Coarse detritus in oligotrophic lake littoral zones – utilization by invertebrates and

contribution to carbon flow

Irene Bohman

Department of Biology and Environmental Science

University of Kalmar Sweden

2005

AKADEMISK AVHANDLING

som kommer att offentligen försvaras för avläggande av filosofie doktorsexamen vid Naturvetenskapliga fakulteten vid Högskolan i Kalmar fredagen den 15 april 2005.

Doctoral Dissertation, 2005 University of Kalmar Faculty of Natural Science Dissertation series, No. 19 Irene Bohman Department of Biology and Environmental Science University of Kalmar SE 391 82 Kalmar Sweden Cover photos: Irene Bohman © 2005 Irene Bohman University of Kalmar, Faculty of Natural Science, Dissertation series, No. 19, ISBN: 91-89584-41-4, ISSN: 1650-2779, pp. 1-38.

2

“Everything that dies someday comes back” B. S.

3

Abstract The general aim of this thesis was to increase the understanding of the

mechanisms behind coarse detritus turnover in oligotrophic lake littoral zones. The reason for this interest is that small lakes located in forested areas often display dependence on detritus based energy sources, both external and internal. Additionally, in lake ecosystems the coarse detritus resource has been comparatively less studied than in streams. Both dissolved and particulate external detritus constitute extra energy contribution to ecosystems, but only if some organisms can assimilate the provided matter. The most common capable organisms to do so in freshwaters are bacteria, fungi and invertebrates, and they return a variety of intermediary products available for other consumers. Further, it has been suggested that a positive relation between species diversity and ecosystem function exists. Therefore the study of both the community and individual species of decomposers may provide information significant to understand changes in ecosystem function.

Within the outline of the thesis, I studied what species are involved in the processing of coarse detritus carbon and what are the key routes for the further use of this littoral carbon. I specially emphasize the temporal pattern of the detritus turnover and the availability of decomposition products to other organisms in the lake ecosystem.

The results showed that microorganisms and invertebrates in the lake littoral zone successively process carbon from coarse detritus during the whole year. The weight loss from coarse detritus displayed a seasonal distinctive pattern temporally connected to shredder appearance and growth. Therefore, I emphasize the key role of certain trichopteran shredder species for litter processing in lakes in this region, southeast Sweden. At the same time, the shredder function of Asellus aquaticus was less important than expected. A. aquaticus was shown to utilize of a quite broad range of food sources and to prefer other habitats during the main decomposition period for leaf litter. In the laboratory I discovered that the decomposition of leaf litter principally results in two products, DOM from passive leakage and FPOM from active leaf litter processing by shredders. The experiment showed that shredders have the potential to consume leaf litter resources before microbial decomposition influence litter weight considerably. Thus, the quantitative importance of microorganisms (fungi and/or bacteria) for leaf litter turnover is suggested to directly depend on density of shredders in lake littoral zones of the kind studied. I have also shown that the combination of detritus types and invertebrate processor species influence the temporal accessibility of intermediate decomposition products.

I conclude that coarse detritus is an attractive food resource for invertebrates also in small oligotrophic lakes like it is in smaller streams. I also conclude, that the lake specific set of shredder species recycle this carbon resource yearly in a fine-scaled temporal sequence – adapted to the predictable seasonal variation of detritus quality on these latitudes. Further, I stress the importance of increased knowledge of decomposing processes before predicting the effects of disturbance on this kind of widespread freshwater systems. Finally, I propose that the decomposition rate of coarse detritus should be tested as an assessment tool for integrating disturbances on ecosystem functions in small oligotrophic lakes, respecting the unique lake characteristics.

4

Sammanfattning Syftet med denna avhandling är att öka förståelsen av hur grovt organiskt material,

sk grovdetritus, tex löv och makrofytrester, bryts ner i sjöars strandzoner. Motivet bakom intresset för detta är att små näringsfattiga sjöar i skogsrika områden ofta är beroende av tillförsel av energi utifrån och att nedbrytningen av grovdetritus är relativt lite undersökt i sjöar. Utifrån tillförd detritus, i löst och partikulär form kan utgöra extra energikälla för sjöekosystem, men bara om några organismer kan tillgodogöra sig detta organiska material. I sötvatten kan sådana organismer vara bakterier, svampar och ryggradslösa djur. Under nedbrytningsförloppet produceras en mängd mellanprodukter som kan användas av andra konsumenter tex fisk. På så sätt återcirkuleras energi och näring från detritus utan fullständig nedbrytning. Vidare har det föreslagits att hög biodiversitet kan resultera i hög ekosystemfunktion, tex effektiv nedbrytning. Därför kan studier av både samhällen och enskilda arter av nedbrytare öka förståelsen av förändringar i hela ekosystemets funktion.

Inom ramen för avhandlingen har jag studerat vilka arter som deltar i nedbrytningen av grovdetritus och vilka möjliga vägar för det fortsatta nyttjandet av detta material som finns. Jag har särskilt betonat det säsongsmässiga mönstret för omsättningen av grovdetritus och för tillgängligheten av mellanprodukter.

Resultaten visar att både mikroorganismer och ryggradslösa djur successivt processar tillgängligt grovt organiskt material under hela året. Viktminskningsmönstret över året hos löv och makrofytrester är nära kopplat till förekomst och tillväxt hos olika arter av nedbrytande ryggradslösa djur, sk fragmenterare. Av de vanligaste förekommande tio arterna fragmenterare, var nio nattsländelarver. Därför drar jag slutsatsen att dessa arter av nattsländelarver spelar en avgörande roll för omsättningen av grovdetritus i sjöstränder i sydöstra Sverige. Samtidigt visar resultaten att sötvattengråsuggan spelar mindre roll för nedbrytningen av grovdetritus än förväntat. Denna art föredrar andra födoämnen åtminstone under våren och undviker de grunda bottnarna där grovdetritus finns under vintern. I laboratorieexperiment har jag visat att nedbrytning av löv i närvaro av fragmenterare huvudsakligen ger upphov till två olika produkter: löst organiskt material och finpartikulära rester. Därmed har jag visat att fragmenterare kan omsätta grovdetritus snabbare än mikroorganismer. Slutsatsen blir att mikroorganismernas kvantitativa bidrag till nedbrytning av grovdetritus är beroende av mängden fragmenterare. Jag har också visat att olika kombinationer av detritussorter och fragmenterararter kan påverka när olika nedbrytningsprodukter blir tillgängliga för andra organismer.

Sammanfattningsvis har jag visat att grovdetritus är en attraktiv födoresurs för ryggradslösa djur i näringsfattiga sjöars strandzoner, precis som i små bäckar. Dessutom visar jag att de arter av fragmenterare som är speciella för sjöar, tillsammans omsätter tillgängligt grovdetritus i ett finskaligt tidsmönster över året. Detta mönster har utvecklats genom anpassning till trädens lövfällning och nedvissningen av vattenväxter som sker på hösten i vårt klimat. Jag vill också betona att ökade kunskaper om nedbrytning av grovdetritus krävs för att kunna förutsäga effekter av olika störningar i dessa ekosystem. Slutligen rekommenderar jag att nedbrytnings-hastigheten för grovdetritus testas som mått på ekosystemfunktion också i sjöar.

5

CONTENTS

Abstract 4 Sammanfattning 5 Contents 6 List of papers 7 Introduction 8 Heterotrophic ecosystems 8 Decomposition – an important ecosystem function 9 Dissolved organic matter (DOM) and microbial growth 10 Coarse detritus processing and invertebrate growth 11 Connection between lake compartments 11 Decomposition and biodiversity 12 Aims of the thesis 13 Methods 14 General approach 14 Temporal aspects 14 Study area 15 Principal methods and modifications 15 Detritus sources 15 Litterbag technique 16 Fine particulate detritus 16 Species identification 16 Microbial methodology 17 The natural stable isotope approach 17 Results and discussion 17 Seasonality of CPOM turnover 18 Links to shredder activity 19 Comparisons of weight loss rates 20 The lake shredder species and their specific roles as decomposers 21 Realized food niche 23 Shredding capacity at ecosystem level 23 A modified view on species-specific shredder function 24 Shredders vs microorganisms 25 Products from decomposition 25 Dissolved fractions 25 Particulate fractions 27 Conclusions and perspectives 28 Perspectives of threats and protection 28 Research perspectives 29 Literature cited 30 Acknowledgements 38

6

List of papers This thesis is based on the following papers, referred to in the text by roman numerals: I Bohman, I. M. and Herrmann, J. The timing of winter-growing shredder

species and leaf litter turnover rate in an oligotrophic lake, SE Sweden (submitted).

II Bjelke, U., Bohman, I. M. and Herrmann, J. 2005. Temporal niches of

shredders in lake littorals with possible implications on ecosystem functioning. Aquatic Ecology, 39: 41-53.

III Bohman, I. M. and Tranvik, L. J. 2001. The effects of shredding invertebrates

on the transfer of organic carbon from littoral leaf litter to water-column bacteria. Aquatic Ecology 35: 43-50.

IV Bohman, I. M. and Bjelke, U. Seasonal variation of food sources in lake littoral

benthic fauna, as indicated by stable isotopes (submitted). V Bohman, I. M. Comparison of temporal weight loss patterns between two

decomposing aquatic macrophytes (manuscript). Published papers are reprinted with the permission of the publishers: Springer Science + Business media.

7

Introduction Classic studies in running waters have long been the basis for both the theoretical

framework and research trends regarding the decomposition of coarse organic matter. The River Continuum Concept describes the river changing from a heterotrophic system to more autotrophic along its reaches and relates sources of organic matter to the functional structure of the benthic community (Vannote et al. 1980). Several reviews summarize results from the extensive studies of decomposition performed in running waters (e.g. Anderson and Sedell, 1979; Webster and Benfield, 1986; Wallace and Webster, 1996; Graça, 2001).

The mechanisms behind and significance of the decomposition of coarse detritus have, by comparison, been less studied in lake ecosystems. Small oligotrophic lakes are in some respects similar to small running waters: small water bodies, located in forested areas, with low primary production and thus dependency on allochthonous energy. However, the dissimilar system complexity in lakes combined with more stable environments creates opportunities for a greater variety of resources and other species than in small streams. Recycling of allochthonous carbon in littoral zones was suggested early on to be important for the whole lake ecosystem, but was insufficiently investigated (Pieczynska, 1972). Only a few papers have been published since on the transformation of coarse detritus in small oligotrophic lakes (Casper, 1987; Oertli, 1993; Tuchman, 1993; Henrikson and Oscarsson, 1996; Pope et al., 1999).

