Biodiversity mitigates drought effects in the decomposer system across biomes.

Multiple facets of global change affect the earth system interactively, with complex consequences for ecosystem functioning and stability. Simultaneous climate and biodiversity change are of particular concern, because biodiversity may contribute to ecosystem resistance and resilience and may mitigate climate change impacts. Yet, the extent and generality of how climate and biodiversity change interact remain insufficiently understood, especially for the decomposition of organic matter, a major determinant of the biosphere-atmosphere carbon feedbacks. With an inter-biome field experiment using large rainfall exclusion facilities, we tested how drought, a common prediction of climate change models for many parts of the world, and biodiversity in the decomposer system drive decomposition in forest ecosystems interactively. Decomposing leaf litter lost less carbon (C) and especially nitrogen (N) in five different forest biomes following partial rainfall exclusion compared to conditions without rainfall exclusion. An increasing complexity of the decomposer community alleviated drought effects, with full compensation when large-bodied invertebrates were present. Leaf litter mixing increased diversity effects, with increasing litter species richness, which contributed to counteracting drought effects on C and N loss, although to a much smaller degree than decomposer community complexity. Our results show at a relevant spatial scale covering distinct climate zones that both, the diversity of decomposer communities and plant litter in forest floors have a strong potential to mitigate drought effects on C and N dynamics during decomposition. Preserving biodiversity at multiple trophic levels contributes to ecosystem resistance and appears critical to maintain ecosystem processes under ongoing climate change.

Climate dependence of the macrofaunal effect on litter decomposition-A global meta-regression analysis.

Litter decomposition by microorganisms and animals is influenced by climate and has been found to be higher in warm and wet than in cold and dry biomes. We, however, hypothesized that the macrofaunal effect on decomposition should increase with temperature and aridity since larger animals are more tolerant to aridity than smaller organisms. This hypothesis was supported by our global analysis of macrofauna exclusion studies. Macrofauna increased litter mass loss on average by 40%, twofold higher than the highest previous estimation of macrofaunal effect on decomposition. The strongest effect was found in subtropical deserts where faunal decomposition had not been considered important. Our results highlight the need to consider animal size when exploring climate dependence of faunal decomposition, and the disproportionately large role of macrofauna in regulating litter decomposition in warm drylands. This new realization is critical for understanding element cycling in the face of global warming and aridification.

Global contribution of invertebrates to forest litter decomposition.

Forest litter decomposition is an essential component of global carbon and nutrient turnover. Invertebrates play important roles in litter decomposition, but the regional pattern of their effects is poorly understood. We examined 476 case studies across 93 sites and performed a meta-analysis to estimate regional effects of invertebrates on forest litter decomposition. We then assessed how invertebrate diversity, climate and soil pH drive regional variations in invertebrate-mediated decomposition. We found that (1) invertebrate contributions to litter decomposition are 1.4 times higher in tropical and subtropical forests than in forests elsewhere, with an overall contribution of 31% to global forest litter decomposition; and (2) termite diversity, together with warm, humid and acidic environments in the tropics and subtropics are positively associated with forest litter decomposition by invertebrates. Our results demonstrate the significant difference in invertebrate effects on mediating forest litter decomposition among regions. We demonstrate, also, the significance of termites in driving litter mass loss in the tropics and subtropics. These results are particularly pertinent in the tropics and subtropics where climate change and human disturbance threaten invertebrate biodiversity and the ecosystem services it provides.

Evolutionary and ecological forces shape nutrient strategies of mycorrhizal woody plants.

The associations of arbuscular mycorrhizal (AM) or ectomycorrhiza (EcM) fungi with plants have sequentially evolved and significantly contributed to enhancing plant nutrition. Nonetheless, how evolutionary and ecological forces drive nutrient acquisition strategies of AM and EcM woody plants remains poorly understood. Our global analysis of woody species revealed that, over divergence time, AM woody plants evolved faster nitrogen mineralization rates without changes in nitrogen resorption. However, EcM woody plants exhibited an increase in nitrogen mineralization but a decrease in nitrogen resorption, indicating a shift towards a more inorganic nutrient economy. Despite this alteration, when evaluating present-day woody species, AM woody plants still display faster nitrogen mineralization and lower nitrogen resorption than EcM woody plants. This inorganic nutrient economy allows AM woody plants to thrive in warm environments with a faster litter decomposition rate. Our findings indicate that the global pattern of nutrient acquisition strategies in mycorrhizal plants is shaped by the interplay between phylogeny and climate.

