The Role of Invertebrates on Leaf Litter Decomposition in Streams – a Review

MANUEL A. S. GRAÇA

Departamento de Zoologia, Universidade de Coimbra, 3004–517 Coimbra, Portugale-mail: [email protected]

The Role of Invertebrates on Leaf Litter Decompositionin Streams – a Review

key words: decomposition, shredders, aquatic fungi, streams, detritus

Abstract

Leaves entering low order streams are subject to physical abrasion, microbial degradation and inver-tebrate fragmentation. Aquatic invertebrates feeding on leaves are known as shredders and their densi-ties tend to be correlated with the spatial and temporal accumulation of organic matter in streams. Shred-ders discriminate among the variety of leaves normally found in the stream; this discrimination may berelated to differences in leaf toughness, plant nutrient content of leaves and the presence of secondarycompounds. Shredders also consume leaves preferentially after the establishment of a well-developedmicrobial community. This preference may be the result of changes in leaf matrix carried out by themicrobial community or the presence of fungal hyphae with a higher nutrition value than the leavesthemselves. The immediate consequence of invertebrate feeding on leaves is the incorporation of plantmaterial into secondary production and the fragmentation of leaves. The relative importance of fungiand 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 poten-tial to control the diversity and abundance of shredders and changes in riparian vegetation have thepotential to affect the assemblages of aquatic invertebrates.

1. Introduction

For a long time, allochthonous organic matter has been considered the main energy sourcefor stream biota of low order streams (VANNOTE et al., 1980). Decomposition of this orga-nic matter is a continuous process involving biotic (decomposers and detritivores) and abio-tic (physical abrasion) factors. Therefore, the interaction “leaves-decomposers-detritivores”has been a central research area for stream ecologists, leading, in recent years, to an increasenumber of papers on decomposition, the role of microbes in this process, and their ecology(for reviews see BÄRLOCHER, 1992; MALTBY, 1992). The trophic ecology of stream in-vertebrates was early reviewed by CUMMINS (1973), CUMMINS and KLUG (1979), ANDERSON

and SEDELL (1979) and more recently by WALLACE and WEBSTER (1996). Other papers havealso analysed several aspects of the trophic ecology of detritivores (e.g. SUBERKROPP, 1992;GRAÇA, 1993). Here I refer to the role of stream invertebrates in litter processing, with aparticular emphasis to research published in the last 10 years.

2. Shredders Are Stream Invertebrates Feeding on Large Particles of Organic Matter

The most representative invertebrates found in streams are generally insects, speciallyEphemeroptera, Plecoptera, Odonata, Diptera and Trichoptera (TACHET et al., 1987). These

Internat. Rev. Hydrobiol. 86 2001 4–5 383–393

II. Leaf Litter Processing and Invertebrates

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organisms are generally not classified by what they eat, but rather by the way they feed(WALLACE and WEBSTER, 1996). In this sense, predators get their nourishment from otheranimals’ tissues. Grazers-scrapers feed on the biofilm covering the surface of submergedstructures such as stones and plant stalks. Other invertebrates feed on fine particulate orga-nic matter (FPOM), filtered from the water column or taken directly from the substrate. Theyare known as collector-filterers, and collector-gatherers respectively. A last group of orga-nisms, known as shredders, feed on coarse particulate organic matter (CPOM). Exceptperhaps for predators, all the others can, to various extents, behave as detritivores. That isthe case of grazer-scrappers, if we consider that the biofilm is composed not only by algaebut also by bacteria, fungi and organic matter embedded in a mucilaginous matrix (LOCK,1993).

Gammarid amphipods, many plecoptera, trichoptera and some tipulid dipterans are typi-cal shredders (TACHET et al., 1987). However, in the absence of those groups, other inver-tebrates may act as shredders. For example, in a Morocco stream lacking of trichoptera andplecoptera, CHERGUI and PATTEE (1991) reported a high shredding effect of the gastropodsMelanopsis praemorsa and Physa acuta on leaves.

