Microbial community dynamics alleviate stoichiometric constraints during litter decay

Under the current paradigm, organic matter decomposition and nutrient cycling rates are a function of the imbalance between substrate and microbial biomass stoichiometry. Challenging this view, we demonstrate that in an individual‐based model, microbial community dynamics alter relative C and N limitation during litter decomposition, leading to a system behaviour not predictable from stoichiometric theory alone. Rather, the dynamics of interacting functional groups lead to an adaptation at the community level, which accelerates nitrogen recycling in litter with high initial C : N ratios and thus alleviates microbial N limitation. This mechanism allows microbial decomposers to overcome large imbalances between resource and biomass stoichiometry without the need to decrease carbon use efficiency (CUE), which is in contrast to predictions of traditional stoichiometric mass balance equations. We conclude that identifying and implementing microbial community‐driven mechanisms in biogeochemical models are necessary for accurately predicting terrestrial C fluxes in response to changing environmental conditions.     

High‐frequency fire alters C : N : P stoichiometry in forest litter

Fire is a major driver of ecosystem change and can disproportionately affect the cycling of different nutrients. Thus, a stoichiometric approach to investigate the relationships between nutrient availability and microbial resource use during decomposition is likely to provide insight into the effects of fire on ecosystem functioning. We conducted a field litter bag experiment to investigate the long‐term impact of repeated fire on the stoichiometry of leaf litter C, N and P pools, and nutrient‐acquiring enzyme activities during decomposition in a wet sclerophyll eucalypt forest in Queensland, Australia. Fire frequency treatments have been maintained since 1972, including burning every 2 years (2yrB), burning every 4 years (4yrB) and no burning (NB). C : N ratios in freshly fallen litter were 29–42% higher and C : P ratios were 6–25% lower for 2yrB than NB during decomposition, with correspondingly lower 2yrB N : P ratios (27–32) than for NB (34–49). Trends in litter soluble and microbial N : P ratios were similar to the overall litter N : P ratios across fire treatments. Consistent with these, the ratio of activities for N‐acquiring to P‐acquiring enzymes in litter was higher for 2yrB than NB, whereas 4yrB was generally intermediate between 2yrB and NB. Decomposition rates of freshly fallen litter were significantly lower for 2yrB (72 ± 2% mass remaining at the end of experiment) than for 4yrB (59 ± 3%) and NB (62 ± 3%), a difference that may be related to effects of N limitation, lower moisture content, and/or litter C quality. Results for older mixed‐age litter were similar to those for freshly fallen litter although treatment differences were less pronounced. Overall, these findings show that frequent fire (2yrB) decoupled N and P cycling, as manifested in litter C : N : P stoichiometry and in microbial biomass N : P ratio and enzymatic activities. Furthermore, these data indicate that fire induced a transient shift to N‐limited ecosystem conditions during the postfire recovery phase.     

Nitrogen limitation of heterotrophic biofilms in boreal streams

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Warming alters coupled carbon and nutrient cycles in experimental streams

Although much effort has been devoted to quantifying how warming alters carbon cycling across diverse ecosystems, less is known about how these changes are linked to the cycling of bioavailable nitrogen and phosphorus. In freshwater ecosystems, benthic biofilms (i.e. thin films of algae, bacteria, fungi, and detrital matter) act as biogeochemical hotspots by controlling important fluxes of energy and material. Understanding how biofilms respond to warming is thus critical for predicting responses of coupled elemental cycles in freshwater systems. We developed biofilm communities in experimental streamside channels along a gradient of mean water temperatures (7.5–23.6 °C), while closely maintaining natural diel and seasonal temperature variation with a common water and propagule source. Both structural (i.e. biomass, stoichiometry, assemblage structure) and functional (i.e. metabolism, N₂‐fixation, nutrient uptake) attributes of biofilms were measured on multiple dates to link changes in carbon flow explicitly to the dynamics of nitrogen and phosphorus. Temperature had strong positive effects on biofilm biomass (2.8‐ to 24‐fold variation) and net ecosystem productivity (44‐ to 317‐fold variation), despite extremely low concentrations of limiting dissolved nitrogen. Temperature had surprisingly minimal effects on biofilm stoichiometry: carbon:nitrogen (C:N) ratios were temperature‐invariant, while carbon:phosphorus (C:P) ratios declined slightly with increasing temperature. Biofilm communities were dominated by cyanobacteria at all temperatures (>91% of total biovolume) and N₂‐fixation rates increased up to 120‐fold between the coldest and warmest treatments. Although ammonium‐N uptake increased with temperature (2.8‐ to 6.8‐fold variation), the much higher N₂‐fixation rates supplied the majority of N to the ecosystem at higher temperatures. Our results demonstrate that temperature can alter how carbon is cycled and coupled to nitrogen and phosphorus. The uncoupling of C fixation from dissolved inorganic nitrogen supply produced large unexpected changes in biofilm development, elemental cycling, and likely downstream exports of nutrients and organic matter.     

