Cory C. Cleveland

Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems

Human activities have clearly caused dramatic alterations of the terrestrial nitrogen cycle, and analyses of the extent and effects of such changes are now common in the scientific literature. However, any attempt to evaluate N cycling processes within ecosystems, as well as anthropogenic influences on the N cycle, requires an understanding of the magnitude of inputs via biological nitrogen fixation (BNF). Although there have been many studies addressing the microbiology, physiology, and magnitude of N fixation at local scales, there are very few estimates of BNF over large scales. We utilized >100 preexisting published estimates of BNF to generate biome- and global-level estimates of biological N fixation. We also used net primary productivity (NPP) and evapotranspiration (ET) estimates from the Century terrestrial ecosystem model to examine global relationships between these variables and BNF as well as to compare observed and Century-modeled BNF. Our data-based estimates showed a strong positive relationship between ecosystem ET and BNF, and our analyses suggest that while the models simple relationships for BNF predict broad scale patterns, they do not capture much of the variability or magnitude of published rates. Patterns of BNF were also similar to patterns of ecosystem NPP. Our “best estimate” of potential nitrogen fixation by natural ecosystems is ∼195 Tg N yr−1, with a range of 100–290 Tg N yr−1. Although these estimates do not account for the decrease in natural N fixation due to cultivation, this would not dramatically alter our estimate, as the greatest reductions in area have occurred in systems characterized by relatively low rates of N fixation (e.g., grasslands). Although our estimate of BNF in natural ecosystems is similar to previously published estimates of terrestrial BNF, we believe that this study provides a more documented, constrained estimate of this important flux.

Towards an ecological understanding of biological nitrogen fixation

N limitation to primary production and other ecosystem processes is widespread. To understand the causes and distribution of N limitation, we must understand the controls of biological N fixation. The physiology of this process is reasonably well characterized, but our understanding of ecological controls is sparse, except in a few cultivated ecosystems. We review information on the ecological controls of N fixation in free-living cyanobacteria, vascular plant symbioses, and heterotrophic bacteria, with a view toward developing improved conceptual and simulation models of ecological controls of biological N fixation.A model (Howarth et al. 1999) of cyanobacterial fixation in lakes (where N fixation generally increases substantially when N:P ratios are low) versus estuaries (where planktonic N fixation is rare regardless of N:P ratios) concludes that an interaction of trace-element limitation and zooplankton grazing could constrain cyanobacteria in estuaries and so sustain N limitation. Similarly. a model of symbiotic N fixation on land (Vitousek & Field 1999) suggests that shade intolerance, P limitation, and grazing on N-rich plant tissues could suppress symbiotic N fixers in late-successional forest ecosystems. This congruence of results raises the question – why do late-successional tropical forests often contain many potentially N-fixing canopy legumes, while N fixers are absent from most late-successional temperate and boreal forests? We suggest that relatively high N availability in lowland tropical forests permits legumes to maintain an N-demanding lifestyle (McKey 1994) without always being required to pay the costs of fixing N.Overall, both the few simulation models and the more-numerous conceptual models of ecological controls of biological N fixation suggest that there are substantial common features across N-fixing organisms and ecosystems. Despite the many groups of organisms capable of fixing N, and the very different ecosystems in which the process is important, we suggest that these common controls provide a foundation for the development of regional and global models that incorporate ecological controls of biological N fixation.

Global patterns in belowground communities

Although belowground ecosystems have been studied extensively and soil biota play integral roles in biogeochemical processes, surprisingly we have a limited understanding of global patterns in belowground biomass and community structure. To address this critical gap, we conducted a meta-analysis of published data (> 1300 datapoints) to compare belowground plant, microbial and faunal biomass across seven of the major biomes on Earth. We also assembled data to assess biome-level patterns in belowground microbial community composition. Our analysis suggests that variation in microbial biomass is predictable across biomes, with microbial biomass carbon representing 0.6-1.1% of soil organic carbon (r(2) = 0.91) and 1-20% of total plant biomass carbon (r(2) = 0.42). Approximately 50% of total animal biomass can be found belowground and soil faunal biomass represents < 4% of microbial biomass across all biomes. The structure of belowground microbial communities is also predictable: bacterial community composition and fungal : bacterial gene ratios can be predicted reasonably well from soil pH and soil C : N ratios respectively. Together these results identify robust patterns in the structure of belowground microbial and faunal communities at broad scales which may be explained by universal mechanisms that regulate belowground biota across biomes.