On the other hand, shredders do not feed exclusively on detrital CPOM. FRIBERG andJACOBSEN (1994) showed that shredders supplement their diet with algae and macrophyte tis-sue even when decomposing leaves were present. Moreover, MIHUC and MIHUC (1995) fed5 species of shredders exclusively with CPOM, FPOM or periphyton and only in one casea reduction of growth in specimens deprived of leaves was observed. FRIBERG and JACOB-SEN (1999) showed that growth of the shredder Sericostoma personatum was not reducedwhen fed on fresh filamentous algae Microspora sp. Finally, shredders have been reportedto also feed on other invertebrates (SOLEM and JOHANSSON, 1991).

In temperate zones litter fall and therefore litter input to streams is seasonal (ABELHO andGRAÇA, 1996, 1998; POZO et al., 1997). This may cause detritus shortages in some seasons(but see PETERSEN et al., 1989) and a consequent food limitation for shredders. It has beenfrequently observed that peaks in shredder densities match peaks of organic matter accu-mulation, regardless of this accumulation occurring in summer (BOULTON and LAKE, 1992)or autumn (GILLER and TWOMEY, 1993; HAAPALA and MUOTKA, 1998). TOWNSEND and HILD-REW (1988) suggested that the density of shredders may be controlled by the availability oforganic matter, which in turn is dependent on retentiveness of streams. In a long term (4 years) manipulative experiment in the Coweeta basin (North Carolina, USA), the exclu-sion of leaf litter resulted indeed in significant reductions of biomass (~ one-sixth) or abun-dance (~ one-tenth) of benthic invertebrates, especially shredders, gatherers and predatorsand, therefore, a reduction in the secondary production (WALLACE et al., 1997, 1999).

Several studies have also shown a significant correlation between stream invertebrates andthe amount of benthic organic matter retained (e.g., HILDREW et al., 1991; PROCHAZKA et al.,1991; BOULTON and LAKE, 1992; FRIBERG, 1997). ROEDING and SMOCK (1989) reported thattotal shredder density and biomass were 4–5 fold higher in debris dams than on sediment,even though dams occupied only 3% of the stream surface. The same authors referred anannual production (dry mass) of 11.6 g · m–2 in dams and only 1.5 g · m–2 on the sediment.

This spatial distribution of shredders can be the consequence of (a) invertebrates beingcontrolled by the same hydraulic factors responsible for detritus accumulation (b) a directresponse to food accumulation and (c) a response to an increase of habitat heterogeneity.

Manipulating litter input in streamside channels, RICHARDSON (1991) showed that den-sities of 2 shredders responded to litter availability. DOBSON et al. (1992) increased litterstanding crop by enhancing litter retention, which resulted in an increase in shredder abun-dance.

In contrast, research carried out in New Zealand revelled a fauna characterised by a poor-ly representation of shredders and a weak relationship between detritus inputs and detriti-vore biomass (LINKLATER, 1995).

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3. Shredders Are Selective Feeders

Under natural conditions, litter in streams is composed of leaves from diverse plant spe-cies. Under laboratory conditions, when given the choice, shredders preferentially feed oncertain leaf types while rejecting others (NOLEN and PEARSON, 1993; CANHOTO and GRAÇA,1992, 1995; SCHULZE and WALKER, 1997). Selection among leaves seems to have a physio-logical basis: the selected leaves are generally the ones promoting higher growth while therejected ones are poor quality resources. For instance, under laboratory conditions, Tipulalateralis preferentially fed on alder (Alnus glutinosa) leaves while rejecting leaves of oak(Quercus faginea) and eucalyptus (Eucalyptus globulus); when the rejected leaves were pre-sented as a sole food source the result was a low growth and survivorship when comparedwith specimens fed on preferred leaves (CANHOTO and GRAÇA, 1992, 1995).

Field data on leaf colonisation by invertebrates support laboratory experiments: In thefield, shredders have been reported to be more abundant on laboratory preferred leaves suchas alder and less abundant on low quality leaves (BASAGUREN and POZO, 1994; MALMQVIST

and OBERLE, 1995; WEBSTER and BENFIELD, 1986).Three aspects may explain this selectivity among leaves: (a) toughness, (b) nutrient con-

tent and (c) the presence of plant secondary components (chemical defences). Leaf tough-ness can be a physical barrier for invertebrate feeding, given that harder leaves are probablymore difficulty to pierce than soft ones. NOLEN and PEARSON (1993) reported that, unlikelater instars of Anisocentropus kirramus (Trichoptera: Calamoceratidae), younger instar werenot able to feed on tough leaves. This relationship between consumption and hardness hasalso been reported for other detritus-based systems. For the generalist salt-marsh crab, Arma-ses cinereum, leaf toughness was more important in determining feeding preferences thansecondary chemistry, silica, salt and protein (PENNINGS et al., 1998). A significant inverserelationship between leaf toughness and feeding rates was also observed for the terrestrialdetritivore Porcillio dispar (MOLLES and GRAÇA, unpublished).

