General reversal of N-decomposition relationship during long-term decomposition in boreal and temperate forests.

Decomposition of dead organic matter is fundamental to carbon (C) and nutrient cycling in terrestrial ecosystems, influencing C fluxes from the biosphere to the atmosphere. Theory predicts and evidence strongly supports that the availability of nitrogen (N) limits litter decomposition. Positive relationships between substrate N concentrations and decomposition have been embedded into ecosystem models. This decomposition paradigm, however, relies on data mostly from short-term studies analyzing controls on early-stage decomposition. We present evidence from three independent long-term decomposition investigations demonstrating that the positive N-decomposition relationship is reversed and becomes negative during later stages of decomposition. First, in a 10-y decomposition experiment across 62 woody species in a temperate forest, leaf litter with higher N concentrations exhibited faster initial decomposition rates but ended up a larger recalcitrant fraction decomposing at a near-zero rate. Second, in a 5-y N-enrichment experiment of two tree species, leaves with experimentally enriched N concentrations had faster decomposition initial rates but ultimately accumulated large slowly decomposing fractions. Measures of amino sugars on harvested litter in two experiments indicated that greater accumulation of microbial residues in N-rich substrates likely contributed to larger slowly decomposing fractions. Finally, a database of 437 measurements from 120 species in 45 boreal and temperate forest sites confirmed that higher N concentrations were associated with a larger slowly decomposing fraction. These results challenge the current treatment of interactions between N and decomposition in many ecosystems and Earth system models and suggest that even the best-supported short-term controls of biogeochemical processes might not predict long-term controls.

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.

Microclimate modulation: An overlooked mechanism influencing the impact of plant diversity on ecosystem functioning.

Changes in climate and biodiversity are widely recognized as primary global change drivers of ecosystem structure and functioning, also affecting ecosystem services provided to human populations. Increasing plant diversity not only enhances ecosystem functioning and stability but also mitigates climate change effects and buffers extreme weather conditions, yet the underlying mechanisms remain largely unclear. Recent studies have shown that plant diversity can mitigate climate change (e.g. reduce temperature fluctuations or drought through microclimatic effects) in different compartments of the focal ecosystem, which as such may contribute to the effect of plant diversity on ecosystem properties and functioning. However, these potential plant diversity-induced microclimate effects are not sufficiently understood. Here, we explored the consequences of climate modulation through microclimate modification by plant diversity for ecosystem functioning as a potential mechanism contributing to the widely documented biodiversity-ecosystem functioning (BEF) relationships, using a combination of theoretical and simulation approaches. We focused on a diverse set of response variables at various levels of integration ranging from ecosystem-level carbon exchange to soil enzyme activity, including population dynamics and the activity of specific organisms. Here, we demonstrated that a vegetation layer composed of many plant species has the potential to influence ecosystem functioning and stability through the modification of microclimatic conditions, thus mitigating the negative impacts of climate extremes on ecosystem functioning. Integrating microclimatic processes (e.g. temperature, humidity and light modulation) as a mechanism contributing to the BEF relationships is a promising avenue to improve our understanding of the effects of climate change on ecosystem functioning and to better predict future ecosystem structure, functioning and services. In addition, microclimate management and monitoring should be seen as a potential tool by practitioners to adapt ecosystems to climate change.

Increasing rates of long-term nitrogen deposition consistently increased litter decomposition in a semi-arid grassland.

