regional and even global scale within the last decade. To date, such surveys have included measurements of plant (typically foliage) or soil δ15N. Correlations between plant δ15N and measures of N saturation have been reported in regional surveys of both Europe and North America, with plant tissue δ15N values increasing under N saturating conditions. Global analyses have shown positive relationships between both soil and foliar δ15N values and mean annual temperature and negative relationships between δ15N values and precipitation. Several factors can drive variations in plant and soil 15N natural abundances, thereby presenting challenges to the use of 15N for inferring nitrogen cycling patterns across large scales. These include: (1) prior land-use, which may leave long-lasting (decades to centuries) imprints on soil and hence plant δ15N; (2) variability in δ15N among species within a given site, which can mask patterns across sites; (3) mycorrhizal associations, which may fractionate strongly under certain conditions; (4) effects of climate, especially precipitation regime, which may influence the value of and temporal variability in plant δ15N. Despite these complicating factors, δ15N surveys at large scales may provide insight into N cycling patterns and processes controlling these patterns in terrestrial ecosystems; maps of δ15N in precipitation may also provide a useful tool for interpreting some patterns in terrestrial ecosystem N dynamics.

Calcium Additions and Microbial Nitrogen Cycle Processes in a Northern Hardwood Forest

Evaluating, and possibly ameliorating, the effects of base cation depletion in forest soils caused by acid deposition is an important topic in the northeastern United States. We added 850 kg Ca ha−1 as wollastonite (CaSiO3) to an 11.8-ha watershed at the Hubbard Brook Experimental Forest (HBEF), a northern hardwood forest in New Hampshire, USA, in fall 1999 to replace calcium (Ca) leached from the ecosystem by acid deposition over the past 6 decades. Soil microbial biomass carbon (C) and nitrogen (N) concentrations, gross and potential net N mineralization and nitrification rates, soil solution and stream chemistry, soil:atmosphere trace gas (CO2, N2O, CH4) fluxes, and foliar N concentrations have been monitored in the treated watershed and in reference areas at the HBEF before and since the Ca addition. We expected that rates of microbial C and N cycle processes would increase in response to the treatment. By 2000, soil pH was increased by a full unit in the Oie soil horizon, and by 2002 it was increased by nearly 0.5 units in the Oa soil horizon. However, there were declines in the N content of the microbial biomass, potential net and gross N mineralization rates, and soil inorganic N pools in the Oie horizon of the treated watershed. Stream, soil solution, and foliar concentrations of N showed no response to treatment. The lack of stimulation of N cycling by Ca addition suggests that microbes may not be stimulated by increased pH and Ca levels in the naturally acidic soils at the HBEF, or that other factors (for example, phosphorus, or Ca binding of labile organic matter) may constrain the capacity of microbes to respond to increased pH in the treated watershed. Possible fates for the approximately 10 kg N ha−1 decline in microbial and soil inorganic pools include components of the plant community that we did not measure (for example, seedlings, understory shrubs), increased fluxes of N2 and/or N storage in soil organic matter. These results raise questions about the factors regulating microbial biomass and activity in northern hardwood forests that should be considered in the context of proposals to mitigate the depletion of nutrient cations in soil.

Patterns of nitrate loss from a chronosequence of clear-cut watersheds

Three clear-cuts at the Hubbard Brook Experimental Forest (NH) have resulted in a chronosequence of forest watersheds in close proximity. Following clear-cutting, the stands, now 12, 21, 27, and 78 years old, have different species composition, nutrient capital, and biogeochemistry. In this study, we compared seasonal patterns of NO3− in streamwater, changes in N capital, and N retention in watersheds of differing stand age. All of the watersheds showed elevated losses of NO3−, H+ and nutrient cations (Ca2+, Mg2+, K+) during the first few years following clear-cutting. Increased retention of N occurred during vegetation regrowth compared to the reference watershed (W6). Nitrate concentrations were low during the summer growing season, increased in the late fall and peaked in March during spring snowmelt. Concentrations of NO3− were lower in the regrowing watersheds than in W6 during all months. In W6, there was considerable year-to-year variability in N retention, which was not initially observed in the manipulated watersheds. However, two cut watersheds exhibited higher export of NO3− in 1989 and 1990, corresponding to a 10-year high value in annual NO3− loss in W6. These results demonstrate the importance of land use and cutting history in assessments of N saturation and loss from forest watersheds.

Conditional vulnerability of plant diversity to atmospheric nitrogen deposition across the United States

Significance Human activities have elevated nitrogen (N) deposition and there is evidence that deposition impacts species diversity, but spatially extensive and context-specific estimates of N loads at which species losses begin remain elusive. Across a wide range of climates, soil conditions, and vegetation types in the United States, we found that 24% of >15,000 sites were susceptible to N deposition-induced species loss. Grasslands, shrublands, and woodlands were susceptible to species losses at lower loads of N deposition than forests, and susceptibility to species losses increased in acidic soils. These findings are pertinent to the protection of biodiversity and human welfare and should be considered when establishing air quality standards. Atmospheric nitrogen (N) deposition has been shown to decrease plant species richness along regional deposition gradients in Europe and in experimental manipulations. However, the general response of species richness to N deposition across different vegetation types, soil conditions, and climates remains largely unknown even though responses may be contingent on these environmental factors. We assessed the effect of N deposition on herbaceous richness for 15,136 forest, woodland, shrubland, and grassland sites across the continental United States, to address how edaphic and climatic conditions altered vulnerability to this stressor. In our dataset, with N deposition ranging from 1 to 19 kg N⋅ha−1⋅y−1, we found a unimodal relationship; richness increased at low deposition levels and decreased above 8.7 and 13.4 kg N⋅ha−1⋅y−1 in open and closed-canopy vegetation, respectively. N deposition exceeded critical loads for loss of plant species richness in 24% of 15,136 sites examined nationwide. There were negative relationships between species richness and N deposition in 36% of 44 community gradients. Vulnerability to N deposition was consistently higher in more acidic soils whereas the moderating roles of temperature and precipitation varied across scales. We demonstrate here that negative relationships between N deposition and species richness are common, albeit not universal, and that fine-scale processes can moderate vegetation responses to N deposition. Our results highlight the importance of contingent factors when estimating ecosystem vulnerability to N deposition and suggest that N deposition is affecting species richness in forested and nonforested systems across much of the continental United States.

Estimated losses of plant biodiversity in the United States from historical N deposition (1985–2010)

Although nitrogen (N) deposition is a significant threat to herbaceous plant biodiversity worldwide, it is not a new stressor for many developed regions. Only recently has it become possible to estimate historical impacts nationally for the United States. We used 26 years (1985-2010) of deposition data, with ecosystem-specific functional responses from local field experiments and a national critical loads (CL) database, to generate scenario-based estimates of herbaceous species loss. Here we show that, in scenarios using the low end of the CL range, N deposition exceeded critical loads over 0.38, 6.5, 13.1, 88.6, and 222.1 million ha for the Mediterranean California, North American Desert, Northwestern Forested Mountains, Great Plains, and Eastern Forest ecoregions, respectively, with corresponding species losses ranging from < 1% to 30%. When we ran scenarios assuming ecosystems were less sensitive (using a common CL of 10 kg x ha(-1) x yr(-1), and the high end of the CL range) minimal losses were estimated. The large range in projected impacts among scenarios implies uncertainty as to whether current critical loads provide protection to terrestrial plant biodiversity nationally and urge greater research in refining critical loads for U.S. ecosystems.