Manuel A. S. Graça

The role of invertebrates on leaf litter decomposition in streams : A review

Leaves entering low order streams are subject to physical abrasion, microbial degradation and invertebrate fragmentation. Aquatic invertebrates feeding on leaves are known as shredders and their densities tend to be correlated with the spatial and temporal accumulation of organic matter in streams. Shredders discriminate among the variety of leaves normally found in the stream; this discrimination may be related to differences in leaf toughness, plant nutrient content of leaves and the presence of secondary compounds. Shredders also consume leaves preferentially after the establishment of a well-developed microbial community. This preference may be the result of changes in leaf matrix carried out by the microbial community or the presence of fungal hyphae with a higher nutrition value than the leaves themselves. The immediate consequence of invertebrate feeding on leaves is the incorporation of plant material into secondary production and the fragmentation of leaves. The relative importance of fungi and invertebrates in the decomposition process depends upon the density of shredders, which, in turn, may depend on litter accumulation in streams. Therefore, the type of riparian vegetation has the potential to control the diversity and abundance of shredders and changes in riparian vegetation have the potential to affect the assemblages of aquatic invertebrates.

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

Reading the Leaves Excess inputs of nutrients—a type of pollution known as eutrophication—threatens biodiversity and water quality in rivers and streams. Woodward et al. (p. 1438; see the Perspective by Palmer and Febria) studied how one key ecosystem process—leaf-litter decomposition—responds to eutrophication across a large nutrient pollution gradient in 100 European streams. Leaf breakdown was stimulated by low to moderate nutrient concentrations but was inhibited at high rates of nutrient loading. Leaf-litter breakdown rates across 100 European streams offer insights into ecosystem health during eutrophication. 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.

A global experiment suggests climate warming will not accelerate litter decomposition in streams but might reduce carbon sequestration

The decomposition of plant litter is one of the most important ecosystem processes in the biosphere and is particularly sensitive to climate warming. Aquatic ecosystems are well suited to studying warming effects on decomposition because the otherwise confounding influence of moisture is constant. By using a latitudinal temperature gradient in an unprecedented global experiment in streams, we found that climate warming will likely hasten microbial litter decomposition and produce an equivalent decline in detritivore-mediated decomposition rates. As a result, overall decomposition rates should remain unchanged. Nevertheless, the process would be profoundly altered, because the shift in importance from detritivores to microbes in warm climates would likely increase CO(2) production and decrease the generation and sequestration of recalcitrant organic particles. In view of recent estimates showing that inland waters are a significant component of the global carbon cycle, this implies consequences for global biogeochemistry and a possible positive climate feedback.

Leaf Barriers to Fungal Colonization and Shredders (Tipula lateralis) Consumption of Decomposing Eucalyptus globulus.

A bstractHerein we assess the importance of leaf cuticle, polyphenolic, and essential oils contents of Eucalyptus globulus leaves to hyphomycete colonization and shredder consumption. Optical and electron microscopy revealed that, at least during the first 5 weeks of conditioning, the cuticle remains virtually intact. Stomata provide the main access for hyphae to internal leaf tissues and, eventually, for spore release. We suggest that in E. globulus leaves, fungal decomposition progresses predominantly in and from the eucalyptus leaf mesophyll to the outside. Malt extract agar media supplemented with either eucalyptus essential oils or tannic acid completely inhibited (Articulospora tetracladia, Lemonniera aquatica, and Tricladium gracile) or depressed (Heliscus lugdunensis, Lunulospora curvula, and Tricladium angulatum) aquatic hyphomycetes growth. The transference of both secondary compounds to alder leaves induced similar and significant reduction in Tipula lateralis larval consumption. Results consistently indicate that eucalyptus oils are stronger deterrents than polyphenols. The waxy cuticle of E. globulus appears to be a key physical factor delaying fungal colonization during decomposition. We hypothesize that the relative influence of leaf phenols and essential oils to aquatic hyphomycetes and shredders may be related to three main factors: (a) initial distribution of such compounds in the leaves; (b) possibility of their decrease through decomposition; and (c) consumption strategies of detritivores.