Reading tea leaves worldwide: Decoupled drivers of initial litter decomposition mass-loss rate and stabilization.

The breakdown of plant material fuels soil functioning and biodiversity. Currently, process understanding of global decomposition patterns and the drivers of such patterns are hampered by the lack of coherent large-scale datasets. We buried 36,000 individual litterbags (tea bags) worldwide and found an overall negative correlation between initial mass-loss rates and stabilization factors of plant-derived carbon, using the Tea Bag Index (TBI). The stabilization factor quantifies the degree to which easy-to-degrade components accumulate during early-stage decomposition (e.g. by environmental limitations). However, agriculture and an interaction between moisture and temperature led to a decoupling between initial mass-loss rates and stabilization, notably in colder locations. Using TBI improved mass-loss estimates of natural litter compared to models that ignored stabilization. Ignoring the transformation of dead plant material to more recalcitrant substances during early-stage decomposition, and the environmental control of this transformation, could overestimate carbon losses during early decomposition in carbon cycle models.

Roots selectively decompose litter to mine nitrogen and build new soil carbon.

Plant-microbe interactions in the rhizosphere shape carbon and nitrogen cycling in soil organic matter (SOM). However, there is conflicting evidence on whether these interactions lead to a net loss or increase of SOM. In part, this conflict is driven by uncertainty in how living roots and microbes alter SOM formation or loss in the field. To address these uncertainties, we traced the fate of isotopically labelled litter into SOM using root and fungal ingrowth cores incubated in a Miscanthus x giganteus field. Roots stimulated litter decomposition, but balanced this loss by transferring carbon into aggregate associated SOM. Further, roots selectively mobilized nitrogen from litter without additional carbon release. Overall, our findings suggest that roots mine litter nitrogen and protect soil carbon.

Photodegradation in terrestrial ecosystems.

The first step in carbon (C) turnover, where senesced plant biomass is converted through various pathways into compounds that are released to the atmosphere or incorporated into the soil, is termed litter decomposition. This review is focused on recent advances of how solar radiation can affect this important process in terrestrial ecosystems. We explore the photochemical degradation of plant litter and its consequences for biotic decomposition and C cycling. The ubiquitous presence of lignin in plant tissues poses an important challenge for enzymatic litter decomposition due to its biological recalcitrance, creating a substantial bottleneck for decomposer organisms. The recognition that lignin is also photolabile and can be rapidly altered by natural doses of sunlight to increase access to cell wall carbohydrates and even bolster the activity of cell wall degrading enzymes highlights a novel role for lignin in modulating rates of litter decomposition. Lignin represents a key functional connector between photochemistry and biochemistry with important consequences for our understanding of how sunlight exposure may affect litter decomposition in a wide range of terrestrial ecosystems. A mechanistic understanding of how sunlight controls litter decomposition and C turnover can help inform management and other decisions related to mitigating human impact on the planet.

Modelling optimal ligninolytic activity during plant litter decomposition.

A large fraction of plant litter comprises recalcitrant aromatic compounds (lignin and other phenolics). Quantifying the fate of aromatic compounds is difficult, because oxidative degradation of aromatic carbon (C) is a costly but necessary endeavor for microorganisms, and we do not know when gains from the decomposition of aromatic C outweigh energetic costs. To evaluate these tradeoffs, we developed a litter decomposition model in which the aromatic C decomposition rate is optimized dynamically to maximize microbial growth for the given costs of maintaining ligninolytic activity. We tested model performance against > 200 litter decomposition datasets collected from published literature and assessed the effects of climate and litter chemistry on litter decomposition. The model predicted a time-varying ligninolytic oxidation rate, which was used to calculate the lag time before the decomposition of aromatic C is initiated. Warmer conditions increased decomposition rates, shortened the lag time of aromatic C oxidation, and improved microbial C-use efficiency by decreasing the costs of oxidation. Moreover, a higher initial content of aromatic C promoted an earlier start of aromatic C decomposition under any climate. With this contribution, we highlight the application of eco-evolutionary approaches based on optimized microbial life strategies as an alternative parametrization scheme for litter decomposition models.