Nutrient content of leaves is a very important factor for animals exploring the detrituspool (see next section). In general, the leaves preferred in laboratory selection experimentsare the ones containing higher nutrient content, especially nitrogen (IRONS et al., 1988). Sig-nificant positive correlations between nitrogen content of several leaves offered as food andgrowth have been reported for the detritivores Porcillio dispar a terrestrial isopod (MOLLES

and GRAÇA, unpublished) and larvae of Aedes spp. (WALKER et al., 1997).However, this subject may still be more complex: FRIBERG and JACOBSEN, (1994) report-

ed that the preferences of two shredders for six food items including decomposing leaves,algae and macrophytes were not correlated with nitrogen content, C : N ratios or leaf tough-ness. This suggests that selection among leaves may be influenced by various combinationsof several factors.

Finally, some secondary compounds, presumably involved in the defence of plants, areknown to remain active after leaf senescence (ROSENTHAL and JENSEN, 1979). They may betoxic, interfere with digestion or give a bitter taste acting as a feeding deterrent. Amongthose compounds are mainly polyphenolics (tannins, lignins and others), but non-proteinaminoacids, terpenoids, saponins, flavonoid pigments, and alkaloids may also be present(ROSENTHAL and JENSEN, 1979; WATERMAN and MOLE, 1994).

Deterrent inhibitory effect of phenolics have been reported for marine systems (e.g. STEIN-BERG, 1988), saltmarsh consumers (BÄRLOCHER and NEWELL, 1994) and freshwater detriti-vores (CANHOTO and GRAÇA, 1995; GRAÇA and BÄRLOCHER, 1998). Moreover, the applica-tion of polyphenolics to food with low phenolics resulted in reduced consumption rates andgrowth (WINTER and ESTES, 1992; KOK et al., 1992; CANHOTO and GRAÇA, 1999).

Invertebrates and Leaf Litter Decomposition 385

4. Detritivores Preferentially Feed on Microbial Conditioned Leaves

When leaves fall from the trees they are already colonised by microorganisms (PAUL andMEYER, 1996). However, it has been shown that the biomass of microorganisms associatedwith leaves greatly increases soon after leaves enter the streams (e.g. SUBERKROPP et al.,1983). This increase is attributed to the colonisation by aquatic hyphomycetes (BÄRLOCHER,1992) which are assumed to replace the terrestrial microbes as decomposition proceeds inthe water (GRAÇA and FERREIRA, 1995; RODRIGUES and GRAÇA, 1997). Bacterial coloniza-tion of leaves has been shown to be relatively unimportant in terms of biomass (FINDLAY

and ARSUFFI, 1989; BALDY et al., 1995).The colonisation of leaves by aquatic hyphomycetes with its implications for decomposi-

tion is known as conditioning (GOLLADAY et al., 1985). There is now a large body of evi-dence suggesting that conditioning is a very important process for stream shredders. Shred-ders have been shown to preferentially feed on conditioned leaves (CHERGUI and PATTEE,1991; GRAÇA et al., 1993b; KIRAN, 1996). In the field, the abundance of shredders has alsobeen reported to be strongly correlated with fungal biomass in leaves (ROBINSON et al.,1998). Of the several explanations (BÄRLOCHER and KENDRICK, 1975; GRAÇA, 1993), two ofthe most apelative are: (1) invertebrates benefit from the fungal action on the leaves and (2)invertebrates feed on fungi.