Freshwater ecosystems are often vulnerable to environmental stressors such as acidification, eutrophication, pollution, climate change and anthropogenic impact on vegetation and hydrology in the catchments (e.g. France et al., 1996; Brönmark and Hansson, 1998; Sala et al., 2000; Wetzel, 2001). Focusing on smaller oligotrophic lakes, acidification, climate change and clear-cutting in riparian zones represent particularly serious threats, possibly influencing ecosystem function. Coarse detritus turnover rate has been used as an assessment tool to monitor ecosystem functioning in running water systems (e.g. Allard and Moreau, 1986; Pascoal et al., 2003; Dangles et al., 2004) but only rarely tested in small lakes (Kelly et al., 1984; Perry and Troelstrup, 1988). Heterotrophic ecosystems

If the external carbon sources (allochthonous) served to the ecosystem exceed the internal carbon supply (autochthonous), ecosystems become net heterotrophic. The degree of heterotrophy of lakes is expected to increase with decreasing size and nutrient status (del Giorgio and Peters, 1994; Cole et al., 2000; Caraco and Cole, 2004). The reason for this is that the edge effect from terrestrial production is often substantial in smaller aquatic systems. Gasith and Hasler (1976) predicted that allochthonous litter input dominates over planktonic primary production in oligotrophic lakes with a wooded shoreline, ordinary shore irregularity and a surface less than 200 ha. Net heterotrophic lakes depend on allochthonous detritus of very varying quality and structure, namely the full continuum from dissolved labile to recalcitrant particulate detritus (Thurman, 1985).

8

Detrital pathways of energy lack the normal biological feedback mechanisms between consumers and food resources found in primary production based ecosystems. Heterotrophic ecosystems are thus referred to as donor-controlled (Persson et al., 1997), which implies that factors that influence detritus input and decomposition rate might have a controlling effect on nutrient recycling and secondary production based on detritus. Further, a detrital food base in the ecosystem buffer top-down effects and trophic cascades, by increasing the uncoupling between the trophic levels (del Giorgio and Gasol, 1995). At the community level, allochthonous subsidies make the food webs more complex and probably more stable than otherwise (Anderson and Polis, 2004). The local effects of external resources depend on the permeability of habitat boundaries and the inherent potential for utilization of the resources in the local food web (Huxel et al., 2004). Thus, external resources can constitute extra energy and nutrient supply to an ecosystem only if some organisms can assimilate the provided organic matter. The most common organisms capable to do so in freshwaters are bacteria, fungi and invertebrates. “We know that terrestrial organic matter is respired in many lakes, but we are just beginning to learn how important this terrestrial carbon is to the food webs that lead to secondary production of invertebrates and fish” (Cole et al., 2002).

Most research on heterotrophic lakes concerns the dissolved fraction of the allochthonous input (Hessen and Tranvik, 1998; Findlay and Sinsabaugh, 2003). Studies of microbial conversion of both labile and recalcitrant fractions of dissolved terrestrial humic substances are extensive and have shed new light on both the mechanisms and the species involved (Tranvik, 1988, 1992; Bergström et al., 2003). Dystrophic lakes are common in forested areas and can be highly dependent on dissolved humic substances. Organic carbon from terrestrial production was estimated to account for 60–70% of total organic carbon in a forest lake in Sweden (Meili, 1992). Among all the sources of organic carbon fuelling heterotrophic pelagic respiration, the detrital carbon from littorals seems to be the least studied.

Besides the dissolved detritus, decomposition of coarse detritus also returns energy and nutrients in available forms to lake ecosystems. Both invertebrates and fungi are able to transform this refractory material into resources for other consumers (Anderson and Sedell 1979; Suberkropp, 1992). Coarse detritus as a resource for the lake littoral food web has been studied respecting macrophytes (Pieczynska, 1990; Gessner et al., 1996), but generally lake studies on coarse detritus decomposition are rare. Decomposition - an important ecosystem function

Decomposition is in the longer time perspective an essential process in all ecosystems, necessary to maintaining production. The value of an increased understanding of the details of decomposition is therefore equal to that of photosynthesis. Complete decomposition, mineralization, results in energy, CO2 and elementary nutrients. However, during the decomposition sequence a variety of intermediate products become available for consumers. Hence, the products from

9

coarse detritus decomposition, CO2, dissolved organic matter, fine particulate detritus, as well as bacterial, fungal and invertebrate biomass, all contribute to further carbon flow in the ecosystem (Gessner et al., 1999).

The ecosystem service in the form of detritus turnover and element recycling in freshwater systems is mainly provided by two categories of vectors: microorganisms and invertebrates. Most studies tend to focus on one of the two categories of decomposers. However, the microbial- and invertebrate-mediated decomposition processes are closely connected. Conceptualizing littoral leaf litter decomposition in lake littoral zones can illustrate some of the possible interactions, as well as the flow of carbon between different intermediate carbon compartments (Figure 1).

Leaf litter Conditioned litter

DOM

Scrapers

Shredders

FPOM Bacteria, fungi

or mixotrophic protists

Predators

Collectors

Export to pelagic zone or sediment

Figure 1. Carbon compartments (boxes) and carbon flow (arrows) during decomposition of leaf litter in lake littoral zones. All living compartments (grey) release respired and excreted/leaking carbon (CO2 and DOC respectively), which are not marked in the figure. Carbon ending up in sediment or the pelagic zone is removed from littoral recycling. Bold markings indicate carbon flow or compartments partly studied within the scope of this thesis. Dissolved organic matter (DOM) and microbial growth

The release of easily soluble organic matter from leaf litter is extensive during the initial phase of decomposition, with values of about 20–30% weight loss commonly reported for the first days (Petersen and Cummins, 1974; Webster and Benfield, 1986). Most of these dissolved compounds are highly bioavailable and create the necessary conditions for microbial growth, both on surfaces of particles and in the water column. The metabolism of aquatic microbes (e.g. bacteria, hyphomycetes and mixotrophic protists) is the main route for mineralization of organic matter in lakes (Findlay and Sinsabaugh, 2003), although DOM also can be exposed to photodegradation (Anesio et al., 1999). Bacterial biomass in the water column mobilizes particulate carbon available for protozoans, zooplankton and possibly fish – the microbial loop (Stockner

10

and Porter, 1988; Azam et al., 1983). DOM released from other stages of coarse detritus decomposition has not been frequently studied, but the release during shredder activity was considered important for small streams (Meyer and O’Hop, 1983). More refractory fractions (often higher molecular weight) of DOM are only slowly utilized and therefore often further transported with water flow in streams and groundwater, ultimately to the sea. Another pathway for DOM is forming floccules or precipitates on surfaces, which can be exploited by primary consumers including invertebrates (collectors) and thus indirectly by fish (Mann, 1988). In oligotrophic lakes, profundal bacteria living on allochthonous detritus provided nearly half of the food requirements for benthic meiofauna, which in turn are consumed by the macrofauna and fish - a meiofaunal loop (Strayer, 1991; Goedkoop and Johnson, 1992).

The microbial colonization (conditioning) of coarse detritus starts parallel to the initial leakage of DOM. Both bacteria and fungi grow on leaf litter carbon in the developing biofilm. Boulton and Boon (1991) concluded that the combined action of a diverse range of species of both fungi and bacteria is needed for complete decomposition of a whole leaf including the most recalcitrant substances. The relative importance of bacteria and fungi for decomposition processes in freshwater has been discussed by e.g. Newell et al., 1995; Mille-Lindblom and Tranvik, 2003. Fungal biomass and production on leaf litter are generally higher than the bacterial ditto (Bärlocher, 1992). In some streams, typically 7-10% of the leaf litter input ends up as fungal biomass (Carter and Suberkropp, 2004). The microbial biofilm on surfaces may also constitute an important complementary food source for scrapers (Kornijow et al., 1995). Coarse detritus processing and invertebrate growth

Conditioned leaf litter, which have a well-developed biofilm, is preferred to unconditioned litter by most shredder species (Kaushik and Hynes, 1971; Graça, 2001). Shredders are the benthic invertebrates feeding on coarse detritus and are consequently responsible for processing of coarse particulate organic matter (CPOM) into fine particulate organic matter (FPOM). This biological fragmentation reduces particle size and increases the surface area of particles, which enhances growth of both microorganisms and collectors (Merritt et al. 1984, Dieterich et al., 1997). Most shredders depend on microbial exoenzymes or endosymbiontic microbes to digest litter polysaccharides (Sinsabaugh et. al., 1985; Walters and Smock, 1991). Thus, the mutual interdependence of the microorganisms and invertebrates is clear, but the importance of possible competition for leaf litter carbon between the two groups is not clearly demonstrated. Fungi and perhaps bacteria can suffer from shredder activity in two ways: predation and competition for the substrate (Suberkropp, 1992). The invertebrates, shredders, collectors and scrapers, are important for continuing carbon flow, e.g. as food for higher trophic levels in freshwater ecosystems (Covich et al., 1999). Connections between lake compartments

Different forms of detritus are important carrier media for the exchange of nutrients and energy among ecosystems and among components within an ecosystem (Rich and Wetzel, 1978; Wetzel, 1995; MacIntyre and Melack, 1995). Processing of

11

coarse detritus in lakes occurs mainly in littoral zones (Pieczynska, 1990, 1993) and the products such as DOM, FPOM and predator biomass can flow between lake compartments. Dissolved organic matter is easily transported with water movements, while fine particles may need special resuspension events, for example lake circulation, to move primary to deeper sediments in the profundal zone. The active transport of organic matter is probably mediated mainly by various mobile species – such as migratory zooplankton or fish (Bohman et al., 2000; Lampert and Sommer 1997). Moreover, dissolved detritus input from the pelagic zone or terrestrial run-off (France et al., 1996) may also contribute substantially to littoral carbon flow. Decomposition and biodiversity

Links between biodiversity and ecosystem function are of great interest when discussing the effects of species extinction (Wall Freckman et al., 1997; Peterson et al., 1998; Gessner et al., 2004). All dimensions of biodiversity may influence the strength of the links – numerical, functional, taxonomic, ecological, temporal etc. The existing theories concerning biodiversity may not be generally applicable over different habitats. Therefore, special approaches and careful experimental design will probably be needed when investigating these issues in aquatic systems due to their many unique properties compared to terrestrial systems (Covich et al., 2004; Giller et al., 2004).

Positive relationships between species diversity and ecosystem function have been proposed (e.g. Cardinale et al., 2002; Loreau and Naeem 2002). A seasonally changing environment has been suggested to both promote species coexistence and facilitate organisms of different life-history strategies to perform a certain ecosystem function (Loreau, 2000). Benthic invertebrates are central to maintaining the carbon flow in lake littoral food webs (Covich et al. 1999) and shredders are potential key species for this ecosystem function (Palmer et al., 1997). The annual decomposition cycle of coarse detritus in temperate freshwaters is a process where a temporally separated set of species may influence ecosystem functioning. Over time, shredder species differ in the efficiency of performing a certain ecosystem function, due to life cycle, size, growth rate, food preference and habitat selection (Friberg and Jacobsen, 1994; Grubbs and Cummins, 1996; Albariño and Balseiro, 1998; Bjelke, 2005). Therefore, it is predicted that the involved species are of differing importance for the maintenance of the decomposition function. Consequently, studies of individual species of decomposers, shredders or microbes, may provide information significant to understand changes in ecosystem function. Furthermore, combinations of species-specific traits of both detritus and shredder diversity are expected to influence the general decomposition rate and give rise to the characteristic temporal patterns of decomposition.

12

Aims of the thesis The overall aim of this thesis was to increase the understanding of the mechanisms

behind coarse detritus turnover in oligotrophic lake littoral zones. The major hypothesis and questions addressed were: Coarse detritus is a significant carbon resource in small oligotrophic lakes, like it is in small streams. What organisms are involved in the processing of this carbon? What are the key routes for the further use of this carbon in the littoral zone?