The continuing nitrogen (N) deposition observed worldwide alters ecosystem nutrient cycling and ecosystem functioning. Litter decomposition is a key process contributing to these changes, but the numerous mechanisms for altered decomposition remain poorly identified. We assessed these different mechanisms with a decomposition experiment using litter from four abundant species (Achnatherum sibiricum, Agropyron cristatum, Leymus chinensis and Stipa grandis) and litter mixtures representing treatment-specific community composition in a semi-arid grassland under long-term simulation of six different rates of N deposition. Decomposition increased consistently with increasing rates of N addition in all litter types. Higher soil manganese (Mn) availability, which apparently was a consequence of N addition-induced lower soil pH, was the most important factor for faster decomposition. Soil C : N ratios were lower with N addition that subsequently led to markedly higher bacterial to fungal ratios, which also stimulated litter decomposition. Several factors contributed jointly to higher rates of litter decomposition in response to N deposition. Shifts in plant species composition and litter quality played a minor role compared to N-driven reductions in soil pH and C : N, which increased soil Mn availability and altered microbial community structure. The soil-driven effect on decomposition reported here may have long-lasting impacts on nutrient cycling, soil organic matter dynamics and ecosystem functioning.

Carbon limitation overrides acidification in mediating soil microbial activity to nitrogen enrichment in a temperate grassland.

Higher ecosystem nitrogen (N) inputs resulting from human activities often suppress soil microbial biomass and respiration, thereby altering biogeochemical cycling. Soil acidification and carbon (C) limitation may drive these microbial responses, yet their relative importance remains elusive, which limits our understanding of the longer term effects of increasing N inputs. In a field experiment with continuous N addition at seven different rates from 0 to 50 g N m-2  year-1 over 6 years in a temperate grassland of Inner Mongolia, China, we examined the responses of soil microbial biomass and respiration to changes in soil acidity and C availability by adding lime and/or glucose to soil samples. Soil microbial biomass and respiration did only weakly respond to increasing soil pH, but increased strongly in response to higher C availability with increasing N addition rates. Soil net N immobilization increased in response to glucose addition, and soil microbial biomass increased at higher rates than microbial respiration along the gradient of previous N addition rates, both suggesting increasingly reinforced microbial C limitation with increasing N addition. Our results provide clear evidence for strong N-induced microbial C limitation, but only little support for soil acidity effects within the initial pH range of 4.73-7.86 covered by our study. Field data support this conclusion by showing reduced plant C allocation belowground in response to N addition, resulting in soil microbial C starvation over the long term. In conclusion, soil microbial biomass and respiration under N addition were strongly dependent on C availability, most likely originating from plant belowground C inputs, and was much less affected by changes in soil pH. Our data help clarify a long-standing debate about how increasing N input rates affect soil microbial biomass and respiration, and improve the mechanistic understanding of the linkages between ecosystem N enrichment and C cycling.

Relative importance of tree species richness, tree functional type, and microenvironment for soil macrofauna communities in European forests.

Soil fauna communities are major drivers of many forest ecosystem processes. Tree species diversity and composition shape soil fauna communities, but their relationships are poorly understood, notably whether or not soil fauna diversity depends on tree species diversity. Here, we characterized soil macrofauna communities from forests composed of either one or three tree species, located in four different climate zones and growing on different soil types. Using multivariate analysis and model averaging we investigated the relative importance of tree species richness, tree functional type (deciduous vs. evergreen), litter quality, microhabitat and microclimatic characteristics as drivers of soil macrofauna community composition and structure. We found that macrofauna communities in mixed forest stands were represented by a higher number of broad taxonomic groups that were more diverse and more evenly represented. We also observed a switch from earthworm-dominated to predator-dominated communities with increasing evergreen proportion in forest stands, which we interpreted as a result of a lower litter quality and a higher forest floor mass. Finally, canopy openness was positively related to detritivore abundance and biomass, leading to higher predator species richness and diversity probably through trophic cascade effects. Interestingly, considering different levels of taxonomic resolution in the analyses highlighted different facets of macrofauna response to tree species richness, likely a result of both different ecological niche range and methodological constraints. Overall, our study supports the positive effects of tree species richness on macrofauna diversity and abundance through multiple changes in resource quality and availability, microhabitat, and microclimate modifications.

Contrasting dynamics and trait controls in first-order root compared with leaf litter decomposition.