A trait-based framework linking the soil metabolome to plant-soil feedbacks.

By modifying the biotic and abiotic properties of the soil, plants create soil legacies that can affect vegetation dynamics through plant-soil feedbacks (PSF). PSF are generally attributed to reciprocal effects of plants and soil biota, but these interactions can also drive changes in the identity, diversity and abundance of soil metabolites, leading to more or less persistent soil chemical legacies whose role in mediating PSF has rarely been considered. These chemical legacies may interact with microbial or nutrient legacies to affect species coexistence. Given the ecological importance of chemical interactions between plants and other organisms, a better understanding of soil chemical legacies is needed in community ecology. In this Viewpoint, we aim to: highlight the importance of belowground chemical interactions for PSF; define and integrate soil chemical legacies into PSF research by clarifying how the soil metabolome can contribute to PSF; discuss how functional traits can help predict these plant-soil interactions; propose an experimental approach to quantify plant responses to the soil solution metabolome; and describe a testable framework relying on root economics and seed dispersal traits to predict how plant species affect the soil metabolome and how they could respond to soil chemical legacies.

Climate warming accelerates carbon release from foliar litter-A global synthesis.

With over one-third of terrestrial net primary productivity transferring to the litter layer annually, the carbon release from litter serves as a crucial valve in atmospheric carbon dioxide concentrations. However, few quantitative global projections of litter carbon release rate in response to climate change exist. Here, we combined a global foliar litter carbon release dataset (8973 samples) to generate spatially explicitly estimates of the response of their residence time (τ) to climate change. Results show a global mean litter carbon release rate ( k $$ k $$ ) of 0.69 year-1 (ranging from 0.09-5.6 year-1). Under future climate scenarios, global mean τ is projected to decrease by a mean of 2.7% (SSP 1-2.6) and 5.9% (SSP 5-8.5) during 2071-2100 period. Locally, the alleviation of temperature and moisture restrictions corresponded to obvious decreases in τ in cold and arid regions, respectively. In contract, τ in tropical humid broadleaf forests increased by 4.6% under SSP 5-8.5. Our findings highlight the vegetation type as a powerful proxy for explaining global patterns in foliar litter carbon release rates and the role of climate conditions in predicting responses of carbon release to climate change. Our observation-based estimates could refine carbon cycle parameterization, improving projections of carbon cycle-climate feedbacks.

Dieback and Replacement of Riparian Trees May Impact Stream Ecosystem Functioning.

Alders are nitrogen (N)-fixing riparian trees that promote leaf litter decomposition in streams through their high-nutrient leaf litter inputs. While alders are widespread across Europe, their populations are at risk due to infection by the oomycete Phytophthora ×alni, which causes alder dieback. Moreover, alder death opens a space for the establishment of an aggressive N-fixing invasive species, the black locust (Robinia pseudoacacia). Shifts from riparian vegetation containing healthy to infected alder and, eventually, alder loss and replacement with black locust may alter the key process of leaf litter decomposition and associated microbial decomposer assemblages. We examined this question in a microcosm experiment comparing three types of leaf litter mixtures: one representing an original riparian forest composed of healthy alder (Alnus lusitanica), ash (Fraxinus angustifolia), and poplar (Populus nigra); one with the same species composition where alder had been infected by P. ×alni; and one where alder had been replaced with black locust. The experiment lasted six weeks, and every two weeks, microbially driven decomposition, fungal biomass, reproduction, and assemblage structure were measured. Decomposition was highest in mixtures with infected alder and lowest in mixtures with black locust, reflecting differences in leaf nutrient concentrations. Mixtures with alder showed distinct fungal assemblages and higher sporulation rates than mixtures with black locust. Our results indicate that alder loss and its replacement with black locust may alter key stream ecosystem processes and assemblages, with important changes already occurring during alder infection. This highlights the importance of maintaining heathy riparian forests to preserve proper stream ecosystem functioning.

Mechanical traits as drivers of trophic interaction between macrodetritivores and leaf litter.