Within the framework of the thesis, I studied the initial phase of decomposition of coarse detritus and the availability of intermediate decomposition products. I intended to identify some of the habitat-specific factors, species and carbon pathways unique for the coarse detritus decomposition processes in lake littoral zones. In my investigations, I applied a finer temporal resolution than generally used in studies of this kind, thereby emphasizing the temporal pattern of detritus turnover and availability of decomposition products to other organisms in the lake ecosystem.

Besides the general scarcity of knowledge on carbon circulation from coarse detritus in small heterotrophic lakes and the unknown importance of products from littoral carbon metabolism to other lake compartments, knowledge of lake-specific decomposition characteristics is also necessary to better understand threats posed, to take protective measures and to develop tools for monitoring ecological functions in these kinds of widespread freshwater systems. The specific aims of the papers in the thesis were: I To investigate the natural decomposition rate of the two most common leaf

litter types in a typical oligotrophic lake over two consecutive winter periods and to relate this to the timing of shredder colonization of the exposed litter. Field experiment.

II To record the species composition, abundance and species-specific growth periods within the shredder functional group in an annual perspective in small oligotrophic lakes. To conceptually link the estimated shredding capacity to changes in the availability of different detritus types. Field inventory.

III To test if shredder activity increases DOC release and bacterial production in the water column. To quantify the relative allocation among carbon products from decomposition with and without shredder activity. Laboratory experiment.

IV To demonstrate the influence of autumnal input of coarse detritus on benthic invertebrate carbon utilization – indicated by stable isotopes at community, functional group and species level. To compare stable isotope signals in common benthic invertebrates with predictions of carbon sources and trophic level. Field sampling.

V To evaluate the effects of detritus properties and shredder activity on the temporal product outcome from decomposition of two macrophytes under natural winter and spring conditions. Parallel field and laboratory experiments.

13

Methods General approach

My objective throughout this thesis has been to work as close to natural conditions as possible, even though experiments were conducted at different levels of complexity. The combination of field studies (papers I, II, IV and V) and laboratory experiments (papers III and V) offered both the sophistication of natural conditions and the control over environmental and experimental factors under artificial circumstances. The laboratory studies provided more straightforward interpretable results, but also manipulation artefacts and therefore results not necessarily transferable to natural conditions. The field sampling in three lakes over more than one year (paper II) made some of the conclusions more generally applicable. Both pilot studies and the sequence of main studies provided information and experiences that were employed in subsequent studies. In addition, I took into account other relevant methodological experience from the extensive literature on decomposition of coarse detritus in streams (e.g. Boulton and Boon, 1991).

Furthermore, the aim was to conduct the studies in non-extreme habitats by avoiding pollution, acidification or lakes with atypical physical-chemical conditions. I therefore endeavoured to choose relatively undisturbed lakes, being representative for the range of normal variation in this geographical region. I worked only in very shallow areas of littoral zones, with a water depth less than 1m, where CPOM aggregations were common (pilot study) and where shredding trichopteran larvae show the most dense populations (Czachorowski, 1993). Further, I used the naturally occurring species of shredders and detritus types, combing them in earlier recorded proportions in all my experiments (papers I, III and V). Lake water with natural composition of microorganisms was used in the laboratory experiments. Temporal aspects

In designing my experiments and sampling, I paid very particular attention to the temporal aspect, since pronounced seasonal patterns occur both among coarse detritus sources and detritivores in freshwater habitats at these latitudes. This is due to the pulsed litter fall in temperate areas, with about 75% of deciduous forest litter falling in autumn (Campbell et al., 1992). Additional factors influence the temporal pattern of decomposition of leaf litter, for example chemical defence compounds, nutrient content, length of conditioning period and proportion of structural compounds (Petersen and Cummins 1974; Webster and Benfield, 1986; Kok et al., 1992). A close link between the riparian vegetation and the species composition of the shredder guild has been earlier highlighted in earlier stream studies (Hynes, 1975; Cummins, 1986; Friberg, 1997). Both the unequal species composition among summer and winter shredders (Cummins et al., 1989), and the fact that certain shredder taxa (crustaceans) have a completely aquatic life cycle (Dangles and Guérold, 1998), may influence the seasonal total shredding capacity in the system. Based on this previous work, I started both the field and laboratory experiments synchronously with natural input of coarse detritus in autumn (papers I, III and V) and adjusted the temporal sampling with respect to the time of the main leaf fall (paper IV).

14

Study area All fieldwork was carried out in the catchment of the River Emån in southeast

Sweden (Figure 2). In the sampling area, the catchment is dominated by coniferous forests, while the riparian vegetation of the lakes is a mixture of deciduous trees and bushes, mainly birch Betula pendula and oak Quercus robur. Sparse populations of sedges (Carex spp.), reed (Phragmites australis) and rush (Schoenoplectus lacustris) form the macrophyte community in most lakes (see papers I, II and IV for more detailed information). The field inventory was conducted in three oligo-mesotrophic lakes (Lake Narrveten, Lake Lilla Granesjön and Lake Välen), chosen to be representative for this region after a pilot study including 18 lakes on different tributaries of the River Emån. The experimental work was based at Lake Välen, selected because of known water chemistry, no acidification history and easily accessible littoral zones.

������

������������

�

Figure 2. Location of the River Emån and the sampled lakes. Principal methods and modifications Detritus sources

All litter used in the experiments was collected in littoral or riparian zones of Lake Välen close to natural senescence to ensure the same types naturally served to the system. However, in all experiments pre-dried leaf litter was used to reduce variability between replicates and to allow the correct determination of weight loss (papers I, III and V). A relatively low drying temperature (50°C) and long time period (48 h) were used to reduce modification of leaf tissue. Pre-drying of leaf litter may increase the amount of DOM released (Chergui and Pattée, 1992), but it does not influence colonizing invertebrate fauna (Gessner and Dobson, 1993). The only exception to this was the leaves of Nymphaea alba L., which were exposed in litterbags in a fresh state (paper V), because of the considerable effects of drying on the very soft structure could be foreseen.

15

Litterbag technique The choice of mesh size in litterbags is a trade-off between losses of material and

access for shredders, but it also affects the microclimate for fungi and bacteria (Boulton and Boon, 1991; D’Angelo and Webster, 1992; Bedford, 2004). The mesh dimensions of litterbags chosen differ a great deal in published studies and it is often not clearly defined what taxa were meant to have access to the litter. This urges a stricter investigation of the species composition of the shredder guild before applying the litterbag technique to evaluate decomposition rates. Pilot sampling revealed that several species of case-bearing caddis larvae are common shredders in the studied lakes. In the field experiments (papers I and V) I therefore used specially designed litterbags to ensure that detritus was accessible to the shredder species present. The mesh size in the top layer of the litterbags was 12 mm and in the bottom layer 6 mm. To reduce the loss of colonizing invertebrates during lifting of the litterbags, I used a specially constructed grab sampler to place underneath and a lid to cover the litterbag (Figure 3). Both grab and lid were made of 0.5 mm metal net.

Figure 3. The grab sampler used during lifting of the litterbags. Fine particulate detritus

Irrespective of the mesh size used in litterbag experiments to allow shredder entrance, FPOM (fine particulate organic matter, < 1mm) will be lost. Therefore, FPOM production must be estimated from laboratory studies (paper III). In addition to the conventional detritus fractions (CPOM = Coarse Particulate Organic Matter, >1mm; FPOM = Fine Particulate Organic Matter, 0.45 µm – 1mm; DOM = Dissolved Organic Matter, <0.45 µm) (Anderson and Sedell, 1979), I used fCPOM for processed coarse detritus. The fCPOM fraction represents the fragmented coarse organic matter often less than 3 mm in particle size, but over 1 mm (paper II). In paper III, the fCPOM and FPOM were sampled together from a subsample of particles in suspension collected on a Whatman GF/C filter. Species identification

Separating species of specific trichopteran larvae is difficult, especially at the early stages. We carried out a hatching programme for the trichopterans to confirm the identity of larvae by identifying adults (paper II). Through this programme we learned

16

to identify larvae of all species and most instars. For Limnephilus flavicornis (Fabricius), Limnephilus marmoratus (Curtis) and Limnephilus rhombicus (L.) only larvae of the 4th and 5th instars could be differentiated. In the laboratory studies, to avoid damages on living larvae before starting the experiments, I did not discriminate between the close species L. flavicornis and L. marmoratus (papers I and V). Microbial methodology

I applied standard microbial methods in the laboratory experiment, with details of procedures given in paper III. Bacterial abundance was measured by microscopic counting of cells on polycarbonate filters after fixation of water samples with formaldehyde and staining with DAPI (4’6-diamidino-2-phenylindole) (Porter and Feig, 1980). Bacterial production was measured using the leucine incorporation technique proposed by Smith and Azam (1992). The principle used in this method is that 3H-labeled leucine is incorporated in bacterial protein synthesis during incubation. Bacterial carbon production (µg C l-1 h-1) was calculated using the conversion factors of Simon and Azam (1989). The natural stable isotope approach

We used natural stable isotopes to estimate the carbon source assimilated by benthic invertebrates (paper IV). Analysis of carbon stable isotopes is frequently carried out to discriminate between carbon originating from different sources (Peterson and Fry, 1987; Post, 2002). The basis is that physical and biological turnover of elements affects the proportions of light and heavy isotopes. Both photosynthesis and diffusion in water reduce the carbon isotope ratio (13C/12C) compared to atmospheric CO2. Consequently, the lowest ratio is found among pelagic primary producers and less reduced ratios in terrestrial primary production. Because both enzymatic metabolism and excretion discriminate against the heavy nitrogen isotope, the nitrogen ratio (15N/14N) will increase with trophic level in the food chain. The analyses of the stable isotope composition of C and N are time-integrated representations of the food sources assimilated by consumers (Lajtha and Michener, 1995; Vander Zanden et al., 1999). Standard fractionation with trophic level has been shown to be less than 1‰ for carbon and about 3.4‰ for nitrogen (Meili et al., 1993; Cabana and Rasmussen, 1994). Isotope ratios (13C/12C and 15N/14N) are expressed as delta values (δ), defined as the per mil (‰) deviation from official isotope standards (Vienna Peedee belemnite limestone and atmospheric nitrogen). Results and Discussion

This thesis shows that the annual decomposition cycle of coarse detritus in small oligotrophic lakes depends on specific combinations of detritus types and of shredder species. The weight loss from coarse detritus showed a distinctive seasonal pattern temporally linked to shredder appearance and growth (papers I and II). Therefore, I concluded that one important mechanism for initial decomposition of coarse detritus in the studied lakes is shredding. This conclusion encouraged me to further examine the different temporal roles among the shredder species (papers II and IV). Closer

17

investigation of this group allowed me then to give a modified picture of the individual species contribution to ecosystem function than that derived from patterns of abundances or biomasses. The identified importance of shredders for decomposition also inspired me to investigate the consequences of shredder activity for carbon allocation (paper III). Hence, in the laboratory I discovered how shredder activity influenced the proportions of the main products from initial decomposition, DOM and FPOM. From the comparison of different types of macrophyte litter, I concluded that these intermediate products become available for other consumers in different proportions and temporal modes (paper V). Seasonality of CPOM turnover (papers I, II and V)

The results show that leaf litter of alder (Alnus glutinosa), birch (Betula pendula) and oak (Quercus robur) is relatively rapidly processed (within 3-6 months after input) in littoral zones of lakes in this area (papers I and II). More recalcitrant litter types such as other leaves (mainly Populus tremula and Myrica gale) and emergent macrophytes (Phragmites australis and Carex spp.) were processed later in spring and during summer (papers II and V). When exposed experimentally, the soft litter from Nymphaea alba was rapidly processed, while litter from Ph. australis did not begin to lose weight due to shredding until after 5 months’ exposure (paper V). The agreement between weight loss in experiments and changes in the standing stock of coarse detritus found during the annual sampling strengthens the conclusion of different turnover regimes among litter types in lakes (Figure 4).

