A meta‐analysis of the effects of nutrient enrichment on litter decomposition in streams

The trophic state of many streams is likely to deteriorate in the future due to the continuing increase in human‐induced nutrient availability. Therefore, it is of fundamental importance to understand how nutrient enrichment affects plant litter decomposition, a key ecosystem‐level process in forest streams. Here, we present a meta‐analysis of 99 studies published between 1970 and 2012 that reported the effects of nutrient enrichment on litter decomposition in running waters. When considering the entire database, which consisted of 840 case studies, nutrient enrichment stimulated litter decomposition rate by approximately 50%. The stimulation was higher when the background nutrient concentrations were low and the magnitude of the nutrient enrichment was high, suggesting that oligotrophic streams are most vulnerable to nutrient enrichment. The magnitude of the nutrient‐enrichment effect on litter decomposition was higher in the laboratory than in the field experiments, suggesting that laboratory experiments overestimate the effect and their results should be interpreted with caution. Among field experiments, effects of nutrient enrichment were smaller in the correlative than in the manipulative experiments since in the former the effects of nutrient enrichment on litter decomposition were likely confounded by other environmental factors, e.g. pollutants other than nutrients commonly found in streams impacted by human activity. However, primary studies addressing the effect of multiple stressors on litter decomposition are still few and thus it was not possible to consider the interaction between factors in this review. In field manipulative experiments, the effect of nutrient enrichment on litter decomposition depended on the scale at which the nutrients were added: stream reach > streamside channel > litter bag. This may have resulted from a more uniform and continuous exposure of microbes and detritivores to nutrient enrichment at the stream‐reach scale. By contrast, nutrient enrichment at the litter‐bag scale, often by using diffusing substrates, does not provide uniform controllable nutrient release at either temporal or spatial scales, suggesting that this approach should be abandoned. In field manipulative experiments, the addition of both nitrogen (N) and phosphorus (P) resulted in stronger stimulation of litter decomposition than the addition of N or P alone, suggesting that there might be nutrient co‐limitation of decomposition in streams. The magnitude of the nutrient‐enrichment effect on litter decomposition was higher for wood than for leaves, and for low‐quality than for high‐quality leaves. The effect of nutrient enrichment on litter decomposition may also depend on climate. The tendency for larger effect size in colder regions suggests that patterns of biogeography of invertebrate decomposers may be modulating the effect of nutrient enrichment on litter decomposition. Although studies in temperate environments were overrepresented in our database, our meta‐analysis suggests that the effect of nutrient enrichment might be strongest in cold oligotrophic streams that depend on low‐quality plant litter inputs.     

Tree litter functional diversity and nitrogen concentration enhance litter decomposition via changes in earthworm communities

Biodiversity is a major driver of numerous ecosystem functions. However, consequences of changes in forest biodiversity remain difficult to predict because of limited knowledge about how tree diversity influences ecosystem functions. Litter decomposition is a key process affecting nutrient cycling, productivity, and carbon storage and can be influenced by plant biodiversity. Leaf litter species composition, environmental conditions, and the detritivore community are main components of the decomposition process, but their complex interactions are poorly understood. In this study, we tested the effect of tree functional diversity (FD) on litter decomposition in a field experiment manipulating tree diversity and partitioned the effects of litter physiochemical diversity and the detritivore community. We used litterbags with different mesh sizes to separate the effects of microorganisms and microfauna, mesofauna, and macrofauna and monitored soil fauna using pitfall traps and earthworm extractions. We hypothesized that higher tree litter FD accelerates litter decomposition due to the availability of complementary food components and higher activity of detritivores. Although we did not find direct effects of tree FD on litter decomposition, we identified key litter traits and macrodetritivores that explained part of the process. Litter mass loss was found to decrease with an increase in leaf litter carbon:nitrogen ratio. Moreover, litter mass loss increased with an increasing density of epigeic earthworms, with most pronounced effects in litterbags with a smaller mesh size, indicating indirect effects. Higher litter FD and litter nutrient content were found to increase the density of surface‐dwelling macrofauna and epigeic earthworm biomass. Based on structural equation modeling, we conclude that tree FD has a weak positive effect on soil surface litter decomposition by increasing the density of epigeic earthworms and that litter nitrogen‐related traits play a central role in tree composition effects on soil fauna and decomposition.     

Functional stability of stream-dwelling microbial decomposers exposed to copper and zinc stress

1. We investigated the resistance of aquatic microbial decomposers to Cu and Zn stress and their ability to recover after release from metal exposure, by examining leaf mass loss, fungal reproduction and microbial biomass and diversity.
2. Alder leaves, colonised in a reference stream, were exposed in microcosms to copper (Cu) or zinc (Zn), alone or in mixtures, with metals added together or sequentially (at day 0 or after 10 days). After 20 days, half of the microcosms were released from metals.
3. Leaf mass loss and fungal reproduction were reduced in most metal treatments, and the structure of fungal and bacterial communities was altered as indicated by identification of conidia and DNA fingerprinting based on denaturing gradient gel electrophoresis. Metals reduced the biomass of bacteria, but not that of fungi.
4. After release from metal stress, the structure of fungal communities became similar to that of control, and a recovery of microbial activity seemed to occur as shown by the lack of differences in leaf mass loss, bacterial biomass and fungal reproduction between control and metal treatments.     

