Duncan N. L. Menge

Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems

New techniques have identified a wide range of organisms with the capacity to carry out biological nitrogen fixation (BNF)—greatly expanding our appreciation of the diversity and ubiquity of N fixers—but our understanding of the rates and controls of BNF at ecosystem and global scales has not advanced at the same pace. Nevertheless, determining rates and controls of BNF is crucial to placing anthropogenic changes to the N cycle in context, and to understanding, predicting and managing many aspects of global environmental change. Here, we estimate terrestrial BNF for a pre-industrial world by combining information on N fluxes with 15N relative abundance data for terrestrial ecosystems. Our estimate is that pre-industrial N fixation was 58 (range of 40–100) Tg N fixed yr−1; adding conservative assumptions for geological N reduces our best estimate to 44 Tg N yr−1. This approach yields substantially lower estimates than most recent calculations; it suggests that the magnitude of human alternation of the N cycle is substantially larger than has been assumed.

Coastal oceanography sets the pace of rocky intertidal community dynamics

The structure of ecological communities reflects a tension among forces that alter populations. Marine ecologists previously emphasized control by locally operating forces (predation, competition, and disturbance), but newer studies suggest that inputs from large-scale oceanographically modulated subsidies (nutrients, particulates, and propagules) can strongly influence community structure and dynamics. On New Zealand rocky shores, the magnitude of such subsidies differs profoundly between contrasting oceanographic regimes. Community structure, and particularly the pace of community dynamics, differ dramatically between intermittent upwelling regimes compared with relatively persistent down-welling regimes. We suggest that subsidy rates are a key determinant of the intensity of species interactions, and thus of structure in marine systems, and perhaps also nonmarine communities.

Large losses of inorganic nitrogen from tropical rainforests suggest a lack of nitrogen limitation

Inorganic nitrogen losses from many unpolluted mature tropical forests are over an order of magnitude higher than losses from analogous temperate forests. This pattern could either reflect a lack of N limitation or accelerated plant-soil N cycling under tropical temperatures and moisture. We used a simple analytical framework of the N cycle and compared our predictions with data of N in stream waters of temperate and tropical rainforests. While the pattern could be explained by differences in N limitation, it could not be explained based on up-regulation of the internal N cycle without invoking the unlikely assumption that tropical plants are two to four times less efficient at taking up N than temperate plants. Our results contrast with the idea that a tropical climate promotes and sustains an up-regulated and leaky - but N-limited - internal N cycle. Instead, they are consistent with the notion that many tropical rainforests exist in a state of N saturation.

Evolutionary tradeoffs can select against nitrogen fixation and thereby maintain nitrogen limitation

Symbiotic nitrogen (N) fixing trees are absent from old-growth temperate and boreal ecosystems, even though many of these are N-limited. To explore mechanisms that could select against N fixation in N-limited, old-growth ecosystems, we developed a simple resource-based evolutionary model of N fixation. When there are no costs of N fixation, increasing amounts of N fixation will be selected for until N no longer limits production. However, tradeoffs between N fixation and plant mortality or turnover, plant uptake of available soil N, or N use efficiency (NUE) can select against N fixation in N-limited ecosystems and can thereby maintain N limitation indefinitely (provided that there are losses of plant-unavailable N). Three key traits influence the threshold that determines how large these tradeoffs must be to select against N fixation. A low NUE, high mortality (or turnover) rate and low losses of plant-unavailable N all increase the likelihood that N fixation will be selected against, and a preliminary examination of published data on these parameters shows that these mechanisms, particularly the tradeoff with NUE, are quite feasible in some systems. Although these results are promising, a better characterization of these parameters in multiple ecosystems is necessary to determine whether these mechanisms explain the lack of symbiotic N fixers—and thus the maintenance of N limitation—in old-growth forests.

Facultative versus obligate nitrogen fixation strategies and their ecosystem consequences.

Symbiotic nitrogen (N) fixers are critical components of many terrestrial ecosystems. There is evidence that some N fixers fix N at the same rate regardless of environmental conditions (a strategy we call obligate), while others adjust N fixation to meet their needs (a strategy we call facultative). Although these strategies are likely to have qualitatively different impacts on their environment, the relative effectiveness and ecosystem‐level impacts of each strategy have not been explored. Using a simple mathematical model, we determine the best facultative strategy and show that it excludes any obligate strategy (fixer or nonfixer) in our basic model. To provide an explanation for the existence of nonfixers and obligate fixers, we show that both costs of being facultative and time lags inherent in the process of N fixation can select against facultative N fixers and also produce the seemingly paradoxical patterns of sustained N limitation and N richness. Finally, we speculate on why the costs and lags may differ between temperate and tropical regions and thus whether they can explain patterns in both biomes simultaneously.

Nitrogen and Phosphorus Limitation over Long-Term Ecosystem Development in Terrestrial Ecosystems

Nutrient limitation to net primary production (NPP) displays a diversity of patterns as ecosystems develop over a range of timescales. For example, some ecosystems transition from N limitation on young soils to P limitation on geologically old soils, whereas others appear to remain N limited. Under what conditions should N limitation and P limitation prevail? When do transitions between N and P limitation occur? We analyzed transient dynamics of multiple timescales in an ecosystem model to investigate these questions. Post-disturbance dynamics in our model are controlled by a cascade of rates, from plant uptake (very fast) to litter turnover (fast) to plant mortality (intermediate) to plant-unavailable nutrient loss (slow) to weathering (very slow). Young ecosystems are N limited when symbiotic N fixation (SNF) is constrained and P weathering inputs are high relative to atmospheric N deposition and plant N:P demand, but P limited under opposite conditions. In the absence of SNF, N limitation is likely to worsen through succession (decades to centuries) because P is mineralized faster than N. Over long timescales (centuries and longer) this preferential P mineralization increases the N:P ratio of soil organic matter, leading to greater losses of plant-unavailable N versus P relative to plant N:P demand. These loss dynamics favor N limitation on older soils despite the rising organic matter N:P ratio. However, weathering depletion favors P limitation on older soils when continual P inputs (e.g., dust deposition) are low, so nutrient limitation at the terminal equilibrium depends on the balance of these input and loss effects. If NPP switches from N to P limitation over long time periods, the transition time depends most strongly on the P weathering rate. At all timescales SNF has the capacity to overcome N limitation, so nutrient limitation depends critically on limits to SNF.