0

10

20

30

40

50

60

70

OctNov Dec Ja

nFeb Mar Apr

May Jun Ju

lAug Sep Oct

%

Alder Birch OakEmergent macrophytes Other leaves Litterbag BirchLitterbag Oak Littterbag Reed

Figure 4. Seasonal comparison of weight loss rates in litterbags combined with changes in litter standing stock. The y-axis shows relative amounts of coarse detritus from sampling of littoral standing stock (paper II) (to increase clarity fragmented CPOM and needle litter are not shown) and the percentage (values divided by 2 for scale fitting) of the remaining dry weight of experimentally exposed litter from papers I and V.

18

The main input of detritus occurs in the autumn, but differences in resistance to

decomposition among the species of plants means that the processing of coarse detritus to continues throughout the year (paper II). The fact that differences in recalcitrance among detritus types leads to a certain temporal sequence of utilization has been documented in streams (Grubbs and Cummins, 1996; Haapala et al. 2001). Also in lakes, this successive decomposition pattern appears to exist and the majority of the leaf litter resource is recycled within the annual perspective. Therefore, I conclude that in small oligotrophic lakes coarse detritus is a highly attractive resource, even if other food sources, such as FPOM-accumulations or benthic and pelagic algae, can be supplementary in lake littoral zones. Links to shredder activity

The weight loss pattern of leaf litter was closely linked to shredder presence in litterbags (paper I), of which larvae of Glyphaotaelius pellucidus and Limnephilus marmoratus (Insecta, Trichoptera) were dominant. Furthermore, the results from paper II indicate a strong temporal link between the disappearance of coarse detritus and trichopteran shredder growth throughout the year (Figure 5). A. aquaticus avoided littoral zones during mid-winter and peaked in biomass per square meter during late summer and early autumn before main decomposition period (papers I and II). For a majority of winter trichopteran shredders, the start of their lives was tied to the main input of detritus during the autumnal leaf fall. Winter-growing shredders have been shown to maintain a high growth rate even at temperatures as low as +1°C (Short and Ward, 1980; Irons et al., 1994; paper II). Other species of trichopteran shredders have an optimal growth temperature that is considerably higher, as Sericostoma vittatum at 13.7-16.7°C, (Gonzáles and Graça, 2003). The winter-growing species were replaced by other shredder species during spring and summer. The identified growth patterns were consistent both between years and lakes (paper II). The substantial acceleration of weight loss rate for reed in litterbags with coarse meshes registered in April-May (paper V) coincides with a shift in species composition within the shredder functional group. During this time of year other species do appear or begin fast growth, Anabolia nervosa, Halesus radiatus and Limnephilus borealis (paper II). Seasonal succession in growth patterns among shredders and life cycles keyed to the predictable timing of seasonal input of leaves exist in streams (Cummins et al. 1989; Grubbs and Cummins 1996; Haapala et al., 2001). I suggest that this is also the case for the identified lake-specific set of shredder species.

I conclude that the recognized lentic shredder species are capable of processing the coarse detritus resource in the studied lakes, including the most recalcitrant fractions. I suggest that summer-growing shredders in lakes depend on the most resistant litter types, like emergent macrophytes (papers II and V). The importance of litter aggregations probably increases after winter/spring, as easy-degradable leaf litter is a diminishing food supply. Hence, recalcitrant litter can be resource islands also in lake littorals when the spring resource bottleneck is reached, in the same way as suggested for streams (Haapala et al., 2001; Schofield et al., 2001).

19

Oct-00

Nov-00

Dec-00

Jan-0

1

Feb-01

Mar-01

Apr-01

May-01

Jun-0

1

Jul-0

1

Aug-01

Sep-01

AlderOak

BirchOther leaves

Emergent macrophytes

0

10

20

30

40

50%

a)

Aug-00

Sep-00

Oct-00

Nov-00

Dec-00

Jan-0

1

Feb-01

Mar-01

Apr-01

May-01

Jun-0

1

Jul-0

1

Aug-01 N

p Gp Lf Lr Lm

Hr Lb An Ln

0.00

0.01

0.02

0.03

0.04

0.05

0.06

0.07

0.08(g)

b) Figure 5. a) Seasonal changes in proportions of the most common coarse litter types in coarse detritus standing stock. b) Individual dry weight over time for larvae of the nine species of trichopterans showing the successive pattern of growth over the year. Based on data from Lake Välen in paper II. Comparisons of weight loss rates

Literature comparisons of weight loss rates for coarse detritus show that leaf litter appears to decompose relatively quickly in Lake Välen (Table 1). Peterson and Cummins (1974) suggested that half-life time (t50) could be used to sort leaf litter into

20

three categories: fast (t50 < 46 days), medium (t50 = 46-138 days) and slow (t50 > 138 days) with respect to turnover rate. In Lake Välen both birch and oak litter can be categorized as medium decomposable under favourable conditions (paper I), whereas oak litter in other studies is sorted in the slow category. This difference is also supported by the observation that oak litter completely disappeared from the CPOM standing stock in less than half a year in all three studied lakes (paper II).

While the turnover rate for leaves from N. alba in Lake Välen seems to be in accordance with published data, the decomposition pattern for reed leaves found in this study was very slow compared to that recorded in some recent studies (Sabetta et al., 2000; van Dokkum et al., 2002; Mancinelli et al., 2002). Besides the difference in time of year between the experiments, the strong influence from gammarids on decomposition rate found in those studies may contribute to the explanation for the differences. Gammarids are not found in Lake Välen. Thus, shredder fauna compositions may well be crucial for decomposition rate of at least reed.

Table 1. Half-life for leaf litter, calculated as the time for 50% weight loss, in this thesis compared to other published data. * denotes values calculated from other kinds of data. Litter type Experimental conditions Half-

life (days)

Reference

Betula pendula Litter bag, 10 mm, whole year 138* Henrikson and Oscarson, 1996

Betula verrucosa Litter bag, 2.5 mm, poor benthic fauna 456* Fjellheim and Raddum, 1988 Betula pubescens Litterbag, 2 mm, autumn 53* Kok and van der Velde, 1994 Betula pendula Litterbag, 12 mm, winter 94/95 and

95/96 89 and 130

Paper I

Quercus robur Litter bag, 12.5 mm, whole year 268* Oertli, 1993 Quercus robur Litterbag, 12 mm, winter 94/95 and

95/96 108 and 170

Paper I

Ph. australis Litterbag, 5 mm, winter 56 Van Dokkum et al., 2002 Ph. australis Litterbag, 0.01 mm, winter 92 Van Dokkum et al., 2002 Ph. australis Litterbag, 5 mm, winter 570* Hietz, 1992 Ph. australis Litterbag, 0.07 mm, winter 645* Hietz, 1992 Ph. australis Litterbag, 12 mm, winter 178 Paper V Ph. australis Litterbag, 1 mm, winter > 225 Paper V N. alba Litterbag, 2 mm, autumn 35* Kok and van der Velde, 1994 N. ambla Litterbag, 6 mm 14* Goncalves et al., 2004 N. lutea Litterbag, 0.27 and 0.78 mm, autumn 32-35* Brock et al., 1985 N. alba Litterbag, 12 mm, winter 37 Paper V N. alba Litterbag, 1 mm, winter 38 Paper V The lake shredder species and their specific roles as decomposers (papers I, II and IV)

The results in this thesis distinguish the shredder species that are most important for the processing of coarse detritus in small oligotrophic lakes in southeast Sweden (Table 2). The prominent feature of these findings is the strong dominance of trichopteran larvae, mostly lake-specific species (paper II). Compared to streams, the absence of gammarids, as well as plecopteran, ephemeropteran and dipteran shredders make the identified shredder guild very limited referring to phylogeny (e.g. Cummins et al., 1989; Dobson, 1994; Giller and Malmqvist, 1998). In order to functionally

21

group the recorded species, we used literature data in combination with our own results and observations (papers I, II and IV). In this procedure we excluded several identified shredder species because of consistently very low abundances: larvae of Lepidostoma hirtum, Limnephilus binotatum, Limnephilus lunatus, Limnephilus stigma, Notidobia ciliaris, Stenophylax permistus and Nemoura cinerea (Plecoptera) (paper II). Analysis of stable isotopes supported the functional role of the winter-active shredders by showing that littoral detritus was main assimilated carbon source (paper IV). Among the nine most frequent trichopteran larvae there was no variation between information of food choice – all could be classified as shredders living of tree leaf or aquatic macrophyte litter. For Asellus aquaticus the categorization was more complicated, the results showed that this species uses different food sources at different times (paper IV).

Some species of the genus Leptophlebia (Ephemeroptera) have occationally been suggested to feed on leaf litter (Brittain 1980; Cummins et al., 1989; Monakov, 2003), but the shredder role of L. marginata L. and L. vespertina L. was neither supported by this study (papers I and IV) nor by laboratory experiments conducted by Bjelke (unpublished). One explanation for such confusion of functional feeding group classification for mayflies is given by Dieterich et al. (1997). They noticed that during laboratory experiments mayfly collectors shredded leaves in order to enhance microbial growth on smaller particles and thereby obtain useful food items (“gardening behavior”). Table 2. The identified lake shredder species in SE Sweden. Support from results in this thesis to functional feeding group (FFG) classification and food preferences found in the literature. Redrawn from papers I, II and IV, where literature references are specified. Species FFG

Food preference This study

Crustacea Isopoda Asellus aquaticus

shredderI, IV/scraperI, IV leavesI, algae IV, fungi Papers I and IV

Insecta Ephemeroptera Leptophlebia marginata shredder/scraper IV detritusIV, periphyton IV Paper IV Leptophlebia vespertina

shredder/scraper IV detritusIV, periphyton IV Paper IV

Insecta Trichoptera Anabolia nervosa shredder plants, animals Glyphotaelius pellucidus shredderI, IV LeavesI, IV, algae, animals IV Papers I and

IV Halesus radiatus shredder plants, animals Limnephilus borealis shredder Limnephilus flavicornis shredder I, III, V Papers I, III

and V Limnephilus marmoratus shredder I, III, IV, V leaves I, III, IV, V, fanerogams,

algae, animals Papers I, III, IV and V

Limnephilus nigriceps shredder Limnephilus rhombicus shredder leaves, algae Nemotaulius punctatolineatus shredder IV leaves IV, animals IV Paper IV

22

Realized food niche Many shredder species have been found to be opportunistic in their food choices

(Friberg and Jacobsen, 1994; Mihuc and Mihuc, 1995). Therefore, lake-dwelling species were also expected to feed on the optimal resource (the most energy- and nutrient-rich food items available at the moment) and possibly change food base over time under natural conditions. In paper IV it was shown that some of the winter shredder species differ in their sources of carbon over time, indicated by shift in stable isotope ratio. A. aquaticus utilized different carbon sources, with mainly littoral detritus carbon during autumn and winter, shifting to a greater portion of algal carbon in spring.

