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.

Energetic mismatch induced by warming decreases leaf litter decomposition by aquatic detritivores.

The balance of energetic losses and gains is of paramount importance for understanding and predicting the persistence of populations and ecosystem processes in a rapidly changing world. Previous studies suggested that metabolic rate often increases faster with warming than resource ingestion rate, leading to an energetic mismatch at high temperature. However, little is known about the ecological consequences of this energetic mismatch for population demography and ecosystem functions. Here, we combined laboratory experiments and modelling to investigate the energetic balance of a stream detritivore Gammarus fossarum along a temperature gradient and the consequences for detritivore populations and organic matter decomposition. We experimentally measured the energetic losses (metabolic rate) and supplies (ingestion rate) of Gammarus and we modelled the impact of rising temperatures and changes in Gammarus body size induced by warming on population dynamics and benthic organic matter dynamics in freshwater systems. Our experimental results indicated an energetic mismatch in a Gammarus population where losses via metabolic rate increase faster than supplies via food ingestion with warming, which translated in a decrease in energetic efficiency with temperature rising from 5 to 20°C. Moreover, our consumer-resource model predicts a decrease in the biomass of Gammarus population with warming, associated with lower maximum abundances and steeper abundance decreases after biomass annual peaks. These changes resulted in a decrease in leaf litter decomposition rate and thus longer persistence of leaf litter standing stock over years in the simulations. In addition, Gammarus body size reductions led to shorter persistence for both leaf litter and Gammarus biomasses at low temperature and the opposite trend at high temperature, revealing that body size reduction was weakening the effect of temperature on resource and consumer persistence. Our model contributes to identifying the mechanisms that explain how thermal effects at the level of individuals may cascade through trophic interactions and influence important ecosystem processes. Considering the balance of physiological processes is crucial to improve our ability to predict the impact of climate change on carbon stocks and ecosystem functions.

Litter Quality Modulates Effects of Dissolved Nitrogen on Leaf Decomposition by Stream Microbial Communities.

Rates of leaf litter decomposition in streams are strongly influenced both by inorganic nutrients dissolved in stream water and by litter traits such as lignin, nitrogen (N) and phosphorus (P) concentrations. As a result, decomposition rates of different leaf species can show contrasting responses to stream nutrient enrichment resulting from human activities. It is unclear, however, whether the root cause of such discrepancies in field observations is the interspecific variation in either litter nutrient or litter lignin concentrations. To address this question, we conducted a controlled laboratory experiment with a known fungal community to determine decomposition rates of 38 leaf species exhibiting contrasting litter traits (N, P and lignin concentrations), which were exposed to 8 levels of dissolved N concentrations representative of field conditions across European streams (0.07 to 8.96 mg N L-1). The effect of N enrichment on decomposition rate was modelled using Monod kinetics to quantify N effects across litter species. Lignin concentration was the most important litter trait determining decomposition rates and their response to N enrichment. In particular, increasing dissolved N supply from 0.1 to 3.0 mg N L-1 accelerated the decomposition of lignin-poor litter (e.g. < 10% of lignin, 2.9× increase ± 1.4 SD, n = 14) more strongly than that of litter rich in lignin (e.g. > 15% of lignin, 1.4× increase ± 0.2 SD, n = 9). Litter nutrient concentrations were less important, with a slight positive effect of P on decomposition rates and no effect of litter N. These results indicate that shifts in riparian vegetation towards species characterized by high litter lignin concentrations could alleviate the stimulation of C turnover by stream nutrient enrichment.

The functional syndrome: linking individual trait variability to ecosystem functioning.

Phenotypic variability is increasingly assessed through functional response and effect traits, which provide a mechanistic framework for investigating how an organism responds to varying ecological factors and how these responses affect ecosystem functioning. Covariation between response and effect traits has been poorly examined at the intraspecific level, thus hampering progress in understanding how phenotypic variability alters the role of organisms in ecosystems. Using a multi-trait approach and a nine-month longitudinal monitoring of individual red-swamp crayfish (Procambarus clarkii), we demonstrated that most of the measured response and effect traits were partially stable during the ontogeny of individuals. Suites of response and effect traits were associated with a response syndrome and an effect syndrome, respectively, which were correlated to form a functional syndrome. Using a bioenergetic model, we predicted that differences in the response syndrome composition of hypothetical populations had important ecological effects on a key ecosystem process (i.e. whole-lake litter decomposition) to a level similar to those induced by doubling population size. Demonstrating the existence of a functional syndrome is likely to improve our understanding of the ecological impacts of phenotypic variation among individuals in wild populations across levels of biological organization, and the linkage between ecosystem and evolutionary ecology.