Decomposition is a key component of the global carbon (C) cycle, yet current ecosystem C models do not adequately represent the contributions of plant roots and their mycorrhizae to this process. The understanding of decomposition dynamics and their control by traits is particularly limited for the most distal first-order roots. Here we followed decomposition of first-order roots and leaf litter from 35 woody plant species differing in mycorrhizal type over 6 years in a Chinese temperate forest. First-order roots decomposed more slowly (k = 0.11 ± 0.01 years-1) than did leaf litter (0.35 ± 0.02 years-1), losing only 35% of initial mass on average after 6 years of exposure in the field. In contrast to leaf litter, nonlignin root C chemistry (nonstructural carbohydrates, polyphenols) accounted for 82% of the large interspecific variation in first-order root decomposition. Leaf litter from ectomycorrhizal (EM) species decomposed more slowly than that from arbuscular mycorrhizal (AM) species, whereas first-order roots of EM species switched, after 2 years, from having slower to faster decomposition compared with those from AM species. The fundamentally different dynamics and control mechanisms of first-order root decomposition compared with those of leaf litter challenge current ecosystem C models, the recently suggested dichotomy between EM and AM plants, and the idea that common traits can predict decomposition across roots and leaves. Aspects of C chemistry unrelated to lignin or nitrogen, and not presently considered in decomposition models, controlled first-order root decomposition; thus, current paradigms of ecosystem C dynamics and model parameterization require revision.

Neighbor identity affects growth and survival of Mediterranean plants under recurrent drought.

The increasing intensity and frequency of droughts predicted for the Mediterranean basin with ongoing climate change will impact plant communities and ecosystem functioning. This study investigated the effect of severe recurrent droughts and the role of the neighbor plant identity on the growth and survival of three abundant and co-existing species of a typical Mediterranean shrubland. Two juvenile plants, either of the same species or in all possible combinations of the two woody species Quercus coccifera and Cistus albidus and the perennial grass species Brachypodium retusum were grown together in rhizotrons under controlled watering regimes for two years. Compared to a treatment with only one drought cycle, three successive droughts reduced the relative growth rates (RGR) of shoots and roots in B. retusum, but not in woody species, and increased the mortality of the woody species, but not that of the grass. The survival of C. albidus and of B. retusum, but not of Q. coccifera, increased when the neighbor individual was a different species than when it was the same species. Our data suggest that both species composition and frequency of drought events will impact the dynamics of plant communities in Mediterranean shrublands under ongoing climate change. The abundance of dehydration sensitive woody species will likely decrease under more frequent drought events at the expense of dehydration-tolerant grass species, resulting in potentially strong changes in the functioning of these ecosystems.

Consequences of biodiversity loss for litter decomposition across biomes.

The decomposition of dead organic matter is a major determinant of carbon and nutrient cycling in ecosystems, and of carbon fluxes between the biosphere and the atmosphere. Decomposition is driven by a vast diversity of organisms that are structured in complex food webs. Identifying the mechanisms underlying the effects of biodiversity on decomposition is critical given the rapid loss of species worldwide and the effects of this loss on human well-being. Yet despite comprehensive syntheses of studies on how biodiversity affects litter decomposition, key questions remain, including when, where and how biodiversity has a role and whether general patterns and mechanisms occur across ecosystems and different functional types of organism. Here, in field experiments across five terrestrial and aquatic locations, ranging from the subarctic to the tropics, we show that reducing the functional diversity of decomposer organisms and plant litter types slowed the cycling of litter carbon and nitrogen. Moreover, we found evidence of nitrogen transfer from the litter of nitrogen-fixing plants to that of rapidly decomposing plants, but not between other plant functional types, highlighting that specific interactions in litter mixtures control carbon and nitrogen cycling during decomposition. The emergence of this general mechanism and the coherence of patterns across contrasting terrestrial and aquatic ecosystems suggest that biodiversity loss has consistent consequences for litter decomposition and the cycling of major elements on broad spatial scales.

Biotic homogenization can decrease landscape-scale forest multifunctionality.