Importance of fungi in the diet of Gammarus pulex and Asellus aquaticus. II: Effects on growth, reproduction and physiology

An important component of the interaction between macroinvertebrates and leaf litter in streams in the extent to which consumers can differentiate between undecomposed and decomposing leaves. The detritivores Gammarus pulex and Asellus aquaticus fed preferentially on conditioned rather on unconditioned leaf material. Growth in A. aquaticus was significantly reduced when unconditioned leaves were provided, but in G. pulex no significant effect of conditioning on growth was observed. The capacity of G. pulex to tolerate reductions in food quality seems to be a consequence of a compensatory system in which respiration rates change to compensate for reductions in food quality. In this way a constant growth rate is maintained. Increases in ingestion rates to compensate for low quality food were not observed.

Decomposition of Eucalyptus globulus leaves and three native leaf species (Alnus glutinosa, Castanea sativa and Quercus faginea) in a Portuguese low order stream

Leaf decomposition of the exotic evergreen Eucalyptus globulus (eucalyptus), and three native deciduous tree species, Alnus glutinosa (alder), Castanea sativa (chestnut) and Quercus faginea (oak), was compared in a second order stream in Central Portugal. Changes in dry weight, nitrogen and polyphenolic compounds and microbial colonization were periodically assessed for three months.Negative exponential curves fit the leaf weight loss with time for all leaf species. Mass loss rate was in the order alder (K = 0.0161) > chestnut (K = 0.0079) > eucalyptus (K = 0.0068) > oak (K = 0.0037). Microbial colonization followed the same pattern as breakdown rates. Evidence of fungal colonization was observed in alder after 3 days in the stream, whereas it took 21 days in oak leaves to have fungal colonization. Fungal diversity was leaf species-dependent and increased with time. In all cases, percent nitrogen per unit leaf weight increased, at least, at the initial stages of decay while soluble polyphenolics (expressed as percentage per unit leaf weight) decreased rapidly in the first month of leaves immersion.Intrinsic factors such as nitrogen and polyphenolic content may explain differences in leaf decomposition. The possible incorporation of eucalyptus litter into secondary production in a reasonable time span is suggested, although community balance and structure might be affected by differences in allochthonous patterns determined by eucalyptus monocultures.

Effects of eucalyptus afforestation on leaf litter dynamics and macroinvertebrate community structure of streams in Central Portugal

To test the hypothesis whether afforestation with Eucalyptus globulus affects litter dynamics in streams and the structure of macroinvertebrate aquatic communities, we compared streams flowing through eucalyptus and deciduous forests, paying attention to: (i) litterfall dynamics, (ii) accumulation of organic matter, (iii) processing rates of two dominant leaf species: eucalyptus and chestnut, and (iv) macroinvertebrate community structure. The amount of allochthonous inputs was similar in both vegetation types, but the seasonality of litter inputs differed between eucalyptus and natural deciduous forests. Eucalyptus forest streams accumulated more organic matter than deciduous forest streams. Decomposition of both eucalyptus and chestnut leaf litter was higher in streams flowing through deciduous forests. The eucalyptus forest soils were highly hydrophobic resulting in strong seasonal fluctuations in discharge. In autumn the communities of benthic macroinvertebrates of the two stream types were significantly different. Deciduous forest streams contained higher numbers of invertebrates and more taxa than eucalyptus forest streams. Mixed forest streams (streams flowing through eucalyptus forests but bordered by deciduous vegetation) were intermediate between the two other vegetation types in all studied characteristics (accumulation of benthic organic matter, density and diversity of aquatic invertebrates). These results suggest that monocultures of eucalyptus affect low order stream communities. However, the impact may be attenuated if riparian corridors of original vegetation are kept in plantation forestry.

Importance of fungi in the diet of Gammarus pulex and Asellus aquaticus I: feeding strategies

The importance of fungi in the trophic biology of the freshwater detritivores Gammarus pulex and Asellus aquaticus was investigated. Inspection of leaves used in feeding trials indicated that whereas A. aquaticus scrapes at the leaf surface, G. pulex bites through the leaf material. Both species discriminated between fungal mycelia, fungally colonized and uncolonized leaf material but, although A. aquaticus selectively consumed fungal mycelia, G. pulex fed preferentially on leaf material. Fungi appear to be an important food source for A. aquaticus and selection of food material was positively correlated with fungal biomass. In contrast, for G. pulex, fungi appear to be more important as modifiers of leaf material. However, no significant correlations were found between food preference and any of the leaf modifications measured.