Global synthesis of the temperature sensitivity of leaf litter breakdown in streams and rivers.

Streams and rivers are important conduits of terrestrially derived carbon (C) to atmospheric and marine reservoirs. Leaf litter breakdown rates are expected to increase as water temperatures rise in response to climate change. The magnitude of increase in breakdown rates is uncertain, given differences in litter quality and microbial and detritivore community responses to temperature, factors that can influence the apparent temperature sensitivity of breakdown and the relative proportion of C lost to the atmosphere vs. stored or transported downstream. Here, we synthesized 1025 records of litter breakdown in streams and rivers to quantify its temperature sensitivity, as measured by the activation energy (Ea , in eV). Temperature sensitivity of litter breakdown varied among twelve plant genera for which Ea could be calculated. Higher values of Ea were correlated with lower-quality litter, but these correlations were influenced by a single, N-fixing genus (Alnus). Ea values converged when genera were classified into three breakdown rate categories, potentially due to continual water availability in streams and rivers modulating the influence of leaf chemistry on breakdown. Across all data representing 85 plant genera, the Ea was 0.34 ± 0.04 eV, or approximately half the value (0.65 eV) predicted by metabolic theory. Our results indicate that average breakdown rates may increase by 5-21% with a 1-4 °C rise in water temperature, rather than a 10-45% increase expected, according to metabolic theory. Differential warming of tropical and temperate biomes could result in a similar proportional increase in breakdown rates, despite variation in Ea values for these regions (0.75 ± 0.13 eV and 0.27 ± 0.05 eV, respectively). The relative proportions of gaseous C loss and organic matter transport downstream should not change with rising temperature given that Ea values for breakdown mediated by microbes alone and microbes plus detritivores were similar at the global scale.

Phenological response of a key ecosystem function to biological invasion.

Although climate warming has been widely demonstrated to induce shifts in the timing of many biological events, the phenological consequences of other prominent global change drivers remain largely unknown. Here, we investigated the effects of biological invasions on the seasonality of leaf litter decomposition, a crucial freshwater ecosystem function. Decomposition rates were quantified in 18 temperate shallow lakes distributed along a gradient of crayfish invasion and a temperature-based model was constructed to predict yearly patterns of decomposition. We found that, through direct detritus consumption, omnivorous invasive crayfish accelerated decomposition rates up to fivefold in spring, enhancing temperature dependence of the process and shortening the period of major detritus availability in the ecosystem by up to 39 days (95% CI: 15-61). The fact that our estimates are an order of magnitude higher than any previously reported climate-driven phenological shifts indicates that some powerful drivers of phenological change have been largely overlooked.

Litter chemistry prevails over litter consumers in mediating effects of past steel industry activities on leaf litter decomposition.

Soil pollution has adverse effects on the performance and life history traits of microorganisms, plants, and animals, yet evidence indicates that even the most polluted sites can support structurally-complex and dynamic ecosystems. The present study aims at determining whether and how litter decomposition, one of the most important soil ecological processes leaf, is affected in a highly trace-metal polluted site. We postulated that past steel mill activities resulting in soil pollution and associated changes in soil characteristics would influence the rate of litter decomposition through two non-exclusive pathways: altered litter chemistry and responses of decomposers to lethal and sub-lethal toxic stress. We carried out a litter-bag experiment using Populus tremula L. leaf litter collected at, and allowed to decompose in, a trace metal polluted site and in three unpolluted sites used as controls. We designed a fully-factorial transplant experimental design to assess effects of litter origin and exposure site on the rate of litter decomposition. We further determined initial litter chemistry, fungal biomass, mesofauna abundance in litter bags, and the soil macrofauna community. Irrespective of the site of litter exposure, litter originating from the polluted site had a two-fold faster decomposition than litter from the unpolluted sites. Litter chemistry, notably the lignin content, seemed most important in explaining the degradation rate of the leaf litter. Abundance of meso and macro-detritivores was higher at the polluted site than at the unpolluted sites. However, litter decomposition proceeded at similar rates in polluted and unpolluted sites. Our results show that trace metal pollution and associated soil and litter changes do not necessarily weaken consumer control on litter decomposition through lethal and sub-lethal toxic stress.

Ecological opportunities and intraspecific competition alter trophic niche specialization in an opportunistic stream predator.