In ecosystems, the rates of resource consumption by animals drive the flows of matter and energy. Consumption rates are known to vary according to consumer energy requirements, resource nutrient content and mechanical properties. The aim of our study is to determine how mechanical constraints, compared to energetic and nutritional constraints, explain the variation in leaf litter consumption rates by macrodetritivores. In particular, we focus on the impact of litter toughness. To this end, we propose a non-linear model describing leaf litter consumption rates of detritivore as a function of litter toughness. We also investigate a possible match between bite force and litter toughness, since consumer-resource co-occurrence is thought to be driven by the match between invertebrate mandibular traits and resource toughness. Our study was designed as follows: leaf litter from oak and hornbeam was exposed to field physical and microbial decomposition in aquatic and terrestrial ecosystems for selected time periods before it was offered to eight macrodetritivore taxa (three forest stream taxa and five forest soil taxa) in no-choice laboratory feeding experiments. Our findings show that, compared to energetic and nutritional constraints, mechanical traits have a greater impact on litter consumption rate by detritivores. After subtracting the contribution of the detritivore body mass, we report that litter consumption rates depend primarily on litter toughness. A sigmoid function is best suited to characterize the relationship between mass-independent consumption rate and litter toughness. We note that the parameters of our sigmoid model are taxon-specific, suggesting biomechanical thresholds and biological differences among taxa. Interestingly, we found no correlation with detritivore bite force, suggesting that food processing by detritivores does not only depend on mandibles strength.

Functional rarity and evenness are key facets of biodiversity to boost multifunctionality.

The functional traits of organisms within multispecies assemblages regulate biodiversity effects on ecosystem functioning. Yet how traits should assemble to boost multiple ecosystem functions simultaneously (multifunctionality) remains poorly explored. In a multibiome litter experiment covering most of the global variation in leaf trait spectra, we showed that three dimensions of functional diversity (dispersion, rarity, and evenness) explained up to 66% of variations in multifunctionality, although the dominant species and their traits remained an important predictor. While high dispersion impeded multifunctionality, increasing the evenness among functionally dissimilar species was a key dimension to promote higher multifunctionality and to reduce the abundance of plant pathogens. Because too-dissimilar species could have negative effects on ecosystems, our results highlight the need for not only diverse but also functionally even assemblages to promote multifunctionality. The effect of functionally rare species strongly shifted from positive to negative depending on their trait differences with the dominant species. Simultaneously managing the dispersion, evenness, and rarity in multispecies assemblages could be used to design assemblages aimed at maximizing multifunctionality independently of the biome, the identity of dominant species, or the range of trait values considered. Functional evenness and rarity offer promise to improve the management of terrestrial ecosystems and to limit plant disease risks.

Nitrogen addition accelerates litter decomposition and arsenic release of Pteris vittata in arsenic-contaminated soil from mine.

The arsenic (As) release from litter decomposition of As-hyperaccumulator (Pteris vittata L.) in mine areas poses an ecological risk for metal dispersion into the soil. However, the effect of atmospheric nitrogen (N) deposition on the litter decomposition of As-hyperaccumulator in the tailing mine area remains poorly understood. In this study, we conducted a microcosm experiment to investigate the As release during the decomposition of P. vittata litter under four gradients of N addition (0, 5, 10, and 20 mg N g-1). The N10 treatment (10 mg N g-1) enhanced As release from P. vittata litter by 1.2-2.6 folds compared to control. Furthermore, Streptomyces, Pantoea, and Curtobacterium were found to primarily affect the As release during the litter decomposition process. Additionally, N addition decreased the soil pH, subsequently increased the microbial biomass, as well as hydrolase activities (NAG) which regulated N release. Thereby, N addition increased the As release from P. vittata litter and then transferred to the soil. Moreover, this process caused a transformation of non-labile As fractions into labile forms, resulting in an increase of available As concentration by 13.02-20.16% within the soil after a 90-day incubation period. Our findings provide valuable insights into assessing the ecological risk associated with As release from the decomposition of P. vittata litter towards the soil, particularly under elevated atmospheric N deposition.

Microbial nutrient limitation and carbon use efficiency changes under different degrees of litter decomposition.