Litter processing along a stream gradient: the role of invertebrates and decomposers

Dissolved nutrients and temperature tend to increase in a downstream direction, whereas shredder density tends to decrease. As a result, the relative importance of microbes (bacteria and fungi) and invertebrates in leaf litter processing may gradually shift along a stream gradient. Therefore, we hypothesized that differences in litter decay between fine-mesh (invertebrates excluded) and coarse-mesh (accessible to invertebrates) bags will be high in low-order streams (i.e., <4) and low in high-order streams (i.e., >4). To test this hypothesis, we investigated the processing of alder (Alnus glutinosa) litter in 12 sites ranging from 2nd to 6th order in central Portugal during autumn/winter and spring/summer seasons. Mass loss rates (measured as % ash-free dry mass [AFDM]) were higher in spring/summer than in autumn/winter and higher in coarse- than in fine-mesh bags. No clear relationship was observed between river order and litter processing (% AFDM loss). In spring/summer, the difference in remaining mass between fine- and coarse-mesh bags was higher in low-order than in high-order streams and decreased in a downstream direction, supporting our hypothesis. Other evidence for shifting in processing vectors includes the observations that 1) the biomass and % of shredders were generally higher in low-order than in high-order streams and tended to decrease downstream, 2) high microbial biomass was reached earlier in high-order than in low-order rivers, and 3) the density of fungal conidia tended to increase with increasing stream order. No pattern of shifting in processing vectors was observed in autumn/winter, possibly because food was nonlimiting.

Leaf-litter breakdown in 3 streams in temperate, Mediterranean, and tropical Cerrado climates

Abstract The objectives of our study were to assess leaf-litter breakdown in 3 streams in 3 climates and to determine the contributions of associated microbial and invertebrate communities to the process. We incubated leaves of Alnus glutinosa in 1 stream in each of 3 climate zones: temperate (mountains of Central Portugal), Mediterranean (South Portugal), and tropical Cerrado (Minas Gerais, Brazil). Leaf-litter breakdown rates (/d) were faster in temperate (k = 0.023–0.017) than in tropical (k = 0.014) or Mediterranean (k = 0.014–0.009) streams. Leaf-litter breakdown rates (/degree day) also were higher in the temperate stream (k = 0.0018–0.0032) and similar between the other 2 streams (k = 0.008–0.0012). Colonization of leaves by aquatic hyphomycetes was faster in the temperate stream (maximum = 421 μg ergosterol/g of leaf by day 24) than in the tropical Cerrado or Mediterranean streams. However, peak ergosterol content was highest in the tropical Cerrado stream (573 μg/g on day 75). Ergosterol content was lowest in the Mediterranean stream (maximum = 341 μg/g on day 7). Total microbial biomass (as ATP) was higher in the tropical Cerrado stream (maximum = 531 nmoles/g on day 75) than in the Mediterranean (maximum = 108 nmoles/g on day 92) and temperate (maximum = 93 nmoles/g on day 7) streams. These results suggest either that not all microorganisms associated with leaves were involved in leaf-litter breakdown or that other less efficient microorganisms than fungi were involved in leaf-litter breakdown in the tropical stream. Leaves exposed to invertebrates (coarse-mesh bags) decomposed significantly faster than leaves protected from invertebrate feeding (fine-mesh bags) only in the temperate stream. This result suggests that invertebrates were important mediators of leaf-litter breakdown only in the temperate stream. A larger proportion of invertebrates recovered from decomposing leaves were shredders in the temperate stream (nearly 5%) than in the Mediterranean (1%) and tropical Cerrado (0%) streams. Leaf-litter processing rates increased with discharge and NO3 concentration in the water. Our results suggest that the positive effect of temperature on breakdown rates of allochthonous organic matter in streams can be overridden by nutrient content in the water and the presence of invertebrate shredders.