Many generalist populations are composed of specialized individuals that use a narrow part of the population's niche. Ecological theories predict that individual specialization and population trophic niche are determined by biotic interactions and resource diversity emerging from environmental variations (i.e. ecological opportunities). However, due to the paucity of empirical and experimental demonstrations, the genuine importance of each of these drivers in determining trophic niche attributes is not fully appreciated. The present study aimed at determining the population level and individual responses of brown trout (Salmo trutta) to variations in ecological opportunities (terrestrial prey inputs) and autochthonous prey communities among 10 stream reaches along a riparian condition gradient using individual longitudinal monitoring and stable isotope analyses. Our results suggested that trophic niche diversity varied along the environmental gradient, while individual trophic specialization was indirectly driven by ecological opportunities through strengthened intraspecific competition. Individual diet was repeatable over the study period, and the growth rate of juvenile brown trout increased with their specialization for aquatic predatory invertebrates. Our findings highlight the dual influences of intraspecific competition and ecological opportunities on individual trophic specialization and population trophic niche.

Predator effects on a detritus-based food web are primarily mediated by non-trophic interactions.

Predator effects on ecosystems can extend far beyond their prey and are often not solely lethally transmitted. Change in prey traits in response to predation risk can have important repercussions on community assembly and key ecosystem processes (i.e. trait-mediated indirect effects). In addition, some predators themselves alter habitat structure or nutrient cycling through ecological engineering effects. Tracking these non-trophic pathways is thus an important, yet challenging task to gain a better grasp of the functional role of predators. Multiple lines of evidence suggest that, in detritus-based food webs, non-trophic interactions may prevail over purely trophic interactions in determining predator effects on plant litter decomposition. This hypothesis was tested in a headwater stream by modulating the density of a flatworm predator (Polycelis felina) in enclosures containing oak (Quercus robur) leaf litter exposed to natural colonization by small invertebrates and microbial decomposers. Causal path modelling was used to infer how predator effects propagated through the food web. Flatworms accelerated litter decomposition through positive effects on microbial decomposers. The biomass of prey and non-prey invertebrates was not negatively affected by flatworms, suggesting that net predator effect on litter decomposition was primarily determined by non-trophic interactions. Flatworms enhanced the deposition and retention of fine sediments on leaf surface, thereby improving leaf colonization by invertebrates - most of which having strong affinities with interstitial habitats. This predator-induced improvement of habitat availability was attributed to the sticky nature of the mucus that flatworms secrete in copious amount while foraging. Results of path analyses further indicated that this bottom-up ecological engineering effect was as powerful as the top-down effect on invertebrate prey. Our findings suggest that predators have the potential to affect substantially carbon flow and nutrient cycling in detritus-based ecosystems and that this impact cannot be fully appreciated without considering non-trophic effects.

Benthic algae stimulate leaf litter decomposition in detritus-based headwater streams: a case of aquatic priming effect?

In detritus-based ecosystems, autochthonous primary production contributes very little to the detritus pool. Yet primary producers may still influence the functioning of these ecosystems through complex interactions with decomposers and detritivores. Recent studies have suggested that, in aquatic systems, small amounts of labile carbon (C) (e.g., producer exudates), could increase the mineralization of more recalcitrant organic-matter pools (e.g., leaf litter). This process, called priming effect, should be exacerbated under low-nutrient conditions and may alter the nature of interactions among microbial groups, from competition under low-nutrient conditions to indirect mutualism under high-nutrient conditions. Theoretical models further predict that primary producers may be competitively excluded when allochthonous C sources enter an ecosystem. In this study, the effects of a benthic diatom on aquatic hyphomycetes, bacteria, and leaf litter decomposition were investigated under two nutrient levels in a factorial microcosm experiment simulating detritus-based, headwater stream ecosystems. Contrary to theoretical expectations, diatoms and decomposers were able to coexist under both nutrient conditions. Under low-nutrient conditions, diatoms increased leaf litter decomposition rate by 20% compared to treatments where they were absent. No effect was observed under high-nutrient conditions. The increase in leaf litter mineralization rate induced a positive feedback on diatom densities. We attribute these results to the priming effect of labile C exudates from primary producers. The presence of diatoms in combination with fungal decomposers also promoted decomposer diversity and, under low-nutrient conditions, led to a significant decrease in leaf litter C:P ratio that could improve secondary production. Results from our microcosm experiment suggest new mechanisms by which primary producers may influence organic matter dynamics even in ecosystems where autochthonous primary production is low.

Continental-scale effects of nutrient pollution on stream ecosystem functioning.

Excessive nutrient loading is a major threat to aquatic ecosystems worldwide that leads to profound changes in aquatic biodiversity and biogeochemical processes. Systematic quantitative assessment of functional ecosystem measures for river networks is, however, lacking, especially at continental scales. Here, we narrow this gap by means of a pan-European field experiment on a fundamental ecosystem process--leaf-litter breakdown--in 100 streams across a greater than 1000-fold nutrient gradient. Dramatically slowed breakdown at both extremes of the gradient indicated strong nutrient limitation in unaffected systems, potential for strong stimulation in moderately altered systems, and inhibition in highly polluted streams. This large-scale response pattern emphasizes the need to complement established structural approaches (such as water chemistry, hydrogeomorphology, and biological diversity metrics) with functional measures (such as litter-breakdown rate, whole-system metabolism, and nutrient spiraling) for assessing ecosystem health.