Many experiments have shown that local biodiversity loss impairs the ability of ecosystems to maintain multiple ecosystem functions at high levels (multifunctionality). In contrast, the role of biodiversity in driving ecosystem multifunctionality at landscape scales remains unresolved. We used a comprehensive pan-European dataset, including 16 ecosystem functions measured in 209 forest plots across six European countries, and performed simulations to investigate how local plot-scale richness of tree species (α-diversity) and their turnover between plots (ß-diversity) are related to landscape-scale multifunctionality. After accounting for variation in environmental conditions, we found that relationships between α-diversity and landscape-scale multifunctionality varied from positive to negative depending on the multifunctionality metric used. In contrast, when significant, relationships between ß-diversity and landscape-scale multifunctionality were always positive, because a high spatial turnover in species composition was closely related to a high spatial turnover in functions that were supported at high levels. Our findings have major implications for forest management and indicate that biotic homogenization can have previously unrecognized and negative consequences for large-scale ecosystem multifunctionality.

Continental mapping of forest ecosystem functions reveals a high but unrealised potential for forest multifunctionality.

Humans require multiple services from ecosystems, but it is largely unknown whether trade-offs between ecosystem functions prevent the realisation of high ecosystem multifunctionality across spatial scales. Here, we combined a comprehensive dataset (28 ecosystem functions measured on 209 forest plots) with a forest inventory dataset (105,316 plots) to extrapolate and map relationships between various ecosystem multifunctionality measures across Europe. These multifunctionality measures reflected different management objectives, related to timber production, climate regulation and biodiversity conservation/recreation. We found that trade-offs among them were rare across Europe, at both local and continental scales. This suggests a high potential for 'win-win' forest management strategies, where overall multifunctionality is maximised. However, across sites, multifunctionality was on average 45.8-49.8% below maximum levels and not necessarily highest in protected areas. Therefore, using one of the most comprehensive assessments so far, our study suggests a high but largely unrealised potential for management to promote multifunctional forests.

Biodiversity and ecosystem functioning relations in European forests depend on environmental context.

The importance of biodiversity in supporting ecosystem functioning is generally well accepted. However, most evidence comes from small-scale studies, and scaling-up patterns of biodiversity-ecosystem functioning (B-EF) remains challenging, in part because the importance of environmental factors in shaping B-EF relations is poorly understood. Using a forest research platform in which 26 ecosystem functions were measured along gradients of tree species richness in six regions across Europe, we investigated the extent and the potential drivers of context dependency of B-EF relations. Despite considerable variation in species richness effects across the continent, we found a tendency for stronger B-EF relations in drier climates as well as in areas with longer growing seasons and more functionally diverse tree species. The importance of water availability in driving context dependency suggests that as water limitation increases under climate change, biodiversity may become even more important to support high levels of functioning in European forests.

Tree species diversity affects decomposition through modified micro-environmental conditions across European forests.

Different tree species influence litter decomposition directly through species-specific litter traits, and indirectly through distinct modifications of the local decomposition environment. Whether these indirect effects on decomposition are influenced by tree species diversity is presently not clear. We addressed this question by studying the decomposition of two common substrates, cellulose paper and wood sticks, in a total of 209 forest stands of varying tree species diversity across six major forest types at the scale of Europe. Tree species richness showed a weak but positive correlation with the decomposition of cellulose but not with that of wood. Surprisingly, macroclimate had only a minor effect on cellulose decomposition and no effect on wood decomposition despite the wide range in climatic conditions among sites from Mediterranean to boreal forests. Instead, forest canopy density and stand-specific litter traits affected the decomposition of both substrates, with a particularly clear negative effect of the proportion of evergreen tree litter. Our study suggests that species richness and composition of tree canopies modify decomposition indirectly through changes in microenvironmental conditions. These canopy-induced differences in the local decomposition environment control decomposition to a greater extent than continental-scale differences in macroclimatic conditions.

Soil warming opens the nitrogen cycle at the alpine treeline.