Human health effects of a changing global nitrogen cycle

Changes to the global nitrogen cycle affect human health well beyond the associated benefits of increased food production. Many intensively fertilized crops become animal feed, helping to create disparities in world food distribution and leading to unbalanced diets, even in wealthy nations. Excessive air- and water-borne nitrogen are linked to respiratory ailments, cardiac disease, and several cancers. Ecological feedbacks to excess nitrogen can inhibit crop growth, increase allergenic pollen production, and potentially affect the dynamics of several vector-borne diseases, including West Nile virus, malaria, and cholera. These and other examples suggest that our increasing production and use of fixed nitrogen poses a growing public health risk.

Phosphorus Limitation of Microbial Processes in Moist Tropical Forests: Evidence from Short-term Laboratory Incubations and Field Studies

AbstractAlthough there is a widespread belief that phosphorus (P) limits basic ecosystem processes in moist tropical forests, direct tests of this supposition are rare. At the same time, it is generally believed that P does not limit soil microorganism respiration or growth in terrestrial ecosystems. We used natural gradients in P fertility created by soils of varying age underlying tropical rain forests in southwestern Costa Rica, combined with direct manipulations of carbon (C) and P supply, to test the effects of P availability on the decomposition of multiple forms of C, including dissolved organic carbon (DOC) and soil organic carbon (SOC). Results from a combination of laboratory and field experiments suggest that C decomposition in old, highly weathered oxisol soils is strongly constrained by P availability. In addition, P additions to these soils (no C added) also revealed that microbial utilization of at least labile fractions of SOC was also P limited. To our knowledge, this is the first direct evidence of P limitation of microbial processes in tropical rain forest soil. We suggest that P limitation of microbial decomposition may have profound implications for C cycling in moist tropical forests, including their potential response to increasing atmospheric carbon dioxide. Furthermore, this site is still relatively rich in P when compared to many other tropical forests on old soils; thus, we believe that P limitation of soil microorganisms throughout the humid tropics is a possibility.

Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere

Terrestrial biosphere–atmosphere carbon dioxide (CO2) exchange is dominated by tropical forests, where photosynthetic carbon (C) uptake is thought to be phosphorus (P)-limited. In P-poor tropical forests, P may also limit organic matter decomposition and soil C losses. We conducted a field-fertilization experiment to show that P fertilization stimulates soil respiration in a lowland tropical rain forest in Costa Rica. In the early wet season, when soluble organic matter inputs to soil are high, P fertilization drove large increases in soil respiration. Although the P-stimulated increase in soil respiration was largely confined to the dry-to-wet season transition, the seasonal increase was sufficient to drive an 18% annual increase in CO2 efflux from the P-fertilized plots. Nitrogen (N) fertilization caused similar responses, and the net increases in soil respiration in response to the additions of N and P approached annual soil C fluxes in mid-latitude forests. Human activities are altering natural patterns of tropical soil N and P availability by land conversion and enhanced atmospheric deposition. Although our data suggest that the mechanisms driving the observed respiratory responses to increased N and P may be different, the large CO2 losses stimulated by N and P fertilization suggest that knowledge of such patterns and their effects on soil CO2 efflux is critical for understanding the role of tropical forests in a rapidly changing global C cycle.

CONTROLS OVER FOLIAR N:P RATIOS IN TROPICAL RAIN FORESTS

Correlations between foliar nutrient concentrations and soil nutrient availability have been found in multiple ecosystems. These relationships have led to the use of foliar nutrients as an index of nutrient status and to the prediction of broadscale patterns in ecosystem processes. More recently, a growing interest in ecological stoichiometry has fueled multiple analyses of foliar nitrogen:phosphorus (N:P) ratios within and across ecosystems. These studies have observed that N:P values are generally elevated in tropical forests when compared to higher latitude ecosystems, adding weight to a common belief that tropical forests are generally N rich and P poor. However, while these broad generalizations may have merit, their simplicity masks the enormous environmental heterogeneity that exists within the tropics; such variation includes large ranges in soil fertility and climate, as well as the highest plant species diversity of any biome. Here we present original data on foliar N and P concentrations from 150 mature canopy tree species in Costa Rica and Brazil, and combine those data with a comprehensive new literature synthesis to explore the major sources of variation in foliar N:P values within the tropics. We found no relationship between N:P ratios and either latitude or mean annual precipitation within the tropics alone. There is, however, evidence of seasonal controls; in our Costa Rica sites, foliar N:P values differed by 25% between wet and dry seasons. The N:P ratios do vary with soil P availability and/or soil order, but there is substantial overlap across coarse divisions in soil type, and perhaps the most striking feature of the data set is variation at the species level. Taken as a whole, our results imply that the dominant influence on foliar N:P ratios in the tropics is species variability and that, unlike marine systems and perhaps many other terrestrial biomes, the N:P stoichiometry of tropical forests is not well constrained. Thus any use of N:P ratios in the tropics to infer larger-scale ecosystem processes must comprehensively account for the diversity of any given site and recognize the broad range in nutrient requirements, even at the local scale.