Incubation time, functional litter diversity, and habitat characteristics predict litter-mixing effects on decomposition.

Plant diversity influences many fundamental ecosystem functions, including carbon and nutrient dynamics, during litter breakdown. Mixing different litter species causes litter mixtures to lose mass at different rates than expected from component species incubated in isolation. Such nonadditive litter-mixing effects on breakdown processes often occur idiosyncratically because their direction and magnitude change with incubation time, litter species composition, and ecosystem characteristics. Taking advantage of results from 18 litter mixture experiments in streams, we examined whether the direction and magnitude of nonadditive mixing effects are randomly determined. Across 171 tested litter mixtures and 510 incubation time-by-mixture combinations, nonadditive effects on breakdown were common and on average resulted in slightly faster decomposition than expected. In addition, we found that the magnitude of nonadditive effects and the relative balance of positive and negative responses in mixtures change predictably over time, and both were related to an index of functional litter diversity and selected environmental characteristics. Based on these, it should be expected that nonadditive effects are stronger for litter mixtures made of functionally dissimilar species especially in smaller streams. Our findings demonstrate that effects of litter diversity on plant mixture breakdown are more predictable than generally thought. We further argue that the consequences of current worldwide homogenization in the composition of plant traits on carbon and nutrient dynamics could be better inferred from long-duration experiments that manipulate both functional litter diversity and ecosystem characteristics in "hotspots of biodiversity effects," such as small streams.

Decomposition of diverse litter mixtures in streams.

In view of growing interest in understanding how biodiversity affects ecosystem functioning, we investigated effects of riparian plant diversity on litter decomposition in forest streams. Leaf litter from 10 deciduous tree species was collected during natural leaf fall at two locations (Massif Central in France and Carpathians in Romania) and exposed in the field in litter bags. There were 35 species combinations, with species richness ranging 1-10. Nonadditive effects on the decomposition of mixed-species litter were minor, although a small synergistic effect was observed in the Massif Central stream where observed litter mass remaining was significantly lower overall than expected from data on single-species litter. In addition, variability in litter mass remaining decreased with litter diversity at both locations. Mean nitrogen concentration of single- and mixed-species litters (0.68-4.47% of litter ash-free dry mass) accounted for a large part of the variation in litter mass loss across species combinations. For a given species or mixture, litter mass loss was also consistently faster in the Massif Central than in the Carpathians, and the similarity in general stream characteristics, other than temperature, suggests that this effect was largely due to differences in thermal regimes. These results support the notion that decomposition of litter mixtures is primarily driven by litter quality and environmental factors, rather than by species richness per se. However, the observed consistent decrease in variability of decomposition rate with increasing plant species richness indicates that conservation of riparian tree diversity is important even when decomposition rates are not greatly influenced by litter mixing.

Riparian plant species loss alters trophic dynamics in detritus-based stream ecosystems.

Riparian vegetation is closely connected to stream food webs through input of leaf detritus as a primary energy supply, and therefore, any alteration of plant diversity may influence aquatic ecosystem functioning. We measured leaf litter breakdown rate and associated biological parameters in mesh bags in eight headwater streams bordered either with mixed deciduous forest or with beech forest. The variety of leaf litter types in mixed forest results in higher food quality for large-particle invertebrate detritivores ('shredders') than in beech forest, which is dominated by a single leaf species of low quality. Breakdown rate of low quality (oak) leaf litter in coarse mesh bags was lower in beech forest streams than in mixed forest streams, a consequence of lower shredder biomass. In contrast, high quality (alder) leaf litter broke down at similar rates in both stream categories as a result of similar shredder biomass in coarse mesh bags. Microbial breakdown rate of oak and alder leaves, determined in fine mesh bags, did not differ between the stream categories. We found however aquatic hyphomycete species richness on leaf litter to positively co-vary with riparian plant species richness. Fungal species richness may enhance leaf litter breakdown rate through positive effects on resource quality for shredders. A feeding experiment established a positive relationship between fungal species richness per se and leaf litter consumption rate by an amphipod shredder (Gammarus fossarum). Our results show therefore that plant species richness may indirectly govern ecosystem functioning through complex trophic interactions. Integrating microbial diversity and trophic dynamics would considerably improve the prediction of the consequences of species loss.