Climate warming may alter ecosystem nitrogen (N) cycling by accelerating N transformations in the soil, and changes may be especially pronounced in cold regions characterized by N-poor ecosystems. We investigated N dynamics across the plant-soil continuum during 6 years of experimental soil warming (2007-2012; +4 °C) at a Swiss high-elevation treeline site (Stillberg, Davos; 2180 m a.s.l.) featuring Larix decidua and Pinus uncinata. In the soil, we observed considerable increases in the NH4+ pool size in the first years of warming (by >50%), but this effect declined over time. In contrast, dissolved organic nitrogen (DON) concentrations in soil solutions from the organic layer increased under warming, especially in later years (maximum of +45% in 2012), suggesting enhanced DON leaching from the main rooting zone. Throughout the experimental period, foliar N concentrations showed species-specific but small warming effects, whereas δ15 N values showed a sustained increase in warmed plots that was consistent for all species analysed. The estimated total plant N pool size at the end of the study was greater (+17%) in warmed plots with Pinus but not in those containing Larix, with responses driven by trees. Irrespective of plot tree species identity, warming led to an enhanced N pool size of Vaccinium dwarf shrubs, no change in that of Empetrum hermaphroditum (dwarf shrub) and forbs, and a reduction in that of grasses, nonvascular plants, and fine roots. In combination, higher foliar δ15 N values and the transient response in soil inorganic N indicate a persistent increase in plant-available N and greater cumulative plant N uptake in warmer soils. Overall, greater N availability and increased DON concentrations suggest an opening of the N cycle with global warming, which might contribute to growth stimulation of some plant species while simultaneously leading to greater N losses from treeline ecosystems and possibly other cold biomes.

Priorities for research in soil ecology.

The ecological interactions that occur in and with soil are of consequence in many ecosystems on the planet. These interactions provide numerous essential ecosystem services, and the sustainable management of soils has attracted increasing scientific and public attention. Although soil ecology emerged as an independent field of research many decades ago, and we have gained important insights into the functioning of soils, there still are fundamental aspects that need to be better understood to ensure that the ecosystem services that soils provide are not lost and that soils can be used in a sustainable way. In this perspectives paper, we highlight some of the major knowledge gaps that should be prioritized in soil ecological research. These research priorities were compiled based on an online survey of 32 editors of Pedobiologia - Journal of Soil Ecology. These editors work at universities and research centers in Europe, North America, Asia, and Australia.The questions were categorized into four themes: (1) soil biodiversity and biogeography, (2) interactions and the functioning of ecosystems, (3) global change and soil management, and (4) new directions. The respondents identified priorities that may be achievable in the near future, as well as several that are currently achievable but remain open. While some of the identified barriers to progress were technological in nature, many respondents cited a need for substantial leadership and goodwill among members of the soil ecology research community, including the need for multi-institutional partnerships, and had substantial concerns regarding the loss of taxonomic expertise.

Temporal dynamics of biotic and abiotic drivers of litter decomposition.

Climate, litter quality and decomposers drive litter decomposition. However, little is known about whether their relative contribution changes at different decomposition stages. To fill this gap, we evaluated the relative importance of leaf litter polyphenols, decomposer communities and soil moisture for litter C and N loss at different stages throughout the decomposition process. Although both microbial and nematode communities regulated litter C and N loss in the early decomposition stages, soil moisture and legacy effects of initial differences in litter quality played a major role in the late stages of the process. Our results provide strong evidence for substantial shifts in how biotic and abiotic factors control litter C and N dynamics during decomposition. Taking into account such temporal dynamics will increase the predictive power of decomposition models that are currently limited by a single-pool approach applying control variables uniformly to the entire decay process.

Plant herbivory responses through changes in leaf quality have no effect on subsequent leaf-litter decomposition in a neotropical rain forest tree community.