Ontogenetic food shifts and change in consumption capacity during growth are common among benthic macroinvertebrates (Chapman and Demory, 1963; Gonzáles and Graça, 2003; Bjelke and Herrmann, 2005), which may be important for the leaf litter turnover pattern. Additionally, late instars of trichopteran larvae have been shown to accumulate triglyceride reserves for metamorphosis and reproduction (Cargill et al., 1985). The results of the analysis of stable isotopes of nitrogen suggest that, for both N. punctatolineatus and G. pellucidus, the demands for higher food quality in the late larval stage are met by shifting to a more animal-based diet by both (paper IV). This was not the case for the winter shredders of the genus Limnephilus. Thus, also among the trichopteran shredders within the same family (Limnephilidae) the food choice differs temporally.

The choice of food for the specific species may also depend on many other factors, such as environmental conditions, interspecific competition and predation pressure (Hargeby, 1990; Reutz et al., 2002; Jones and Waldron, 2003). The reverse abundance patterns between caddis larvae and A. aquaticus during the two subsequent years may indicate a one-way competitive relationship between the two taxa during spring (paper I). When the trichopteran shredders were not prevented from exploiting the leaf litter, they were capable of emptying that resource. However, when trichopteran abundance was low (probably due to freezing), the remaining leaf litter resource was passed on to A. aquaticus in spring. Other factors than food availability are likely to make A. aquaticus leave this substrate during the mid-winter period, for example intolerance to low temperatures. A. aquaticus does not grow at temperatures lower than +3˚C and has been suggested to migrate to deeper water when ice formation occurs in the littoral zone (Berglund, 1968; Andersson, 1969). Therefore, the role of A. aquaticus in the initial transforming of coarse detritus in littoral zones is probably less important than previously thought (Prus, 1981; Andersson, 1985; Henrikson and Oscarsson, 1996). Shredding capacity at ecosystem level

Often some species tend to dominate with respect to population biomass within a system (Schwartz et al., 2000). This has implications for further conclusions regarding species-specific importance for ecosystem functions. In lakes in SE Sweden, A. aquaticus is strongly dominant among the shredders, both numerically and in terms of total biomass in the littoral zone, whereas the opposite seems to be the case for the trichopteran shredders showing much lower abundances (paper II). To come closer to the likely natural contribution from different species to the ecosystem function of decomposition in the studied lakes, we multiplied the recorded abundance data

23

(biomass/m2) with shredding capacity (leaf litter consumed per gram animal biomass), published by Monakov (2003). In this, we reduced the weight of A. aquaticus by a factor of 10 when presenting relative shredding capacity per m2 (Figure 6 in paper II). This procedure revealed that during winter (November – April) A. aquaticus contributed relatively little to the estimated total shredding capacity in all three lakes – a temporal abundance pattern corresponding to the earlier observed absence of A. aquaticus on experimentally exposed leaf litter in the littoral zone during winter (paper I). During the rest of the year, A. aquaticus dominated the species-specific shredding capacity in both Lake Lilla Granesjön and Lake Narrveten, even though the lower consumption capacity was taken into account. Thus, species composition of shredders, their relative abundance and their seasonal growth periods represent factors potentially crucial for decomposition rates. A modified view of species-specific shredder function

Using the above observations of actual shredding function among the involved invertebrate species and the species capacity at ecosystem level produces an even more refined picture of the connection between litter disappearance and shredder growth (Figure 6). Thus, at the same time as the total shredding capacity peaks, the fastest disappearance of CPOM is recorded. Further, winter growing species utilize alder, birch and oak litter, whereas the summer shredder species depend on the more recalcitrant CPOM fractions. There seems to exist a surprisingly fine-scaled temporal niche separation among trichopteran shredder life cycles, which may have arisen from long adaptation to the predictive seasonal changes of availability of the most important food resources.

0

10

20

30

40

50

60

70

Oct-00

Nov-00

Dec-00

Jan-0

1

Feb-01

Mar-01

Apr-01

May-01

Jun-0

1Ju

l-01

Aug-01

Sep-01

%

00.10.20.30.40.50.60.70.80.91

g/m

2

Aa

Lm Np

Aa Aa Np

Lm

LnLnLbAn

LmLb

LmLmLm

Lm

Lm

GpGpGp

Gp

Gp

Gp

Np Np

Np

Figure 6. Tentative presentation of species-specific contribution to total shredding capacity (biomass, g/m2) conceptually linked to the decrease of coarse detritus (relative proportions, %, see legend in figure 4). Data from Lake Välen (paper II), with modifications based on Monakov, 2003 and results from papers I and IV (Aa leaving litter substrate during winter and eat as a rough estimate 50% algae in spring, Np is 100% carnivorous from February, Gp is 50% carnivorous from February). The most dominant shredder species are marked by a two-letter abbreviation: Aa Asellus aquaticus, Np Nemotaulius punctatolineatus, Gp Glyphotaelius pellucidus, Lm Limnephilus marmoratus, Lb Limnephilus borealis, An Anabolia nervosa and Ln Limnephilus nigriceps.

24

The temporally separated set of shredder species can influence ecosystem functioning by their combined ability to recycle each detritus type, i.e. accomplish a more complete ecosystem function. However, it can be expected that species differ in importance for maintenance of the decomposition function and that some species play “key roles” (Dangles and Guérold, 2001). Alteration of species composition and abundances in the shredder community in water may be one of the primary factors influencing decomposition rate. Benthic functional groups, being rather species-poor, have been proposed to be particularly useful for further studies of the linkage between ecosystem function and biodiversity (Palmer et al, 1997). I emphasize that the shredder guild in the type of lakes investigated in this thesis to is suitable for such studies because of its close connection to turnover of coarse detritus. Shredders vs microorganisms

Excluding shredders, only 29% of the initial leaf carbon was converted to other carbon fractions during the laboratory experiment, compared to almost 80% with shredders (paper III). Consequently, this study shows that shredders have the potential to consume leaf litter resources before microbial decomposition influences litter weight substantially. Although aquatic fungi live mainly on decomposing litter and indeed are fully capable of processing their substrate, the invertebrate community structure may be crucial for fungal significance to litter processing (Graca et al., 2001). Furthermore, the difference in detritus turnover rate between coarse- and fine-meshed litterbags found by Gessner et al. (1998) and Robinson and Gessner (2003) is a strong indication that fungi-mediated decomposition is inferior in terms of turnover rate. Thus, the quantitative importance of microorganisms (fungi and/or bacteria) for leaf litter turnover is here suggested to be directly dependent on the density of shredders in lake littoral zones. Products from decomposition (papers III and V)

In two of the papers the proportions of intermediate decomposition products from leaf and macrophyte detritus were estimated. The first experiment (paper III) aimed to analyse most fractions of the carbon budget in the microcosms. The results showed that the major products from coarse detritus decomposition are DOM and FPOM, the former product being almost independent of shredder activity and the latter practically entirely shredder induced (paper III). In paper V simplified methods (differences in weight loss of incubated litter and absorbance) were used to follow the temporal formation of these dominating products. Dissolved fractions

Besides the passive initial DOM release, we registered very little increase in DOM resulting from shredder activity; we therefore concluded that such shredder-induced release is of minor importance for the total carbon flow from leaf litter (paper III). Although the shredder-derived DOM constituted a minor fraction of the total carbon budget, the bacterial production in the water was several times higher with shredders than without (paper III). In contrast to the initially rapid release of DOM from tree leaf litter and litter from Nymphaea alba (papers III and V), the release of dissolved

25

compounds from submerged reed (Phragmites australis) litter was continuous throughout the whole experiment (paper V).

Dissolved carbon and nutrients released from leaf litter seem to be highly bioavailable (Sun et al., 1997). During a leaf fall in autumn, the rich initial release of DOM might provide an important supply of accessible carbon for bacteria in littoral zones. The ecosystem significance of the two examples of delayed DOM release above do not seem to be quantitatively important, but may contribute qualitatively. That is, if the existing DOM pool during winter is highly recalcitrant, a continuous release of fresh DOM may enhance bacterial or fungi production. However, bacterial growth in water-column may be temperature-limited during winter in lakes, at least below +7˚C (Felip et al., 1996).

After 126 days of incubation, the dry mass of leaf litter decreased by 80% in the presence of shredders. On average, 55% of initial leaf dry weight ended up as fine particulate organic matter (Figure 7). Without shredders, only 29% of the initial leaf carbon was converted to other carbon fractions and leaf litter was apparently unaffected at the end of the experiment (Figure 8). These results suggest that Limnephilus flavicornis/marmoratus have a strong impact on the transformation rate of leaves to finer particulate organic matter, without enhancing the mineralization per se. As aquatic insect assimilation efficiency for detritus is low, 6-35%, (Benke, 1984; Petersen et. al., 1989; Oertli and Dall, 1993), most of the organic matter is, after shredding, left for other consumers, microorganisms and FPOM collectors.

DOC

23.7

0.44

54.1 24.4

Leaf litter

76.5

0

3.1

20.4

Bacterial production

in water column

FPOC

Shredder production

Leaf rest Figure 7. The carbon allocation from leaf litter at the end of the laboratory experiment as a percentage of the initial amount. Grey boxes refer to microcosms with and white boxes to microcosms without shredders. The DOC compartment includes the initial leakage, most of it available for bacterial production (indicated by the dotted arrow). Bacterial and shredder production figures are integrated over time and include respired carbon. Based on paper III.

26

Figure 8. Leaf litter from the two treatments at the end of experiment (paper III), with shredders (left) and without shredders (right). Particulate fractions

Particulate products, fCPOM and FPOM, are the major result of shredder processing of leaf litter (paper III). This fine particulate detritus that is produced is expected to be a coveted resource for other consumers, collectors and microbes (Dieterich et al., 1997; Graça, 2001). The FPOM fractions at least are transportable to other compartments of the lake due to resuspension (MacIntyre and Melack, 1995). The observed changes in carbon signal in surface sediment showing more littoral origin during winter, revealed by stable isotope analysis, may have resulted from such a transport of littoral FPOM (paper IV). In general, the processed detritus is more refractory than leaf litter and is also transported further than intact leaves, contributing to the particulate half of total carbon transport to the oceans (Webster et al., 1999).

There are very few studies on the further fate of fine particulate carbon from

shredder activity within lake ecosystems (Heard and Richardson, 1995; Wallace and Webster, 1996). However, Dieterich et al. (1997) found a close shredder-collector connection – both in feeding tests and by comparing temporal phenology between the two groups. This is contrary to the finding by Usio et al. (2001), who reported that young amphipods did not grow better on FPOM from shredders than on CPOM. Nevertheless, I assume that some collectors at least are most probably supported by shredder activity. The high ratio of stable carbon isotopes, close to littoral coarse detritus, observed in oligochaetas could be one such example (paper IV).