Land‐use change shifts and magnifies seasonal variations of the decomposer system in lowland tropical landscapes

Deforestation and agricultural expansion in the tropics affect local and regional climatic conditions, leading to synergistic negative impacts on land ecosystems. Climatic changes manifest in increased inter‐ and intraseasonal variations and frequency of extreme climatic events (i.e., droughts and floods), which have evident consequences for aboveground biodiversity. However, until today, there have been no studies on how land use affects seasonal variations below ground in tropical ecosystems, which may be more buffered against climatic variation. Here, we analyzed seasonal variations in soil parameters, basal respiration, microbial communities, and abundances of soil invertebrates along with microclimatic conditions in rainforest and monocultures of oil palm and rubber in Sumatra, Indonesia. About 75% (20 out of 26) of the measured litter and soil, microbial, and animal parameters varied with season, with seasonal changes in 50% of the parameters depending on land use. Land use affected seasonal variations in microbial indicators associated with carbon availability and cycling rate. The magnitude of seasonal variations in microbial parameters in the soil of monocultures was almost 40% higher than in the soil of rainforest. Measured parameters were associated with short‐term climatic conditions (3‐day period air humidity) in plantations, but not in rainforest, confirming a reduced soil buffering ability in plantations. Overall, our findings suggest that land use temporally shifts and increases the magnitude of seasonal variations of the belowground ecosystem compartment, with microbial communities responding most strongly. The increased seasonal variations in soil biota in plantations likely translate into more pronounced fluctuations in essential ecosystem functions such as nutrient cycling and carbon sequestration, and these ramifications ultimately may compromise the stability of tropical ecosystems in the long term. As the observed seasonal dynamics is likely to increase with both local and global climate change, these shifts need closer attention for the long‐term sustainable management of plantation systems in the tropics.     

Responses of belowground communities to large aboveground herbivores: Meta‐analysis reveals biome‐dependent patterns and critical research gaps

The importance of herbivore–plant and soil biota–plant interactions in terrestrial ecosystems is amply recognized, but the effects of aboveground herbivores on soil biota remain challenging to predict. To find global patterns in belowground responses to vertebrate herbivores, we performed a meta‐analysis of studies that had measured abundance or activity of soil organisms inside and outside field exclosures (areas that excluded herbivores). Responses were often controlled by climate, ecosystem type, and dominant herbivore identity. Soil microfauna and especially root‐feeding nematodes were negatively affected by herbivores in subarctic sites. In arid ecosystems, herbivore presence tended to reduce microbial biomass and nitrogen mineralization. Herbivores decreased soil respiration in subarctic ecosystems and increased it in temperate ecosystems, but had no net effect on microbial biomass or nitrogen mineralization in those ecosystems. Responses of soil fauna, microbial biomass, and nitrogen mineralization shifted from neutral to negative with increasing herbivore body size. Responses of animal decomposers tended to switch from negative to positive with increasing precipitation, but also differed among taxa, for instance Oribatida responded negatively to herbivores, whereas Collembola did not. Our findings imply that losses and gains of aboveground herbivores will interact with climate and land use changes, inducing functional shifts in soil communities. To conceptualize the mechanisms behind our findings and link them with previous theoretical frameworks, we propose two complementary approaches to predict soil biological responses to vertebrate herbivores, one focused on an herbivore body size gradient, and the other on a climate severity gradient. Major research gaps were revealed, with tropical biomes, protists, and soil macrofauna being especially overlooked.     

An experimental test of the hypothesis of non‐homeostatic consumer stoichiometry in a plant litter–microbe system

Stoichiometric homeostasis of heterotrophs is a common, but not always well‐examined premise in ecological stoichiometry. We experimentally evaluated the relationship between substrate (plant litter) and consumer (microorganisms) stoichiometry for a tropical terrestrial decomposer system. Variation in microbial C : P and N : P ratios tracked that of the soluble litter fraction, but not that of bulk leaf litter material. Microbial N and P were not isometrically related, suggesting higher rates of P than N sequestration in microbial biomass. Shifts in microbial stoichiometry were related to changes in microbial community structure. Our results indicate that P in dissolved form is a major driver of terrestrial microbial stoichiometry, similar to aquatic environments. The demonstrated relative plasticity in microbial C : P and N : P and the critical role of P have important implications for theoretical modelling and contribute to a process‐based understanding of stoichiometric relationships and the flow of elements across trophic levels in decomposer systems.     