With some exceptions, detritivores do not seem to have the enzymatic ability to break-down the abundant structural compounds of leaves (BÄRLOCHER and PORTER, 1986; WAL-TERS and SMOCK, 1991). In some cases, detritivores possess gut endosymbionts (KLUG andKOTARSKI, 1980; SINSABAUGH et al., 1985), which may be involved in the digestion of cel-lulose; the same being known for terrestrial detritivores (e.g. ZIMMER and TOPP, 1998). Fungiand bacteria colonising leaves produce cellulases, xilanases, pectinases and other enzymes(BÄRLOCHER, 1992; JENKINS and SUBERKROPP, 1995; RODRIGUES and GRAÇA, 1997) able todigest plant cell walls and to liberate simple compounds which can be assimilated by detri-tivores. Therefore, fungi increase the palatability of leaves by promoting the transformationof inedible plant material into edible compounds. Moreover, fungal colonisation results in adecrease of leaf toughness (SUBERKROPP et al., 1983; GRAÇA et al., 1993b; JENKINS and SUBERKROPP, 1995) which may facilitate feeding by shredders.

Fungi themselves may be a feeding target for shredders. It is generally accepted that in-sect herbivores are limited by nutrients more than by energy (BEGON et al., 1990). If that istrue for terrestrial insect herbivores, we may expect that the same applies to animals feedingon detritus given that during senescence, nutrients in leaves decrease due to reabsorption(STAPEL and HEMMINGA, 1997). Based on a review of a large number of plant species, AERTS

(1996) calculated that nearly 50% of N (n = 287) and P (n = 226) in leaves were reabsor-bed during senescence. It is ecologically significant that nutrient content in fungi myceliacolonising leaves is higher than the nutrient content in the senescent leaves: whereas insenescent leaves nitrogen content may range from 0.5 to 1.5%, in fungal mycelia it mayrange from 1 to 7% (SLANSKY and SCRIBER, 1985). In terms of nitrogen (and other nutrients)content, fungi are therefore a better food source than leaves. This also implies that colonisedleaves are a better food source than uncolonised ones.

Discrimination for fungi in leaves only has an ecological significance if the fungal bio-mass is enough to cover the energetic requirements of consumers. Recent papers have esti-mated that up to 10–15% of decomposing leaves correspond to fungal biomass (GESSNER

and SCHWOERBEL, 1991; GESSNER and CHAUVET, 1994). According to PAUL and MEYER

(1996), the biomass of fungi in decomposing leaves at an Appalachian stream was enoughto meet the carbon ingestion demand of shredders, from October to January, even consider-ing that fungal biomass estimates were on the lower range of other estimates (but see FIND-LAY et al., 1986). A preferential feeding for fungi was also observed in other detritus-basedsystems. The salt-marsh snail Littoraria irrorata caused a higher decrease in fungal than in

386 M. A. S. GRAÇA

leaf biomass when feeding on decaying Spartina leaves, even when having the enzymaticcapability to digest cellulose (NEWELL and BÄRLOCHER, 1993; GRAÇA et al., 2001). Pre-ferential feeding towards fungi when compared with fungal modified leaves was reportedfor the caddisfly Psychoglypha sp. (ARSUFFI and SUBERKROPP, 1988) and the isopod Asellusaquaticus, but not for the amphipod Gammarus pulex (GRAÇA et al., 1993a).

Independently of the key factors behind the preference for conditioned leaves, it has beenfound that feeding exclusively on unconditioned leaves has costs in terms of growth (GRAÇA

et al., 1993b; LAWSON et al., 1984), survivorship (BUELER, 1984) and reproductive output(GRAÇA et al., 1993b). Fungi are, therefore, a key factor for the trophic ecology of streamdetritivores.

Fungi may also provide shredders with micronutrients not present in leaf tissues. CARGILL

et al. (1985) showed that late instars of the shredder caddisflies preferentially ingested lipid-coated detritus. Crude lipid and the neutral lipid fraction from aquatic hyphomycetes, werealso preferred.

Fungal colonisation is important for the trophic ecology of shredders, but decompositionof leaves does not culminate in invertebrate feeding (GESSNER et al., 1999; see next section).Both invertebrates and fungi act over the leaf substrates and they may even compete fornutrients in leaves (BÄRLOCHER, 1980).

Consumption by stream shredders may not only be affected by the conditioning status butalso by the fungal species colonising leaves. In laboratory experiments it has been shownthat shredders discriminate among leaf substrates colonised by different fungal species(ARSUFFI and SUBERKROPP, 1989; SUBERKROPP, 1992; GRAÇA et al., 1993a).