The invertebrate biomass produced based on coarse detritus (e.g. shredders and

collectors) represent another route of the further littoral carbon flow, being a food resource for various predators, including predatory invertebrates. Paper IV reveals littoral carbon dependence for Sialis lutaria, known to feed mainly on oligochaetas and chironomides.

27

Conclusions and perspectives The results of this thesis support the hypothesis that coarse detritus is an important

resource in littoral zones of small oligotrophic lakes. This carbon source is successively processed by microorganisms and invertebrates in the littoral zone over the whole year. Different combinations of detritus types and invertebrate processor species are suggested to influence the further accessibility of intermediate decomposition products. More specifically this thesis:

- shows that coarse detritus is an attractive food source also in lake littorals (as in smaller streams) and that this resource is processed according to an annual sequential pattern,

- emphasizes the key role of certain trichopteran shredder species for litter processing in lakes in this region, by revealing the temporally finely resolved annual succession pattern among the nine species in the studied lakes,

- amplifies the importance of a quite broad range of food sources for the isopod Asellus aquaticus, by demonstrating a food shift to algae in spring or opportunistic feeding on leaf litter if available,

- suggests that the decomposition of leaf litter results principally in two products, DOM from passive leakage and FPOM from active leaf litter processing by shredders,

- stresses that such products become available for the rest of the ecosystem in different proportions and at different times of the year depending on the combination of litter type and species composition of the functional group of shredders and

- proposes an applicability of the decomposition rate of coarse detritus as an assessment tool for integrating disturbances onto ecosystem functions also in small oligotrophic lakes, respecting the unique lake characteristics.

Perspectives of threats and protection

A wide range of disturbances can affect freshwater ecosystems. Net heterotrophic systems are specifically sensitive to nutrient addition, CO2 increase or changes in land use (Palmer et al., 2000; Riley and Jefferies, 2004). Loss or change of subsidized resources might dramatically alter the conditions for many species in recipient habitats of otherwise low productivity (France and Peters, 1995; Huxel et al., 2004). Mechanisms can be of several types, declining diversity in plant resources or less influx of terrestrial invertebrate prey, as identified by Palmer et al. (2000) and Baxter et al. (2005). In all smaller aquatic systems the edge effect from terrestrial production is substantial, but most studies are conducted in streams and data from lakes are scarce. Deforestation or other human disturbances of the vegetation or the hydrology in drainage area can possibly influence the distribution of both dissolved and particulate detritus (France et al., 1996). Disturbance of littoral detritus input or processing may therefore potentially result effects in other parts of the lake ecosystem.

Further, every specific threat to benthic fauna, such as toxic pollution, acidification or turbidity (Herrmann et al., 1993; Gage et al., 2004), may alter the key function of

28

coarse detritus processing. Loss of shredder population due to insecticide contamination has been shown to decrease CPOM decomposition (Cuppen et al., 1995). Nutrient addition most likely changes the whole system from heterotrophic to more autotrophic, but may in the short run contribute to increased shredder feeding (Robinson and Gessner, 2000). Wherever larvae of flying insects, e.g. trichopterans, are important for shredder function, changes in the terrestrial habitat have a twofold effect – both altered food input and changed reproduction conditions for the adults. Alteration of species composition and abundances in the shredder community is probably one of the primary factors influencing the decomposition rate of coarse detritus in water. Protection of riparian zones with respect to vegetation structure and species composition, and to hydrology seems crucial to sustaining functions in small oligotrophic lakes. Research perspectives

The results of this thesis generate new questions, and future studies are necessary to understand the further flow of carbon in littoral zones in small oligotrophic lakes. It is clear that increased knowledge of mechanisms influencing decomposition processes is fundamental to predicting the effects of disturbance on the carbon cycling in littoral zones. In my view, there are a number of interesting future research projects:

- Evaluating the ecological significance of the opened “time windows” of carbon availability, i.e. the accelerated carbon flow due to shredder activity. Are the intermediate products such as shredder biomass and FPOM vital for the ecosystem during the period in question?

- More detailed studies of FPOM detritus as a resource for other littoral consumers, including the dynamics of the relation between microorganisms and invertebrates (collectors).

- Prediction of effects of gradually reduced abundance or biodiversity among shredder guilds in different regions. This will most likely identify several important shredder species as the key-species.

- Disturbance of coarse detritus processing as a result of climate change. Different effects depending on geographical location through various scenarios: drought, no ice, more winter run-off, more storms etc. Identify risk situations both on land and in the water.

29

Literature cited Albariño R. J. and Balseiro E. G. 1998. Larval Size and Leaf Conditioning in the

breakdown of Nothofagus pumilo Leaves by Klapopteryx kuscheli (Insecta, Plecoptera) in a South Andean Stream. International Review of Hydrobiology 83: 397-404.

Allard M. and Moreau G. 1986. Leaf decomposition in an experimentally acidified stream channel. Hydrobiologia 139: 109-117.

Anderson N. H. and Sedell J. R. 1979. Detritus processing by macroinvertebrates in stream ecosystems. Annual Review of Entomology 24: 351-377.

Anderson W. B. and Polis G. A. 2004. Allochthonous Nutrient and Food Inputs: Consequences for Temporal Stability. In: Food Webs at the Landscape Level, G. A. Polis, M. E. Power, and G. R. Huxel (eds). The University of Chicago Press, Chicago, pp. 82-95.

Andersson E. 1969. Life-cycle and growth of Asellus aquaticus (L.). Institute of Freshwater Research, Drottningholm, Sweden. 49: 5-26.

Andersson G. 1985. Decomposition of alder leaves in acid waters. Ecological Bulletins 37: 293-299.

Anesio A. M., Tranvik L. J. and Graneli W. 1999. Production of inorganic carbon from aquatic macrophytes by solar radiation. Ecology 80: 1852-1859.

Azam F., Fenchel T., Field J. G., Grey J. S., Meyer-Reil L. A. and Thingstad F. 1983. The ecological role of water-column microbes in the sea. Marine Ecology - Progress Series 10: 257-263.

Bärlocher F. 1992. Community Organization. In: F. Bärlocher. The Ecology of Aquatic Hyphomycetes. Springer-Verlag, Berlin.

Baxter C. V., Fausch K. D. and Saunders W. C. 2005. Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshwater Biology 50: 201-220.

Bedford A. P. 2004. A modified litter bag design for use in lentic habitats. Hydrobiologia 529: 187-193.

Benke A. C. 1984. Secondary production of aquatic insects. In: The ecology of aquatic insects. V. H. Resh and D. M. Rosenberg (eds). Praeger, New York, pp. 289-322.

Berglund T. 1968. The influence of predation by brown trout on Asellus in a pond. Institute of Freshwater Research, Drottningholm, Sweden. 48: 77-101.

Bergström A-K., Jansson M., Drakare S. and Blomqvist P. 2003. Occurrence of mixotrophic flagellates in relation to bacterioplankton production, light regime and availability of inorganic nutrients in unproductive lakes with differing humic contents. Freshwater Biology 48: 868-877.

Bjelke U. 2005. Species richness and functional diversity among lake-living shredders: links to decomposition in littoral zones. Dissertation thesis, University of Kalmar.

Bjelke U. and Herrmann J. 2005. Processing of two detritus types by lake-dwelling shredders: species-specific impacts and effects of species richness. Journal of Animal Ecology, 74: 92-98.

Bohman I. M., Hansson M. and Herrmann J. 2000. Horizontal diurnal migration (HDM) of zooplankton- a littoral pelagic coupling? Verh.Internat.Verein.Limnol. 27: 2870-2874.

Boulton A. J. and Boon P. I. 1991. A review of methodology used to measure leaf litter decomposition in lotic environments: Time to turn over an old leaf? Australian Journal of Marine and Freshwater Research 42:1-43.

30

Brittain J. E. 1980. Mayfly strategies in a norwegian subalpine lake. In: Advances in Ephemeropteran biology. J. F. Flannagan and K. E. Marshall (eds). Plenum Publishing Corporation, pp. 179-186.

Brock T. C. M., De Lyon M. J. H., Van Laar E. M. J. M. and Van Loon E. M. M. 1985. Field studies on the breakdown of Nuphar lutea (L.)Sm. (Nymphaeaceae), and comparison of three mathematical models for organic weight loss. Aquatic Botany 21: 1-22.

Brönmark C. and Hansson L-A. 1998. The Biology of Lake and Ponds, Oxford University Press, Oxford.

Cabana G. and Rasmussen J. B.1994. Modelling food-chain structure and contaminant bioaccumulation using stable nitrogen isotopes. Nature 372: 255-257.

Campbell I. C., James K. R., Hart B. T. and Devereaux A. 1992. Allochthonous coarse particulate organic material in forest and pasture reaches of two south-eastern Australian streams. I. Litter accession. Freshwater Biology 27: 341-352.

Caraco N. and Cole J. 2004. When Terrestrial Organic Matter Is Sent Down the River: The Importance of Allochthonous Carbon Inputs to the Metabolism of Lakes and Rivers. In: Food Webs at the Landscape Level, edited by G. A. Polis, M. E. Power, and G. R. Huxel. The University of Chicago Press, Chicago pp. 301-316.

Cardinale B. J., Palmer M. A. and Collins S. L. 2002. Species diversity enhances ecosystem functioning through interspecific fascilation. Nature 415: 426-429.

Cargill A. S., Cummins K. W., Hanson B. J. and Lowry R. R. 1985. The role of lipids as feeding stimulants for shredding aquatic insects. Freshwater Biology 15: 455-464.

Carter M. D. and Suberkropp K. 2004. Respiration and annual fungal production associated with decomposing leaf litter in two streams. Freshwater Biology 49: 1112-1122.

Casper P. 1987. Bedeutung von terrestrischen pflantzenmaterial fur den stoffhaushalt eines oligotrophen gewässers (Stechlinsee). Limnologica (Berlin) 18: 423-430.

Chapman D. W. and Demory R. L. 1963. Seasonal changes in the food ingested by aquatic insect larvae and nymphs in two Oregon streams. Ecology 44: 140-146.

Chergui H. and Patee E. 1992. Processing of fresh and dry Salix leaves in a Moroccan river system. Acta Oecologica 13: 291-298.

Cole J. J., Pace M. L., Carpenter S. R. and Kitchell J. F. 2000. Persistence of net heterotrophy in lakes during nutrient addition and food web manipulations. Limnology and Oceanography 45: 1718-1730.

Cole J. J., Carpenter S. R., Kitchell J. F. and Pace M. L. 2002. Pathways of organic carbon utilization in small lakes: Results from a whole-lake 13C addition and coupled model. Limnology and Oceanography 47:1664-1675.

Covich A. P., Palmer M. A. and Crowl T. A. 1999. The role of benthic invertebrate species in freshwater ecosystems. BioScience 49: 119-127.

Covich A. P., Austen M. C., Bärlocher F., Chauvet E., Cardinale B. J., Biles C. L., Inchausti P., Dangles O., Solan M., Gessner M. O., Statzner B. and Moss B. 2004. The Role of Biodiversity in the Functioning of Freshwater and Marine Benthic Ecosystems. BioScience 54: 767-775.

Czachorowski S. 1993. Distribution of Trichoptera larvae in vertical profile of lakes. Polskie Archiwium Hydrobiologii 40: 139-163.