Dynamics of coastal meta-ecosystems: the intermittent upwelling hypothesis and a test in rocky intertidal regions

The intermittent upwelling hypothesis (IUH) predicts that the strength of ecological subsidies, organismal growth responses, and species interactions will vary unimodally along a gradient of upwelling from persistent downwelling to persistent upwelling, with maximal levels at an intermediate or “intermittent” state of upwelling. To test this model, we employed the comparative-experimental method to investigate these processes at 16–44 wave-exposed rocky intertidal sites in Oregon, California, and New Zealand, varying in average upwelling and/or downwelling during spring–summer. As predicted by the IUH, ecological subsidies (phytoplankton abundance, prey recruitment rates), prey responses (barnacle colonization, mussel growth), and species interactions (competition rate, predation rate and effects) were unimodally related to upwelling. On average, unimodal relationships with upwelling magnitude explained ∼50% of the variance in the various processes, and unimodal and monotonic positive relationships agains...

Emergence and maintenance of nutrient limitation over multiple timescales in terrestrial ecosystems.

Nutrient availability often limits primary production, yet the processes governing the dynamics of nutrient limitation are poorly understood. In particular, plant‐available (e.g., nitrate) versus plant‐unavailable (e.g., dissolved organic nitrogen) nutrient losses may have qualitatively different impacts on nutrient limitation. We examine processes controlling equilibrium and transient nutrient dynamics at three separate timescales in a model of a nutrient cycling through plants and soil. When the only losses are from the plant‐available nutrient pool, nutrient limitation at a long‐term equilibrium is impossible under a wide class of conditions. However, plant biomass will appear to level off on a timescale controlled by plant nutrient turnover (years in grasslands, decades to centuries in forests), even though it can grow slowly forever. Primary production can be nutrient limited in the long‐term when there are losses of plant‐unavailable nutrients or when the mineralization flux saturates with increasing detrital mass. The long timescale required for soil nutrient buildup is set by the plant‐unavailable loss rate (centuries to millennia). The short timescale (hours to days) at which available nutrients in the soil equilibrate in the model is controlled by biotic uptake. These insights into processes controlling different timescales in terrestrial ecosystems can help guide empirical and experimental studies.

Gauging the impact of meta-analysis on ecology

Meta-analyses are an increasingly used set of statistical tools that allow for data from multiple studies to be drawn together allowing broader, more generalizable conclusions. The extent to which the increase in the number of meta-analyses in ecology, relative to other types of papers, has influenced how questions are asked and the current state of knowledge has not been assessed before. Here, we gauge the impact of meta-analyses in ecology quantitatively and qualitatively. For the quantitative assessment, we conducted an analysis of 240 published meta-analyses to examine trends in ecological meta-analyses. Our examination shows that publication rates of meta-analyses in ecology have increased through time, and that more recent meta-analyses have been more comprehensive, including more studies and a greater temporal range of studies. Meta-analyses in ecology are the result of larger collaborations with meta-analyses being authored by larger teams than other studies, and those funded by collaborative centers have even larger collaborations. These larger collaborations result in a larger scope and scale of the analyses—by using more papers, datasets, species and years of data. Qualitatively, we discuss three examples: the strength of competition, the nature of how biodiversity affects ecosystem function, and the response of species to global climate change, where meta-analyses supplied the critical evaluation of accepted ecological explanations. As scientific criticism and controversy mount, the true power of meta-analyses is to serve as the capstone evidence supporting the validity of an explanation and to possibly herald the shift to other potential explanations.

Diversity of nitrogen fixation strategies in Mediterranean legumes

Symbiotic N2 fixation (SNF) brings nitrogen into ecosystems, fuelling much of the worlds agriculture1 and sustaining carbon storage2,3. However, it can also cause nitrogen saturation, exacerbating eutrophication and greenhouse warming4–7. The balance of these effects depends on the degree to which N2-fixing plants adjust how much N2 they fix based on their needs (their SNF ‘strategies’)5,6. Genetic, biochemical and physiological details of SNF are well known for certain economically important species8,9, but the diversity of N2-fixing plants10 and bacteria11 is enormous, and little is known about most N2-fixing symbioses in natural ecosystems12. Here, we show that co-occurring, closely related herbs exhibit diverse SNF strategies. In response to a nitrogen supply gradient, four species fixed less N2 than they needed (over-regulation), two fixed what they needed (facultative) and two did not downregulate SNF (obligate). No species downregulated but fixed more N2 than it needed (under-regulation or incomplete downregulation), but some species under-regulated or incompletely downregulated structural allocation to SNF. In fact, most species maintained nodules (the root structures that house symbionts) when they did not fix N2, suggesting decoupling of SNF activity and structure. Simulations showed that over-regulation of SNF activity is more adaptive than under-regulation or incomplete downregulation, and that different strategies have wildly different effects on ecosystem-level nitrogen cycling.