Dissimilar responses of fungal and bacterial communities to soil transplantation simulating abrupt climate changes

Both fungi and bacteria play essential roles in regulating soil carbon cycling. To predict future carbon stability, it is imperative to understand their responses to environmental changes, which is subject to large uncertainty. As current global warming is causing range shifts toward higher latitudes, we conducted three reciprocal soil transplantation experiments over large transects in 2005 to simulate abrupt climate changes. Six years after soil transplantation, fungal biomass of transplanted soils showed a general pattern of changes from donor sites to destination, which were more obvious in bare fallow soils than in maize cropped soils. Strikingly, fungal community compositions were clustered by sites, demonstrating that fungi of transplanted soils acclimatized to the destination environment. Several fungal taxa displayed sharp changes in relative abundance, including Podospora, Chaetomium, Mortierella and Phialemonium. In contrast, bacterial communities remained largely unchanged. Consistent with the important role of fungi in affecting soil carbon cycling, 8.1%–10.0% of fungal genes encoding carbon‐decomposing enzymes were significantly (p < 0.01) increased as compared with those from bacteria (5.7%–8.4%). To explain these observations, we found that fungal occupancy across samples was mainly determined by annual average air temperature and rainfall, whereas bacterial occupancy was more closely related to soil conditions, which remained stable 6 years after soil transplantation. Together, these results demonstrate dissimilar response patterns and resource partitioning between fungi and bacteria, which may have considerable consequences for ecosystem‐scale carbon cycling.     

Plant sizes mediate mowing‐induced changes in nutrient stoichiometry and allocation of a perennial grass in semi‐arid grassland

While mowing‐induced changes in plant traits and their effects on ecosystem functioning in semi‐arid grassland are well studied, the relations between plant size and nutrient strategies are largely unknown. Mowing may drive the shifts of plant nutrient limitation and allocation. Here, we evaluated the changes in nutrient stoichiometry and allocation with variations in sizes of Leymus chinensis, the dominant plant species in Inner Mongolia grassland, to various mowing frequencies in a 17‐yr controlled experiment. Affected by mowing, the concentrations of nitrogen (N), phosphorus (P), and carbon (C) in leaves and stems were significantly increased, negatively correlating with plant sizes. Moreover, we found significant trade‐offs between the concentrations and accumulation of N, P, and C in plant tissues. The N:P ratios of L. chinensis aboveground biomass, linearly correlating with plant size, significantly decreased with increased mowing frequencies. The ratios of C:N and C:P of L. chinensis individuals were positively correlated with plant size, showing an exponential pattern. With increased mowing frequencies, L. chinensis size was correlated with the allocation ratios of leaves to stems of N, P, and C by the tendencies of negative parabola, positive, and negative linear. The results of structure equation modeling showed that the N, P, and C allocations were co‐regulated by biomass allocation and nutrient concentration ratios of leaves to stems. In summary, we found a significant decoupling effect between plant traits and nutrient strategies along mowing frequencies. Our results reveal a mechanism for how long‐term mowing‐induced changes in concentrations, accumulations, ecological stoichiometry, and allocations of key elements are mediated by the variations in plant sizes of perennial rhizome grass.     