Alpine ecosystems are important terrestrial carbon (C) pools, and microbial decomposers play a key role in litter decomposition. Microbial metabolic limitations in these ecosystems, however, remain unclear. The objectives of this study aim to elucidate the characteristics of microbial nutrient limitation and their C use efficiency (CUE), and to evaluate their response to environmental factors. Five ecological indicators were utilized to assess and compare the degree of microbial elemental homeostasis and the nutrient limitations of the microbial communities among varying stages of litter decomposition (L, F, and H horizon) along an altitudinal gradient (2800, 3000, 3250, and 3500 m) under uniform vegetation (Abies fabri) on Gongga Mountain, eastern Tibetan Plateau. In this study, microorganisms in the litter reached a strictly homeostatic of C content exclusively during the middle stage of litter decomposition (F horizon). Based on the stoichiometry of soil enzymes, we observed that microbial N- and P-limitation increased during litter degradation, but that P-limitation was stronger than N-limitation at the late stages of degradation (H horizon). Furthermore, an increase in microbial CUE corresponded with a reduction in microbial C-limitation. Additionally, redundancy analysis (RDA) based on forward selection further showed that microbial biomass C (MBC) is closely associated with the enzyme activities and their ratios, and MBC was also an important factor in characterizing changes in microbial nutrient limitation and CUE. Our findings suggest that variations in MBC, rather than N- and P-related components, predominantly influence microbial metabolic processes during litter decomposition on Gongga Mountain, eastern Tibetan Plateau.

Functional identity drives tree species richness-induced increases in litterfall production and forest floor mass in young tree communities.

Forest floor accumulation is a key process that influences ecosystem carbon cycling. Despite evidence suggesting that tree diversity and soil carbon are positively correlated, most soil carbon studies typically omit the response of the forest floor carbon to tree diversity loss. Here, we evaluated how tree species richness affects forest floor mass and how this effect is mediated by litterfall production and forest floor decay rate in a tree diversity experiment in a subtropical forest. We observed that greater tree species richness leads to higher forest floor accumulation at the soil surface through increasing litterfall production - positively linked to functional trait identity (i.e. community-weighted mean functional trait) rather than functional diversity - and unchanged forest floor decay. Interestingly, structural equation modelling revealed that this lack of overall significant tree species richness effect on forest floor decay rate was due to two indirect and opposite effects cancelling each other out. Indeed, tree species richness increased forest floor decay rate through increasing litterfall production while decreasing forest floor decay rate by increasing litter species richness. Our reports of greater organic matter accumulation in the forest floor in species-rich forests suggest that tree diversity may have long-term and important effect on ecosystem carbon cycling and services.

Fungal community composition and genetic potential regulate fine root decay in northern temperate forests.

Understanding how genetic differences among soil microorganisms regulate spatial patterns in litter decay remains a persistent challenge in ecology. Despite fine root litter accounting for ~50% of total litter production in forest ecosystems, far less is known about the microbial decay of fine roots relative to aboveground litter. Here, we evaluated whether fine root decay occurred more rapidly where fungal communities have a greater genetic potential for litter decay. Additionally, we tested if linkages between decay and fungal genes can be adequately captured by delineating saprotrophic and ectomycorrhizal fungal functional groups based on whether they have genes encoding certain ligninolytic class II peroxidase enzymes, which oxidize lignin and polyphenolic compounds. To address these ideas, we used a litterbag study paired with fungal DNA barcoding to characterize fine root decay rates and fungal community composition at the landscape scale in northern temperate forests, and we estimated the genetic potential of fungal communities for litter decay using publicly available genomes. Fine root decay occurred more rapidly where fungal communities had a greater genetic potential for decay, especially of cellulose and hemicellulose. Fine root decay was positively correlated with ligninolytic saprotrophic fungi and negatively correlated with ECM fungi with ligninolytic peroxidases, likely because these saprotrophic and ectomycorrhizal functional groups had the highest and lowest genetic potentials for plant cell wall degradation, respectively. These fungal variables overwhelmed direct environmental controls, suggesting fungal community composition and genetic variation are primary controls over fine root decay in temperate forests at regional scales.

Litter and soil biodiversity jointly drive ecosystem functions.