Divergence of feeding channels within the soil food web determined by ecosystem type

Understanding trophic linkages within the soil food web (SFW) is hampered by its opacity, diversity, and limited niche adaptation. We need to expand our insight between the feeding guilds of fauna and not just count biodiversity. The soil fauna drive nutrient cycling and play a pivotal, but little understood role within both the carbon (C) and nitrogen (N) cycles that may be ecosystem dependent. Here, we define the structure of the SFW in two habitats (grassland and woodland) on the same soil type and test the hypothesis that land management would alter the SFW in these habitats. To do this, we census the community structure and use stable isotope analysis to establish the pathway of C and N through each trophic level within the ecosystems. Stable isotope ratios of C and N from all invertebrates were used as a proxy for trophic niche, and community‐wide metrics were obtained. Our empirically derived C/N ratios differed from those previously reported, diverging from model predictions of global C and N cycling, which was unexpected. An assessment of the relative response of the different functional groups to the change from agricultural grassland to woodland was performed. This showed that abundance of herbivores, microbivores, and micropredators were stimulated, while omnivores and macropredators were inhibited in the grassland. Differences between stable isotope ratios and community‐wide metrics, highlighted habitats with similar taxa had different SFWs, using different basal resources, either driven by root or litter derived resources. Overall, we conclude that plant type can act as a top‐down driver of community functioning and that differing land management can impact on the whole SFW.     

Salinisation effects on leaf litter decomposition in fresh waters: Does the ionic composition of salt matter?

1. Salinisation (i.e. increased ion concentrations) in fresh waters is a growing threat worldwide that impacts freshwater communities. However, less is known about how increased salt concentrations affect key ecosystem processes such as leaf decomposition.
2. We designed a laboratory experiment to assess the effects of a concentration gradient (1, 3, and 6 g/L) of three different salts (NaCl, CaCl₂ and CH₃CO₂K), on leaf litter decomposition mediated by microbial decomposers and the larvae of a cased caddis fly (Schizopelex festiva, Trichoptera). Leaf discs of Quercus robur inoculated with microbial decomposers (a mixture of 5 fungal species) were incubated in microcosms under every possible salt × concentration combination and without salt addition (control), with a single individual of the cased caddis fly. Half of the leaf disks were not available for consumption by the trichopteran and represent a microbial only treatment when leaf mass loss was measured.
3. Leaf decomposition driven by microbial decomposers was not affected by salinity despite the fact that all salt treatments depressed fungal biomass and microbial respiration compared to the control. However, the caddis flies were strongly affected by the high salt concentrations and consumed less leaf material at 6 g/L salt concentrations compared to control microcosms. The feeding activity of the trichopteran further depended on the salt type: CaCl₂ had the most deleterious effects.
4. Salinisation of fresh waters depresses leaf litter decomposition, mainly through deleterious effects on detritivores, the magnitude of the response being dependent on the ionic composition. Our results reiterate the need to reduce terrestrial run-off of salts into fresh waters because salinisation (especially increased levels of CaCl₂) affects invertebrates and the key ecosystem processes they drive.

     

Variable temperature effects between heterotrophic stream processes and organisms

1. Temperature is known to stimulate metabolism with cascading effects on multiple biological processes. These effects may, however, vary across processes, types of organisms or levels of biological organisation. They can also vary with nutrient availability, with potentially stronger temperature effects when nutrients are not limiting. This context dependence of temperature effects on processes challenges our ability to anticipate their consequences on ecosystems in a changing world.
2. In headwater streams, the decomposition of allochthonous leaf litter, driven by both microbial decomposers and invertebrates, is known to respond to both temperature and nutrient availability. These food webs are highly tractable and a useful model system to investigate the variations of temperature effects on processes across types of organisms (microbes versus invertebrates), resource availability levels (nutrient concentration), and levels of biological organisation (from individual to ecosystem).
3. In a microcosm experiment, we measured the effects of temperature and nitrogen availability (four levels each) on respiration rates of litter-consuming microbes and invertebrates and their decomposition activity in different contexts of food web complexity. The latter included one treatment without invertebrate detritivore (microbial decomposers only), three single invertebrate taxa (Gammarus, Potamophylax, and Sericostoma) treatments, and one mixed invertebrate taxa treatment (three-species altogether).
4. Microbial processes increased nearly exponentially with temperature (Arrhenius model, activation energy (± 95% confidence interval) = 0.56 ± 0.53 and 1.00 ± 0.23 eV for litter decomposition and respiration), while invertebrate-driven processes increased (activation energy from 0.47–1.15 eV) up to a maximal value at an intermediate temperature (c. 11–15°C depending on species and process), above which process rates decreased. By contrast, litter consumption in mixed invertebrate species treatments was not significantly influenced by temperature, because of a negative effect of species mixing occurring above 12°C. Nitrogen had a weaker influence, only slightly stimulating litter consumption by mixed-species invertebrates, which limited the scope for synergies with temperature effects.
5. Our results raise issues about how aquatic litter consumers meet their energy requirements at high temperature and suggest that a general consequence of warming could be loss of carbon through mineralisation in headwater stream food webs. In several aspects, our results deviate from expectations based on universal relationships between temperature and individual metabolism (e.g. metabolic theory of ecology), suggesting that we may need to develop less simplistic assumptions to predict the consequence of warming on ecosystem processes.