Effects of incubation conditions on nutrient mineralisation rates in fish and shrimp

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Convergent responses of nitrogen and phosphorus resorption to nitrogen inputs in a semiarid grassland

Human activities have significantly altered nitrogen (N) availability in most terrestrial ecosystems, with consequences for community composition and ecosystem functioning. Although studies of how changes in N availability affect biodiversity and community composition are relatively common, much less remains known about the effects of N inputs on the coupled biogeochemical cycling of N and phosphorus (P), and still fewer data exist regarding how increased N inputs affect the internal cycling of these two elements in plants. Nutrient resorption is an important driver of plant nutrient economies and of the quality of litter plants produce. Accordingly, resorption patterns have marked ecological implications for plant population and community fitness, as well as for ecosystem nutrient cycling. In a semiarid grassland in northern China, we studied the effects of a wide range of N inputs on foliar nutrient resorption of two dominant grasses, Leymus chinensis and Stipa grandis. After 4 years of treatments, N and P availability in soil and N and P concentrations in green and senesced grass leaves increased with increasing rates of N addition. Foliar N and P resorption significantly decreased along the N addition gradient, implying a resorption‐mediated, positive plant–soil feedback induced by N inputs. Furthermore, N : P resorption ratios were negatively correlated with the rates of N addition, indicating the sensitivity of plant N and P stoichiometry to N inputs. Taken together, the results demonstrate that N additions accelerate ecosystem uptake and turnover of both N and P in the temperate steppe and that N and P cycles are coupled in dynamic ways. The convergence of N and P resorption in response to N inputs emphasizes the importance of nutrient resorption as a pathway by which plants and ecosystems adjust in the face of increasing N availability.     

Effects of three global change drivers on terrestrial C:N:P stoichiometry: a global synthesis

Over the last few decades, there has been an increasing number of controlled‐manipulative experiments to investigate how plants and soils might respond to global change. These experiments typically examined the effects of each of three global change drivers [i.e., nitrogen (N) deposition, warming, and elevated CO₂] on primary productivity and on the biogeochemistry of carbon (C), N, and phosphorus (P) across different terrestrial ecosystems. Here, we capitalize on this large amount of information by performing a comprehensive meta‐analysis (>2000 case studies worldwide) to address how C:N:P stoichiometry of plants, soils, and soil microbial biomass might respond to individual vs. combined effects of the three global change drivers. Our results show that (i) individual effects of N addition and elevated CO₂ on C:N:P stoichiometry are stronger than warming, (ii) combined effects of pairs of global change drivers (e.g., N addition + elevated CO₂, warming + elevated CO₂) on C:N:P stoichiometry were generally weaker than the individual effects of each of these drivers, (iii) additive interactions (i.e., when combined effects are equal to or not significantly different from the sum of individual effects) were more common than synergistic or antagonistic interactions, (iv) C:N:P stoichiometry of soil and soil microbial biomass shows high homeostasis under global change manipulations, and (v) C:N:P responses to global change are strongly affected by ecosystem type, local climate, and experimental conditions. Our study is one of the first to compare individual vs. combined effects of the three global change drivers on terrestrial C:N:P ratios using a large set of data. To further improve our understanding of how ecosystems might respond to future global change, long‐term ecosystem‐scale studies testing multifactor effects on plants and soils are urgently required across different world regions.     

Grazing intensity significantly affects belowground carbon and nitrogen cycling in grassland ecosystems: a meta‐analysis