The basis of such selection is not clear. Possible explanations may be related with differ-ences in the synthesis of micronutrients by fungi, the production of feeding stimulants or theproduction of distasteful compounds (ARSUFFI and SUBERKROPP, 1989). RONG et al. (1995)showed that the rank preferences of two consumers for leaves colonised by different fungalspecies could be reproduced by extracting mycelia with non-polar solvents and applying theextracts to uncolonised leaves.

By feeding on conditioned leaves and among patches colonised by different fungal species, invertebrates may also influence the assemblages of aquatic hyphomycetes. In astream treated with insecticide, SUBERKROPP and WALLACE (1992) reported a higher amountof conidia in the water than in a reference stream with a normal invertebrate community.However, no differences were found in fungal species composition.

5. Shredders Contribute to the Decomposition of Leaves

Soon after leaves enter the streams, they are rapidly colonised by aquatic hyphomycetesand also by invertebrates, especially shredders (MCARTHUR and BARNES, 1988). By feedingon leaves, shredders incorporate some nutrients in secondary production, accelerate leaf frag-mentation and produce abundant faecal pellets. Shredders have therefore the potential toaccelerate decomposition.

One widely used method to assess the role of invertebrates on leaf breakdown is the useof coarse meshed (~5mm) and fine meshed (~0.5mm) litter bags. The results of such exper-iments are contradictory. Some authors have reported higher mass loss in coarse mesh bags(e.g. IMBERT and POZO, 1989; HOWE and SUBERKROPP, 1994) whereas others have observedno differences (e.g., STOCKLEY et al., 1998). These contrasting results may be related to dif-ferences in invertebrate densities in streams.

STEWART (1992) implanted leaves in streams with high and low densities of invertebra-tes; when invertebrates were abundant, leaves decomposed approximately 15 times faster incoarse than in fine mesh bags. However, when densities of invertebrates were low, this dif-ference was also lower, and in some cases no differences were observed. Consistently, rapid


processing rates of leaves were reported by ROBINSON et al. (1998) at sites where the shred-der Acrophylax zerberus was abundant in contrast to sites where only few shredders occur-red.

CHERGUI and PATTEE (1991) reported that shredding by gastropods could be responsiblefor 8 to 40% of leaf fragmentation. According to PETERSEN et al. (1989) macroinvertebrateassimilation, defined as the sum of respiration and growth, removed annually 11.6% of thedetritus standing crop.

One of the most convincing evidences of the importance of detritivores in the decompo-sition of organic matter was provided by the research taking place in North Carolina, USAand reported by CUFFNEY et al. (1990) and WALLACE et al. (1995). By treating a stream withinsecticide, the authors were able to reduce the invertebrates in the stream. The insecticidedid not affect microbial assemblages (activity or biomass), but the invertebrate reductionresulted in a 50–74% reduction of leaf decomposition and 33% of FPOM export.

The production of FPOM can be ecologically important for populations of collectors inha-biting lower reaches of streams. In this sense, we can say that there is a functional link alongthe rivers (VANNOTE et al., 1980). In practice, this relationship between FPOM productionby shredders and its use by collectors has been poorly investigated. However, DIETERICH

et al. (1997), working in a temporary stream, found that shredders emerged early in the season, whereas collectors emerged later. Moreover, in laboratory conditions, the presenceof shredders enhanced the growth of collectors.

6. Riparian Vegetation

Given that (a) riparian vegetation is the source of leaves and, therefore the main energysource to streams, (b) stream invertebrates are selective among leaf types (see previous sec-tions) and (c) invertebrates may be limited by food (RICHARDSON, 1991; DOBSON et al., 1992;WALLACE et al., 1997, 1999), it is plausible that forest cover may influence the populationof shredders. Literature references regarding this subject are some how contradictory: GRUBS

and CUMMINS (1994) reported a low number of shredders in summer in a stream lacking ofslow processing leaf material in comparison with a reference stream where slow processingleaves were present. This information is consistent with the reported by STOUT et al. (1993),which compared the populations of shredders in streams running to through a mature forestand streams running through a forest cleared 11 years before. The mature forests were richerin trees with slow decomposing leaves whereas the opposite was found for perturbed forests.The standing stock of leaves was higher in the mature forests. However, total shredder pro-duction was higher in perturbed forest. ABELHO and GRAÇA (1996) showed that in streamsrunning through monocultures of eucalypt plantations had a lower abundance of invertebratetaxa comparatively to mixed deciduous forests. This was related to a low quality of euca-lyptus leaves for shredders (CANHOTO and GRAÇA, 1995, 1999).