It is commonly accepted that plant responses to foliar herbivory (e.g. plant defenses) can influence subsequent leaf-litter decomposability in soil. While several studies have assessed the herbivory-decomposability relationship among different plant species, experimental tests at the intra-specific level are rare, although critical for a mechanistic understanding of how herbivores affect decomposition and its consequences at the ecosystem scale. Using 17 tree species from the Yasuní National Park, Ecuadorian Amazonia, and applying three different herbivore damage treatments, we experimentally tested whether the plant intra-specific responses to herbivory, through changes in leaf quality, affect subsequent leaf-litter decomposition in soil. We found no effects of herbivore damage on the subsequent decomposition of leaf litter within any of the species tested. Our results suggest that leaf traits affecting herbivory are different from those influencing decomposition. Herbivore damage showed much higher intra-specific than inter-specific variability, while we observed the opposite for decomposition. Our findings support the idea that interactions between consumers and their resources are controlled by different factors for the green and the brown food-webs in tropical forests, where herbivory may not necessarily generate any direct positive or negative feedbacks for nutrient cycling.

Soil warming and CO2 enrichment induce biomass shifts in alpine tree line vegetation.

Responses of alpine tree line ecosystems to increasing atmospheric CO2 concentrations and global warming are poorly understood. We used an experiment at the Swiss tree line to investigate changes in vegetation biomass after 9 years of free air CO2 enrichment (+200 ppm; 2001-2009) and 6 years of soil warming (+4 °C; 2007-2012). The study contained two key tree line species, Larix decidua and Pinus uncinata, both approximately 40 years old, growing in heath vegetation dominated by dwarf shrubs. In 2012, we harvested and measured biomass of all trees (including root systems), above-ground understorey vegetation and fine roots. Overall, soil warming had clearer effects on plant biomass than CO2 enrichment, and there were no interactive effects between treatments. Total plant biomass increased in warmed plots containing Pinus but not in those with Larix. This response was driven by changes in tree mass (+50%), which contributed an average of 84% (5.7 kg m(-2) ) of total plant mass. Pinus coarse root mass was especially enhanced by warming (+100%), yielding an increased root mass fraction. Elevated CO2 led to an increased relative growth rate of Larix stem basal area but no change in the final biomass of either tree species. Total understorey above-ground mass was not altered by soil warming or elevated CO2 . However, Vaccinium myrtillus mass increased with both treatments, graminoid mass declined with warming, and forb and nonvascular plant (moss and lichen) mass decreased with both treatments. Fine roots showed a substantial reduction under soil warming (-40% for all roots <2 mm in diameter at 0-20 cm soil depth) but no change with CO2 enrichment. Our findings suggest that enhanced overall productivity and shifts in biomass allocation will occur at the tree line, particularly with global warming. However, individual species and functional groups will respond differently to these environmental changes, with consequences for ecosystem structure and functioning.

C, N and P fertilization in an Amazonian rainforest supports stoichiometric dissimilarity as a driver of litter diversity effects on decomposition.

Plant leaf litter generally decomposes faster as a group of different species than when individual species decompose alone, but underlying mechanisms of these diversity effects remain poorly understood. Because resource C : N : P stoichiometry (i.e. the ratios of these key elements) exhibits strong control on consumers, we supposed that stoichiometric dissimilarity of litter mixtures (i.e. the divergence in C : N : P ratios among species) improves resource complementarity to decomposers leading to faster mixture decomposition. We tested this hypothesis with: (i) a wide range of leaf litter mixtures of neotropical tree species varying in C : N : P dissimilarity, and (ii) a nutrient addition experiment (C, N and P) to create stoichiometric similarity. Litter mixtures decomposed in the field using two different types of litterbags allowing or preventing access to soil fauna. Litter mixture mass loss was higher than expected from species decomposing singly, especially in presence of soil fauna. With fauna, synergistic litter mixture effects increased with increasing stoichiometric dissimilarity of litter mixtures and this positive relationship disappeared with fertilizer addition. Our results indicate that litter stoichiometric dissimilarity drives mixture effects via the nutritional requirements of soil fauna. Incorporating ecological stoichiometry in biodiversity research allows refinement of the underlying mechanisms of how changing biodiversity affects ecosystem functioning.