Livestock grazing activities potentially alter ecosystem carbon (C) and nitrogen (N) cycles in grassland ecosystems. Despite the fact that numerous individual studies and a few meta‐analyses had been conducted, how grazing, especially its intensity, affects belowground C and N cycling in grasslands remains unclear. In this study, we performed a comprehensive meta‐analysis of 115 published studies to examine the responses of 19 variables associated with belowground C and N cycling to livestock grazing in global grasslands. Our results showed that, on average, grazing significantly decreased belowground C and N pools in grassland ecosystems, with the largest decreases in microbial biomass C and N (21.62% and 24.40%, respectively). In contrast, belowground fluxes, including soil respiration, soil net N mineralization and soil N nitrification increased by 4.25%, 34.67% and 25.87%, respectively, in grazed grasslands compared to ungrazed ones. More importantly, grazing intensity significantly affected the magnitude (even direction) of changes in the majority of the assessed belowground C and N pools and fluxes, and C : N ratio as well as soil moisture. Specifically,light grazing contributed to soil C and N sequestration whereas moderate and heavy grazing significantly increased C and N losses. In addition, soil depth, livestock type and climatic conditions influenced the responses of selected variables to livestock grazing to some degree. Our findings highlight the importance of the effects of grazing intensity on belowground C and N cycling, which may need to be incorporated into regional and global models for predicting effects of human disturbance on global grasslands and assessing the climate‐biosphere feedbacks.     

Simulated Nitrogen Deposition Causes a Decline of Intra- and Extraradical Abundance of Arbuscular Mycorrhizal Fungi and Changes in Microbial Community Structure in Northern Hardwood Forests

Increased nitrogen (N) deposition caused by human activities has altered ecosystem functioning and biodiversity. To understand the effects of altered N availability, we measured the abundance of arbuscular mycorrhizal fungi (AMF) and the microbial community in northern hardwood forests exposed to long-term (12 years) simulated N deposition (30 kg N ha⁻¹ y⁻¹) using phospholipid fatty acid (PLFA) analysis and hyphal in-growth bags. Intra- and extraradical AMF biomass and total microbial biomass were significantly decreased by simulated N deposition by 36, 41, and 24%, respectively. Both methods of extraradical AMF biomass estimation (soil PLFA 16:1ω5c and hyphal in-growth bags) showed comparable treatment responses, and extraradical biomass represented the majority of total (intra-plus extraradical) AMF biomass. N deposition also significantly affected the microbial community structure, leading to a 10% decrease in fungal to bacterial biomass ratios. Our observed decline in AMF and total microbial biomass together with changes in microbial community structure could have substantial impacts on the nutrient and carbon cycling within northern hardwood forest ecosystems.     

Nitrogen deposition weakens plant–microbe interactions in grassland ecosystems

Soil carbon (C) and nitrogen (N) stoichiometry is a main driver of ecosystem functioning. Global N enrichment has greatly changed soil C : N ratios, but how altered resource stoichiometry influences the complexity of direct and indirect interactions among plants, soils, and microbial communities has rarely been explored. Here, we investigated the responses of the plant‐soil‐microbe system to multi‐level N additions and the role of dissolved organic carbon (DOC) and inorganic N stoichiometry in regulating microbial biomass in semiarid grassland in northern China. We documented a significant positive correlation between DOC and inorganic N across the N addition gradient, which contradicts the negative nonlinear correlation between nitrate accrual and DOC availability commonly observed in natural ecosystems. Using hierarchical structural equation modeling, we found that soil acidification resulting from N addition, rather than changes in the plant community, was most closely related to shifts in soil microbial community composition and decline of microbial respiration. These findings indicate a down‐regulating effect of high N availability on plant–microbe interactions. That is, with the limiting factor for microbial biomass shifting from resource stoichiometry to soil acidity, N enrichment weakens the bottom‐up control of soil microorganisms by plant‐derived C sources. These results highlight the importance of integratively studying the plant‐soil‐microbe system in improving our understanding of ecosystem functioning under conditions of global N enrichment.     

The phosphorus‐rich signature of fire in the soil–plant system: a global meta‐analysis

The biogeochemical and stoichiometric signature of vegetation fire may influence post‐fire ecosystem characteristics and the evolution of plant ‘fire traits’. Phosphorus (P), a potentially limiting nutrient in many fire‐prone environments, might be particularly important in this context; however, the effects of fire on P cycling often vary widely. We conducted a global‐scale meta‐analysis using data from 174 soil studies and 39 litter studies, and found that fire led to significantly higher concentrations of soil mineral P as well as significantly lower soil and litter carbon:P and nitrogen:P ratios. These results demonstrate that fire has a P‐rich signature in the soil–plant system that varies with vegetation type. Further, they suggest that burning can ease P limitation and decouple the biogeochemical cycling of P, carbon and nitrogen. These effects resemble a transient reversion to an earlier stage of ecosystem development, and likely underpin at least some of fire's impacts on ecosystems and organisms.     