Cummins K. W. 1986. Riparian influence on stream ecosystems. In: Stream protection, edited by I. C. Campbell, Water studies center, Chisholm Institute of Technology, Caufield, Australia pp. 45-55.

31

Cummins K. W., Wilzbach M. A., Gates D. M., Perry J. B. and Taliaferro W. B. 1989. Shredders and riparian vegetation. Leaf litter that falls into streams influences communities of stream invertebrates. BioScience 39: 24-30.

Cuppen J. G. M., Gylstra R., van Beusekom S., Budde B. J. and Brock T. C. M. 1995. Effects of nutrient loading and insecticide application on the ecology of Elodea-dominated freshwater microcosms. III. Responses of macroinvertebrate detritivores, breakdown of plantlitter, and final conclusions. Archiv für Hydrobiologie 134: 157-177.

D’Angelo D. J. and Webster J. R. 1992. Natural and constrainment-induced factors influencing the breakdown of dogwood and oak leaves. Hydrobiologia 237: 39-46.

Dangles O., Gessner M. O., Guérold F. and Chauvet E. 2004. Impacts of stream acidification on litter breakdown: implications for assessing ecosystem functioning. Journal of Applied Ecology 41: 365-378.

Dangles O. and Guérold F. 1998. A comparative study of beech leaf break-down, energetic content, and associated fauna in acidic and non-acidic streams. Archiv für Hydrobiologie 144: 25-39.

Dangles O. and Guérold F. 2001. Linking Shredders and Leaf Litter Processing: Insights from an Acidic Stream Study. International Review of Hydrobiology 86: 395-406.

del Giorgio P. A. and Peters R. H. 1994. Patters in planktonic P:R ratios in lakes: Influence of lake trophy and dissolved organic carbon. Limnology and Oceanography 39: 772-787.

del Giorgio P. A. and Gasol J. M. 1995. Biomass distribution in freshwater plankton communities. American Naturalist 146: 135-152.

Dieterich M., Anderson N. H. and Anderson T. M. 1997. Shredder-collector interactions in temporary streams of western Oregon. Freshwater Biology 38: 387-393.

Dobson M. 1994. Microhabitat as a determinant of diversity: stream invertebrates colonizing leaf packs. Freshwater Biology 32: 565-572.

Felip M., Pace M. L. and Cole J. J. 1996. Regulation of planktonic bacterial growth rates: The effects of temperature and resources. Microbial Ecology 31: 15-28.

Findlay S. E. G. and Sinsabaugh R. L. 2003. Aquatic ecosystems: interactivity of dissolved organic matter, Academic Press, San Diego.

Fjellheim A. and Raddum G. G. 1988. Birch leaf processing and associated macroinvertebrates in an acidified lake subjected to liming. Hydrobiologia 157: 89-94.

France R. L. and Peters R. H. 1995. Predictive model of the effects on lake metabolism of decreased airborne litterfall through riparian deforestation. Conservation Biology 9: 1578-1586.

France R., Culbert H. and Peters R. 1996. Decreased Carbon and Nutrient Input to Boreal Lakes from Particulate Organic Matter Following Riparian Clear-Cutting. Environmental Management 20: 579-583.

Friberg N. and Jacobsen D. 1994. Feeding plasticity of two detrivore-shredders. Freshwater Biology 32: 133-142.

Friberg N. 1997. Benthic invertebrate communities in six Danish forest streams: Impact of forest type on structure and function. Ecography 20: 19-28.

Gage M. S., Spivak A., and Paradise C. J. 2004. Effects of Land Use and disturbance on Benthic Insects in Headwater Streams Draining Small Watersheds North of Charlotte, NC. Southeastern Naturalist 3: 345-358.

32

Gasith A. and Hasler A. D. 1976. Airborne litterfall as a source of organic matter in lakes. Limnology and Oceanography 21: 253-258.

Gessner M. O., Chauvet E. and Dobson M. 1999. A perspective on litter breakdown in streams. OIKOS 85: 377-384.

Gessner M. O. and Dobson M. 1993. Colonisation of fresh and dried leaf litter by lotic macroinvertebrates. Archive für Hydrobiologie 127: 141-149.

Gessner M. O., Inchausti P., Persson L., Raffaaelli D. G. and Giller P. S. 2004. Biodiversity effects on ecosystem functioning: insights from aquatic systems. OIKOS 104: 419-422.

Gessner M. O., Robinson C. T. and Ward J. V. 1998. Leaf breakdown in streams of an alpine glacial floodplain: dynamics of fungi and nutrients. Journal of North American Benthological Society 17: 403-419.

Gessner M. O., Schieferstein B., Muller U., Barkmann S. and Lenfers U. A. 1996. A partial budget of primary organic carbon flows in the littoral zone of a hardwater lake. Aquatic Botany 55: 93-105.

Giller P. S. and Malmqvist B. 1998. The Biology of Streams and Rivers, Oxford University Press, Oxford.

Giller P. S., Hillebrand H., Berninger U-G., Gessner M. O., Hawkins S., Inchausti P., Inglis C., Leslie H., Malmqvist B., Monaghan M. T., Morin P. J., and O'Mullan G. 2004. Biodiversity effects on ecosystem functioning: emerging issues and their experimental test in aquatic environments. OIKOS 104: 423-436.

Goedkoop W. and Johnson R. K. 1992. Modeling the importance of sediment bacterial carbon for profundal macroinvertebrates along a lake nutrient gradient. Netherlands Journal of Aquatic Ecology 26: 477-483.

Goncalves Jr J. F., Santos A. M. and Esteves F. A. 2004. The influence of the chemical composition of Typha domingensis and Nymphaea ampla detritus on invertebrate colonization during decomposition in a Brazilian lagoon. Hydrobiologia 527: 125-137.

Gonzáles J. M. and Graça M. A. S. 2003. Conversion of leaf litter to secondary production by shredding caddies-fly. Freshwater Biology 48: 1578-1592.

Graça, M. A. S. 2001. The Role of Invertebrates on Leaf Litter Decomposition in Streams - a Review. International Review of Hydrobiology 86: 383-393.

Grubbs S. A. and Cummins K. W. 1996. Linkages between riparian forest composition and shredder voltinism. Archiv für Hydrobiologie 137: 39-58.

Haapala A., Moutka T. and Markkola A. 2001. Breakdown and macroinvertebrate and fungal colonization of alder, birch and willow leaves in a boreal forest stream. Journal of North American Benthological Society 20: 395-407.

Hargeby A. 1990. Effects of pH, humic substances and animal interactions on survival and physiological status of Asellus aquaticus L. and Gammarus pulex (L.) – A field experiment. Oecologia 82: 348-354.

Heard S. B. and Richardson J. S. 1995. Shredder-collector facilitation in stream detrital food webs: is there enough evidence? OIKOS 72: 359-366.

Henrikson L. and Oscarson H. G.1996. Retarded breakdown of leaves in acidified lakes - a consequence of decreased invertebrate fragmentation. In: L. Henrikson. Acidification and liming of freshwater ecosystems - Examples of biotic responses and mechanisms. Dissertation thesis, Göteborg University.

Herrmann J., Degerman E., Gerhardt A., Johansson C., Lingdell P-E. and Muniz I. P. 1993. Acid-stress Effects on Stream Biology. Ambio 22:298-307.

Hessen D. O. and Tranvik L. J. 1998. Aquatic Humic Substances. Ecology and Biogeochemistry. Springer, Berlin.

33

Hietz P. 1992. Decomposition and nutrient dynamics of reed (Phragmites australis (Cav.) Trin: ex Steud.) litter in Lake Neusiedl, Austria. Aquatic Botany 43: 211-230.

Huxel G. R., Polis G. A. and Holt R. D. 2004. At the Frontier of the Integration of Food Web Ecology and Landscape Ecology. In: Food Webs at the Landscape Level, edited by G. A. Polis, M. E. Power, and G. R. Huxel. The University of Chicago Press, Chicago, pp 434-451.

Hynes H. B. N. 1975. The stream and its valley. Verh.Internat.Verein.Limnol. 19 :1-15, 1975.

Irons III J. G., Oswood M. W., Stout R. J. and Pringle C. M. 1994. Latitudinal patterns in leaf litter breakdown:is temperature really important? Freshwater Biology 32: 401-411.

Jones J. I. and Waldron S. 2003. Combined stable isotope and gut contents analysis of food webs in plant-dominated, shallow lakes. Freshwater Biology 48: 1396-1407.

Kaushik N. K. and Hynes H. B. N. 1971. The fate of dead leaves that fall into streams. Archiv für Hydrobiologie 68: 465-515.

Kelly C. A., M. Rudd J. W., Furutani A. and Schindler D. W. 1984. Effects of lake acidification on rates of organic matter decomposition in sediments. Limnology and Oceanography 29:687-694.

Kok C. J., Hof C. H. J., Lenssen J. P. M. and van der Velde G. 1992. The influence of pH on concentrations of protein and phenoloics and resource quality of decomposing floating leaf material of Nymphaea alba L. (Nymphaeaceae) for the detrivore Asellus aquaticus (L.). Oecologia 91: 229-234.

Kok C. J. and van der Velde G. 1994. Decomposition and Macroinvertebrate Colonization of Aquatic and Terrestrial Leaf Material in Alkaline and Acid Still Water. Freshwater Biology 31: 65-75.

Kornijow R., Gulati R. D. and Ozimek T. 1995. Food preference of freshwater invertebrates: comparing fresh and decomposed angiosperm and filamentous alga. Freshwater Biology 33: 205-212.

Lajtha K. and Michener R. H. 1995. Stable isotopes in ecology and environmental science, Blackwell Scientific Publications, London.

Lampert W. and Sommer U. 1997. Limnoecology: The Ecology of Lakes and Streams. Oxford University Press, Oxford, p 279.

Loreau M. 2000. Biodiversity and ecosystem functioning: recent theoretical advances. OIKOS 91: 3-17.

Loreau M. and Naeem S. 2002. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294: 804-808.

MacIntyre S. and Melack J. M. 1995. Vertical and horizontal transport in lakes: linking littoral, benthic and pelagic habitats. Journal of North American Benthological Society 14: 599-615.

Mancinelli G., Constantini M. L. and Rossi L. 2004. Cascading effects of predatory fish exclusion on the detritus-based food-web of a lake littoral zone (Lake Vico.central Italy). Oecologia 133: 402-411.

Mann K. H. 1988. Production and use of detritus in various freshwater, estuarine, and coastal marine ecosystems. Limnology and Oceanography 33: 910-930.

Meili M. 1992. Sources, concentrations and characteristics of organic matter in softwater lakes and streams of the Swedish forest region. Hydrobiologia 229: 23-41.

Meili M., Fry B. and Kling G. W. 1993. Fractionation of stable isotops (13C, 15N) in the food web of a humic lake. Verh.Internat.Verein.Limnol. 25: 501-505.

34

Merritt R. W., Cummins K. W. and Burton T. M. 1984. The role of aquatic insects in the processing and cycling of nutrients. In: The ecology of aquatic insects., V. H. Resh and D. M. Rosenberg (eds), Praeger Publisher, New York, pp: 134-163.

Meyer J. L. and O'Hop J. 1983. Leaf-shredding insects as a source of dissolved organic carbon in headwater streams. The American Midland Naturalist 109: 175-183.