The decomposition of litter and the supply of nutrients into and from the soil are two fundamental processes through which the above- and belowground world interact. Microbial biodiversity, and especially that of decomposers, plays a key role in these processes by helping litter decomposition. Yet the relative contribution of litter diversity and soil biodiversity in supporting multiple ecosystem services remains virtually unknown. Here we conducted a mesocosm experiment where leaf litter and soil biodiversity were manipulated to investigate their influence on plant productivity, litter decomposition, soil respiration, and enzymatic activity in the littersphere. We showed that both leaf litter diversity and soil microbial diversity (richness and community composition) independently contributed to explain multiple ecosystem functions. Fungal saprobes community composition was especially important for supporting ecosystem multifunctionality (EMF), plant production, litter decomposition, and activity of soil phosphatase when compared with bacteria or other fungal functional groups and litter species richness. Moreover, leaf litter diversity and soil microbial diversity exerted previously undescribed and significantly interactive effects on EMF and multiple individual ecosystem functions, such as litter decomposition and plant production. Together, our work provides experimental evidence supporting the independent and interactive roles of litter and belowground soil biodiversity to maintain ecosystem functions and multiple services.

Resolving the influence of lignin on soil organic matter decomposition with mechanistic models and continental-scale data.

Confidence in model estimates of soil CO2 flux depends on assumptions regarding fundamental mechanisms that control the decomposition of litter and soil organic carbon (SOC). Multiple hypotheses have been proposed to explain the role of lignin, an abundant and complex biopolymer that may limit decomposition. We tested competing mechanisms using data-model fusion with modified versions of the CN-SIM model and a 571-day laboratory incubation dataset where decomposition of litter, lignin, and SOC was measured across 80 soil samples from the National Ecological Observatory Network. We found that lignin decomposition consistently decreased over time in 65 samples, whereas in the other 15 samples, lignin decomposition subsequently increased. These "lagged-peak" samples can be predicted by low soil pH, high extractable Mn, and fungal community composition as measured by ITS PC2 (the second principal component of an ordination of fungal ITS amplicon sequences). The highest-performing model incorporated soil biogeochemical factors and daily dynamics of substrate availability (labile bulk litter:lignin) that jointly represented two hypotheses (C substrate limitation and co-metabolism) previously thought to influence lignin decomposition. In contrast, models representing either hypothesis alone were biased and underestimated cumulative decomposition. Our findings reconcile competing hypotheses of lignin decomposition and suggest the need to precisely represent the role of lignin and consider soil metal and fungal characteristics to accurately estimate decomposition in Earth-system models.

Mycorrhizae enhance reactive minerals but reduce mineral-associated carbon.

Soil organic carbon (C) is the largest active C pool of Earth's surface and is thus vital in sustaining terrestrial productivity and climate stability. Arbuscular mycorrhizal fungi (AMF) form symbioses with most terrestrial plants and critically modulate soil C dynamics. Yet, it remains unclear whether and how AMF-root associations (i.e., mycorrhizae) interact with soil minerals to affect soil C cycling. Here we showed that the presence of both roots and AMF increased soil dissolved organic C and reactive Fe minerals, as well as litter decomposition and soil CO2 emissions. However, it reduced mineral-associated C. Also, high-resolution nanoscale secondary ion mass spectrometry images showed the existence of a thin coating (0.5-1.0 µm thick) of 56 Fe16 O- (Fe minerals) on the surface of 12 C14 N- (fungal biomass), illustrating the close physical association between fungal hyphae and soil Fe minerals. In addition, AMF genera were divergently related to reactive Fe minerals, with Glomus being positively but Paraglomus and Acaulospora negatively correlated with reactive Fe minerals. Moreover, the presence of roots and AMF, particularly when combined with litter addition, enhanced the abundances of several critical soil bacterial genera that are associated with the formation of reactive minerals in soils. A conceptual framework was further proposed to illustrate how AMF-root associations impact soil C cycling in the rhizosphere. Briefly, root exudates and the inoculated AMF not only stimulated the decomposition of litter and SOC and promoted the production of CO2 emission, but also drove soil C persistence by unlocking mineral elements and promoting the formation of reactive minerals. Together, these findings provide new insights into the mechanisms that underlie the formation of reactive minerals and have significant implications for understanding and managing soil C persistence.