Stoichiometric relationships among producers,consumers and nutrient cycling in pelagic ecosystems

Most ecosystem models consolidate members of food-webs, e.g. species, into a small number of functional components. Each of these is then described by a single state variable such as biomass. When a multivariate approach incorporating multiple substances within components is substituted for this univariate one, a stoichiometric model is formed. Here we show that the Nitrogen:Phosphorus ratio within zooplankton herbivores varies substantially intraspecifically but not intraspecifically. By using stoichiometric theory and recent measurements of the N:P ratio within different zooplankton taxa, we calculate large differences in ratios of nutrients recycled by different zooplankton species. Finally, we demonstrate that N:P stoichiometry can successfully account for shifts in N- and P-limitation previously observed in whole-lake experiments. Species stoichiometry merges food-web dynamics with biogeochemical cycles to yield new insights.Abbreviations b N:P in zooplankton biomass - f N:P in algal biomass - L maximum accumulation eficiency - N:P ratio of nitrogen to phosphorus (moles:moles) - s N:P supply ratio from grazers - TN Total nitrogen = seston N + dissolved N (µmoles/liter) - TP Total phosphorus = seston P + dissolved P (µmoles/liter)     

Rapid adaptation of herbivore consumers to nutrient limitation: eco‐evolutionary feedbacks to population demography and resource control

Humans alter biogeochemical cycles of essential elements such as phosphorus (P). Prediction of ecosystem consequences of altered elemental cycles requires integration of ecology, evolutionary biology and the framework of ecological stoichiometry. We studied micro‐evolutionary responses of a herbivorous rotifer to P‐limited food and the potential consequences for its population demography and for ecosystem properties. We subjected field‐derived, replicate rotifer populations to P‐deficient and P‐replete algal food, and studied adaptation in common garden transplant experiments after 103 and 209 days of selection. When fed P‐limited food, populations with a P‐limitation selection history suffered 37% lower mortality, reached twice the steady state biomass, and reduced algae by 40% compared to populations with a P‐replete selection history. Adaptation involved no change in rotifer elemental composition but reduced investment in sex. This study demonstrates potentially strong eco‐evolutionary feedbacks from shifting elemental balances to ecosystem properties, including grazing pressure and the ratio of grazer:producer biomass.     

Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta‐analysis

Nitrogen (N) and phosphorus (P), either individually or in combination, have been demonstrated to limit biomass production in terrestrial ecosystems. Field studies have been extensively synthesized to assess global patterns of N impacts on terrestrial ecosystem processes. However, to our knowledge, no synthesis has been done so far to reveal global patterns of P impacts on terrestrial ecosystems, especially under different nitrogen (N) levels. Here, we conducted a meta‐analysis of impacts of P addition, either alone or with N addition, on aboveground (AGB) and belowground biomass production (BGB), plant and soil P concentrations, and N : P ratio in terrestrial ecosystems. Overall, our meta‐analysis quantitatively confirmed existing notions: (i) colimitation of N and P on biomass production and (ii) more P limitation in tropical forest than other ecosystems. More importantly, our analysis revealed new findings: (i) P limitation on biomass production was aggravated by N enrichment and (ii) plant P concentration was a better indicator of P limitation than soil P availability. Specifically, P addition increased AGB and BGB by 34% and 13%, respectively. The effect size of P addition on biomass production was larger in tropical forest than grassland, wetland, and tundra and varied with P fertilizer forms, P addition rates, or experimental durations. The P‐induced increase in biomass production and plant P concentration was larger under elevated than ambient N. Our findings suggest that the global limitation of P on biomass production will become severer under increasing N fertilizer and deposition in the future.     