Mihuc T. B. and Mihuc J. R. 1995. Trophic ecology of five shredders in a Rocky Mountain stream. Journal of Freshwater Ecology 10: 209-216.

Mille-Lindblom C. and Tranvik L. J. 2003. Antagonism between Bacteria and Fungi on decomposing Aquatic Plant Litter. Microbial Ecology 45: 173-182.

Monakov A. V. 2003. Feeding of freshwater invertebrates. Kenobi productions, Ghent.

Newell S. Y., Moran M. A., Wicks R. and Hodson R. E. 1995. Productivities of microbial decomposers during early stages of decomposition of leaves of a freshwater sedge. Freshwater Biology 34: 135-148.

Oertli B. 1993. Leaf Litter Processing and Energy Flow Through Macroinvertebrates in a Woodland Pond (Switzerland). Oecologia 96: 466-477.

Oertli B. and Dall P. C. 1993. Population dynamics and energy budget of Nemoura avicularis (Plecoptera) in Lake Esrom, Denmark. Limnologica 23: 115-122.

Palmer M. A., Covich A. P., Finlay B. J., Gibert J., Hyde K. D., Johnson R. K., Kairesalo T., Lake S., Lovell C. R., Naiman R. J., Ricci C., Sabater F. and. Strayer D. 1997. Biodiversity and ecosystem processes in freshwater sediments. Ambio 26: 571-577.

Palmer M. A., Covich A. P., Lake S., Biro P., Brooks J. J., Cole J., Dahm C., Gibert J., Goedkoop W., Martens K., Verhoven J., and van der Bund W. J. 2000. Linkages between aquatic sediment biota and life above sediments as potential drivers of biodiversity and ecological processes. BioScience 50: 1062-1075.

Pascoal C., Pinho M., Cássio F. and Gomes P. 2003. Assessing structural and functional ecosystem condition using leaf breakdown: studies on a polluted river. Freshwater Biology 48: 2033-2044.

Perry J. A. and Troelstrup Jr. N. H. 1988. Whole ecosystem manipulation: a productive avenue for test system research? Environmental Toxicology and Chemistry 7: 941-951.

Persson L., Bengtsson J., Menge B. A. and Power M. E. 1997. Productivity and consumer regulation - concepts, patterns and mechanisms. In: Food Webs. Integration of patterns and dynamics. G. A. Polis and K. O. Winemiller (eds). Chapman and Hall, New York, pp. 396-434.

Petersen R. C. and Cummins. K. W. 1974. Leaf processing in a Woodland stream. Freshwater Biology 4: 343-368.

Petersen Jr R. C., Cummins K. W. and Ward G. M. 1989. Microbial and animal processing of detritus in a woodland stream. Ecological Monographs 59: 21-39.

Peterson B. J. and Fry B. 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18: 293-320.

Peterson G., Allen C. R. and Holling C. S. 1998. Ecological resilience, biodiversity and scale. Ecosystems 1: 6-18.

Pieczynska E. 1972. The role of allochthonous matter in lakes. Wiadomosci Ekologiczne 18: 131-140.

Pieczynska E. 1990. Lentic aquatic-terrestrial ecotones: their structure, functions and importance. In: The ecology and management of aquatic-terrestrial ecotones. R. J. Naiman and H. Decamps (eds). Unesco, Paris, pp. 103-140.

35

Pieczynska E. 1993. Detritus and nutrient dynamics in the shore zone of lakes: a review. Hydrobiologia 251: 49-58.

Pope R. J., Gordon A. M. and Kaushik N. K. 1999. Leaf litter colonization by invertebrates in the littoral zone of a small oligotrophic lake. Hydrobiologia 392: 99-112.

Porter K. G. and Feig Y. S. 1980. The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography 25: 943-948.

Post D. M. 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703-718.

Prus T. 1981. Decomposition of leaf litter by Asellus aquaticus L. (Isopda, Crustacea). Verh.Internat.Verein.Limnol. 21: 1585-1588.

Reutz III C. R., Newman R. M. and Vondracek B. 2002. Top-down control in detritus based food web: fish, shredders and leaf breakdown. Oecologia 132: 307-315.

Rich P. H. and Wetzel R. G. 1978. Detritus in the lake ecosystem. The American Naturalist 112: 57-71.

Riley R. H. and Jefferies R. L. 2004. Subsidy dynamics and Global Change. In: Food Webs at the Landscape Level, edited by G. A. Polis, M. E. Power, and G. R. Huxel. The University of Chicago Press, Chicago pp. 410-433.

Robinson C. T. and Gessner M. O. 2000. Nutrient addition accelerates leaf breakdown in an alpine springbrook. Oecologia 122: 258-263.

Robinson C. T. and Gessner M. O. 2003. Litter decomposition. In: Ecology of glacial a flood plain, edited by J. V. Ward and U. Uehlinger. Kluwer, Dordrecht, pp. 217-230.

Sabetta L., Constantini M. L., Maggi O., Persiani A. M. and Rossi L. 2000. Interactions between detritivores and microfungi during the leaf detritus decomposition in a volcanic lake (Lake Vingra - central Italy). Hydrobiologia 439: 49-60.

Sala O. E., Chapin III F. S., Armesto J. J., Berlow E., Bloomfield J., Dirzo R., Huber-Sanwald E., Huenneke L. F., Kinzig A., Leemans R., Lodge D. M., Mooney H. A., Oesterheld M., LeRoy Poff N., Sykes M. T., Walker B. H., Walker M. and Wall D. H. 2000. Global biodiversity scenarios for the year 2100. Science 287: 1770-1774.

Schofield K. A., Pringle C. M., Meyer J. L., and Sutherland A. B. 2001. The importance of crayfish in the breakdown of rhododendron leaf litter. Freshwater Biology 46: 1191-1204.

Schwartz M. W., Brigham C. A., Hoeksema J. D., Lyons K. G., Mills M. H. and van Mantgem P. J. 2000. Linking biodiversity to ecosystem function: implications for conservation ecology. Oecologia 122: 297-305.

Short R. A. and Ward J. V. 1980. Trophic ecology of three winter stoneflies (Plecoptera). American Midland Naturalist 105: 341-347.

Simon M. and Azam F. 1989. Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser 51: 201-213.

Sinsabaugh R. L., Likens A. E. and Benfield E. F. 1985. Cellulose digestion and assimilation by three leaf-shredding aquatic insects. Ecology 66: 1464-1471.

Smith D. C. and Azam F. 1992. A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Marine Microbial Food Webs 6: 107-114.

Stockner J. G. and Porter K. G. 1988. Microbial food webs in freshwater planktonic ecosystems. In: Complex interactions in lake communities, edited by S. R. Carpenter. Springer-Verlag, New York, pp. 69-160.

36

Strayer D. 1991. Perspectives on the size and structure of lacustrine zoobenthos, its causes, and its consequences. Journal of North American Benthological Society 10: 210-221.

Suberkropp K. 1992. Interaction with invertebrates. In:F. Bärlocher. The Ecology of Aquatic Hyphomycetes. Springer-Verlag, Berlin.

Sun L., Perdue, E. M. Meyer J. L. and. Welch H. E. 1997. Use of elemental composition to predict bioavailability of dissolved organic matter in a Georgia river. Limnology and Oceanography 42: 714-721.

Thurman E. M. 1985. Organic geochemistry of natural waters, Nijhoff/Junk, Boston. Tranvik L. J.1988. Availability of dissolved organic carbon for planktonic bacteria in

oligotrophic lakes of different humic content. Microbial Ecology 16:311-322. Tranvik L. J. 1992. Allochthonous dissolved organic matter as an energy source for

pelagic bacteria and the concept of micobial loop. Hydrobiologia 229: 107-114. Tuchman N. C. 1993. Relative importance of microbes versus macroinvertebrate

shredders in the process of leaf decay in lakes of differing pH. Canadian Journal of Fisheries and Aquatic Science 50: 2707-2712.

Usio N., Konishi M., and Nakano S. 2001. Is invertebrate shredding critical for collector invertebrates? Ecological Research 16: 319-326.

van Dokkum H. P, Slijkerman M. E., Rossi L. and Constantini M. L. 2002. Variation in the decomposition of Phragmites australis litter in a monomictic lake: the role of gammarids. Hydrobiologia 482: 69-77.

Vander Zanden M. J., Casselman J. M. and Rasmussen J. B.1999. Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401: 464-469.

Vannote R. L., Minshall G. W., Cummins K. W., Sedell J. R., and Cushing C. E. 1980. The River Continuum Concept. Canadian Journal of Fisheries and Aquatic Science 37: 130-137.

Wall Freckman D., Blackburn T. H., Brussard L., Hutchings P., Palmer M. A., and Snelgrove P. V. R. 1997. Linking biodiversity and ecosystem functioning of soils and sediments. Ambio 26: 556-562.

Wallace J. B. and Webster J. R. 1996. The role of macroinvertebrates in stream ecosystem function. Annual Review of Entomology 41: 115-139.

Walters K. H. and Smock L. A. 1991. Cellulase activity of leaf litter and stream-dwelling, shredder macroinvertebrates. Hydrobiologia 220: 29-35.

Webster J. R. and Benfield E. F. 1986. Vascular plant breakdown in freshwater ecosystems. Annual Review of Ecology and Systematics 17: 567-594.

Webster J. R., Benfield E. F., Ehrman T. P., Schaeffer M. A., Tank J. L., Hutchens J. J. and D’Angelo D. J. 1999. What happens to allochthonous material that falls into streams? A synthesis of new and published information from Coweeta. Freshwater Biology 41: 687-705.

Wetzel R. G. 1995. Death, detritus, and energy flow in aquatic ecosystems. Freshwater Biology 33: 83-89.

Wetzel R. G. 2001. Limnology. Lake and River Ecosystems. Academic Press, San Diego.

37

Acknowledgements The time of thesis work has brought me new invaluable insights of both research and the essence of life. I could not have made this without the support and stimulation from many people. It is not possible to mention all of you, so a warm thank you to everyone! Still, I want to recognize some persons who have been especially important for my work. My supervisors Jan Herrmann, Lars Tranvik and Jan Stenson, for all kinds of help, for many stimulating discussions, for believing in me and for having patience with me when the work was resting of different reasons. Ulf Bjelke, for sharing my scientific interests and for high-quality teamwork in the field, laboratory and in front of the computer. Edna Granéli, for general support and personal encouragement. All PhD students in Kalmar and Göteborg, for fine companionship and discussions. My “adjunkt”-colleagues; Anna, Crister, Per-Eric and Roland, who showed me that it is possible to produce a thesis parallel to other tasks at the Department. Everyone at the Department of Biology and Environmental Science has meant a lot to me during my long time as a PhD-student. Patrik and Roland gave valuable statistical advice. Görgen provided map charts. Bosse and Brita facilitated my last months of writing. The girl meetings with Ann-Karin, Katarina, Kerstin, Maria, Mia and Päivi have been most valuable to get perspectives on all kind of issues of work and life. My mother and father, who always stimulated me to do what I believe in, even the most incomprehensible things as studying detritus for almost ten years. My fantastic family; Thomas, Anton and Julia, for filling my life with meaning and happiness. Your everlasting support was really important for this work. Thank you!

38