However, in a study carried out in New Zealand, LINKLATER and WINTERBOURN (1993)did not find differences in densities and life-history of invertebrate shredders inhabiting streams which differed in the quality of leaves produced by the riparian cover. LESTER et al.(1994) examined the effects of introduced willow tree species (Salix fragilis) on macroin-vetebrate densities in New Zealand and found that invertebrate densities and biomass weresignificantly reduced at willow lined sections of the stream. This was attributed to a reducedsubstrate size and lowering of primary production due to a shading effect at the Salix linedsections. The significantly higher CPOM at willow lined sections did not result in an increaseof invertebrates, as reported for other regions.

CUMMINS et al. (1989) proposed a model to evaluate how changes in riparian vegetationaffect aquatic systems. According to the model, seasonal changes in shredder biomass can

388 M. A. S. GRAÇA

be predicted based on the composition of riparian vegetation or the percentage of covering.Deviations from the predicted shredder biomass could therefore be used as indicator of animpact. However, this model has not been widely tested.

7. Final Remarks

The nutrient and energy content of leaves are incorporated into secondary production byfungi and invertebrates (GESSNER et al., 1999). Leaves are also fragmented as a result of themicrobial enzymatic degradation, invertebrate feeding and physical abrasion. Decompositiondoes not, therefore, stop with the fragmentation of leaves. The resulted fine particles oforganic matter and dissolved organic matter are further decomposed by microorganisms orused as food by collectors. The role of bacteria, fungi and consumers in the total breakdownof those materials is out of the scope of the present paper. However, they are an importantstep to total decomposition of litter.

There are several areas of potential interest regarding the role of invertebrates on leafdecomposition. M. GESSNER rised the question (2nd European Meeting on Litter Breakdownin Rivers and Streams) whether decomposition rates may be used as a functional tool toassess changes in water quality. If shredders play a key role in leaf decomposition / frag-mentation, one would expect that the elimination of shredder populations will result in adecrease in decomposition rates. However, little is known on the relationship between waterquality – shredder density – decomposition (but see the paper by PASCUAL et al. in this issue).

With some exceptions, all references cited in this paper regard to research taking place intemperate regions (Europe, North America, New Zealand). Looking at papers cited in theCurrent Contents (Agriculture, Biology and Environmental Sciences) regarding litter decom-position in freshwaters for the period 1996–1997, 79% (n = 47) were carried out in tempe-rate zones. I obtained a similar proportion (82%, n = 45) of papers dealing with the trophicecology of shredders, for a longer period. A relevant question in this context is whether wecan generalise about what we know on detritus based systems to non-temperate regions. Forinstance, COVICH (1988) suggest that the apparently high flexibility in life-history and mobi-lity of neotropical consumers may be reflected in a more flexible exploitation of food sour-ces and therefore food webs in the tropics are dominated by generalist feeders. The relevantquestion in the context of this paper is whether tropical shredders are more generalist thantemperate ones. Our preliminary observations (GRAÇA et al., 2001) do not seem to corrobo-rate this strategy.

What is the relative importance of microbial degradation and invertebrate feeding in thedecomposition of leaves? The recent quantitative approaches for measuring fungal and bac-terial biomass and production may give us more information on this process. Based on whatwe know on the factors affecting the decomposition of leaves and the feeding activities ofshredders, can we develop models predicting the ecological effects of plant replacement inthe riparian zones? How do shredders locate conditioned leaves in a heterogeneous streamenvironment? What is the fate of secondary plant compound in decaying leaves? How dosecondary plant compounds affect invertebrate feeding? These are some of the still relevantquestions in the relationship between invertebrates and decomposition.

8. Acknowledgements

I would like to express my thanks to LÍLIA SANTOS, CRISTINA CANHOTO, MANUELA ABEL-HO, NUNO COIMBRA and two anonymous referees for suggestions and criticisms along sever-al versions of this paper.


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The Role of Invertebrates on Leaf Litter Decomposition in Streams – a Review