Effects of land use on the structure and function of leaf‐litter microbial communities in boreal streams

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Invasive plants differentially affect soil biota through litter and rhizosphere pathways: a meta‐analysis

Invasive plants affect soil biota through litter and rhizosphere inputs, but the direction and magnitude of these effects are variable. We conducted a meta‐analysis to examine the different effects of litter and rhizosphere of invasive plants on soil communities and nutrient cycling. Our results showed that invasive plants increased bacterial biomass by 16%, detritivore abundance by 119% and microbivore abundance by 89% through litter pathway. In the rhizosphere, invasive plants reduced bacterial biomass by 12%, herbivore abundance by 55% and predator abundance by 52%, but increased AM fungal biomass by 36%. Moreover, CO₂ efflux, N mineralisation rate and enzyme activities were all higher in invasive than native rhizosphere soils. These findings indicate that invasive plants may support more decomposers that in turn stimulate nutrient release via litter effect, and enhance nutrient uptake by reducing root grazing but forming more symbioses in the rhizosphere. Thus, we hypothesise that litter‐ and root‐based loops are probably linked to generate positive feedback of invaders on soil systems through stimulating nutrient cycling, consequently facilitating plant invasion. Our findings from limited cases with diverse contexts suggest that more studies are needed to differentiate litter and rhizosphere effects within single systems to better understand invasive plant‐soil interactions.     

Complex effects of mammalian grazing on extramatrical mycelial biomass in the Scandes forest‐tundra ecotone

Mycorrhizal associations are widespread in high‐latitude ecosystems and are potentially of great importance for global carbon dynamics. Although large herbivores play a key part in shaping subarctic plant communities, their impact on mycorrhizal dynamics is largely unknown. We measured extramatrical mycelial (EMM) biomass during one growing season in 16‐year‐old herbivore exclosures and unenclosed control plots (ambient), at three mountain birch forests and two shrub heath sites, in the Scandes forest‐tundra ecotone. We also used high‐throughput amplicon sequencing for taxonomic identification to investigate differences in fungal species composition. At the birch forest sites, EMM biomass was significantly higher in exclosures (1.36 ± 0.43 g C/m²) than in ambient conditions (0.66 ± 0.17 g C/m²) and was positively influenced by soil thawing degree‐days. At the shrub heath sites, there was no significant effect on EMM biomass (exclosures: 0.72 ± 0.09 g C/m²; ambient plots: 1.43 ± 0.94). However, EMM biomass was negatively related to Betula nana abundance, which was greater in exclosures, suggesting that grazing affected EMM biomass positively. We found no significant treatment effects on fungal diversity but the most abundant ectomycorrhizal lineage/cortinarius, showed a near‐significant positive effect of herbivore exclusion (p = .08), indicating that herbivory also affects fungal community composition. These results suggest that herbivory can influence fungal biomass in highly context‐dependent ways in subarctic ecosystems. Considering the importance of root‐associated fungi for ecosystem carbon balance, these findings could have far‐reaching implications.     

Belowground carbon flux links biogeochemical cycles and resource‐use efficiency at the global scale

Nutrient limitation is pervasive in the terrestrial biosphere, although the relationship between global carbon (C) nitrogen (N) and phosphorus (P) cycles remains uncertain. Using meta‐analysis we show that gross primary production (GPP) partitioning belowground is inversely related to soil‐available N : P, increasing with latitude from tropical to boreal forests. N‐use efficiency is highest in boreal forests, and P‐use efficiency in tropical forests. High C partitioning belowground in boreal forests reflects a 13‐fold greater C cost of N acquisition compared to the tropics. By contrast, the C cost of P acquisition varies only 2‐fold among biomes. This analysis suggests a new hypothesis that the primary limitation on productivity in forested ecosystems transitions from belowground resources at high latitudes to aboveground resources at low latitudes as C‐intensive root‐ and mycorrhizal‐mediated nutrient capture is progressively replaced by rapidly cycling, enzyme‐derived nutrient fluxes when temperatures approach the thermal optimum for biogeochemical transformations.