Microbial Community Succession in an Unvegetated, Recently Deglaciated Soil

Primary succession is a fundamental process in macroecosystems; however, if and how soil development influences microbial community structure is poorly understood. Thus, we investigated changes in the bacterial community along a chronosequence of three unvegetated, early successional soils (∼20-year age gradient) from a receding glacier in southeastern Peru using molecular phylogenetic techniques. We found that evenness, phylogenetic diversity, and the number of phylotypes were lowest in the youngest soils, increased in the intermediate aged soils, and plateaued in the oldest soils. This increase in diversity was commensurate with an increase in the number of sequences related to common soil bacteria in the older soils, including members of the divisions Acidobacteria, Bacteroidetes, and Verrucomicrobia. Sequences related to the Comamonadaceae clade of the Betaproteobacteria were dominant in the youngest soil, decreased in abundance in the intermediate age soil, and were not detected in the oldest soil. These sequences are closely related to culturable heterotrophs from rock and ice environments, suggesting that they originated from organisms living within or below the glacier. Sequences related to a variety of nitrogen (N)-fixing clades within the Cyanobacteria were abundant along the chronosequence, comprising 6–40% of phylotypes along the age gradient. Although there was no obvious change in the overall abundance of cyanobacterial sequences along the chronosequence, there was a dramatic shift in the abundance of specific cyanobacterial phylotypes, with the intermediate aged soils containing the greatest diversity of these sequences. Most soil biogeochemical characteristics showed little change along this ∼20-year soil age gradient; however, soil N pools significantly increased with soil age, perhaps as a result of the activity of the N-fixing Cyanobacteria. Our results suggest that, like macrobial communities, soil microbial communities are structured by substrate age, and that they, too, undergo predictable changes through time.

Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis

Tropical rain forests play a dominant role in global biosphere-atmosphere CO(2) exchange. Although climate and nutrient availability regulate net primary production (NPP) and decomposition in all terrestrial ecosystems, the nature and extent of such controls in tropical forests remain poorly resolved. We conducted a meta-analysis of carbon-nutrient-climate relationships in 113 sites across the tropical forest biome. Our analyses showed that mean annual temperature was the strongest predictor of aboveground NPP (ANPP) across all tropical forests, but this relationship was driven by distinct temperature differences between upland and lowland forests. Within lowland forests (< 1000 m), a regression tree analysis revealed that foliar and soil-based measurements of phosphorus (P) were the only variables that explained a significant proportion of the variation in ANPP, although the relationships were weak. However, foliar P, foliar nitrogen (N), litter decomposition rate (k), soil N and soil respiration were all directly related with total surface (0-10 cm) soil P concentrations. Our analysis provides some evidence that P availability regulates NPP and other ecosystem processes in lowland tropical forests, but more importantly, underscores the need for a series of large-scale nutrient manipulations - especially in lowland forests - to elucidate the most important nutrient interactions and controls.

Global patterns in the biogeography of bacterial taxa.

Bacteria control major nutrient cycles and directly influence plant, animal and human health. However, we know relatively little about the forces shaping their large-scale ecological ranges. Here, we reveal patterns in the distribution of individual bacterial taxa at multiple levels of phylogenetic resolution within and between Earths major habitat types. Our analyses suggest that while macro-scale habitats structure bacterial distribution to some degree, abundant bacteria (i.e. detectable using 16S rRNA gene sequencing methods) are confined to single assemblages. Additionally, we show that the most cosmopolitan taxa are also the most abundant in individual assemblages. These results add to the growing body of data that support that the diversity of the overall bacterial metagenome is tremendous. The mechanisms governing microbial distribution remain poorly understood, but our analyses provide a framework with which to test the importance of macro-ecological environmental gradients, relative abundance, neutral processes and the ecological strategies of individual taxa in structuring microbial communities.