Institute of Biochemistry and Biology Ecology and Ecosystem Modelling Food web regulation under different forcing regimes in shallow lakes – synthesis and modelling Ph D. Thesis (cummulative) in partial fulfillment for the award of the degree “doctor rerum naturalium” (Dr. rer. nat.) in the scientific discipline of “Ecology” submitted to the Faculty of Science University of Potsdam by Betty Lischke Berlin, November 2015 Published online at the Institutional Repository of the University of Potsdam: URN urn:nbn:de:kobv:517-opus4-89149 http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-89149 Institut für Biochemie und Biologie Ökologie und Ökosystemmodellierung Food web regulation under different forcing regimes in shallow lakes – synthesis and modelling Dissertation (kumulativ) zur Erlangung des akademischen Grades "doctor rerum naturalium" (Dr. rer. nat.) in der Wissenschaftsdisziplin „Ökologie“ eingereicht an der Mathematisch-Naturwissenschaftlichen Fakultät der Universität Potsdam von Betty Lischke Berlin, November 2015 Contents Contents GENERAL INTRODUCTION 1 Thesis outline 8 DECLARATION OF CONTRIBUTIONS 9 CHAPTER I – Enhanced t-POM flux reduces resilience of clear state 11 Abstract 12 Introduction 12 Methods 14 PCLake 14 Critical phosphorus loading (CPL) 16 Bifurcation analysis 17 Terrestrial particulate organic matter 17 Scenarios 18 Results 19 Discussion 21 Acknowledgements 25 References 26 Supporting Information 30 CHAPTER II – Winterkill of fish 35 Abstract 36 Introduction 36 Methods 38 Study sites 38 Water sampling and analyses 38 Fish abundance 38 Carbon stable isotope ratios and gut content analysis of roach 40 Phytoplankton and crustacean biomass 40 Data analysis 40 Results 41 Fish biomass, abundance and community structure after partial winterkill 41 Seasonal changes in roach diet after partial winterkill 42 Seasonal development of phytoplankton and crustacean biomass before (2007) and after partial winterkill 44 Discussion 45 Effects of the partial winterkill on fish biomass and community composition 45 Contents Differences in phytoplankton development after a partial winterkill 46 Implications for climate effects on temperate small eutrophic shallow lakes 47 Acknowledgements 48 References 49 CHAPTER III – Ciliates dominating zooplankton 53 Abstract 54 Introduction 54 Methods 56 Study site 56 Zooplankton 57 Phytoplankton 57 Bacteria 58 Data analysis 58 Data for cross lake comparisons 59 Results 59 Metazooplankton biomass and composition 60 Phytoplankton biomass and composition 61 Ciliates biomass and composition 61 Bacterial biomass 63 Ciliate top-down effects on phytoplankton and bacteria 63 Discussion 65 Metazooplankton under severe grazing pressure 65 Effects on phytoplankton 66 Severe top-down control by ciliate dominance 67 Conclusions 70 Acknowledgements 70 References 71 Supporting Information 77 CHAPTER IV – Pelagic and benthic carbon fluxes in shallow lakes 81 Abstract 82 Introduction 82 Methods 83 General overview 83 Autotrophs 84 Bacteria 85 Zooplankton 85 Macrobenthos 85 Fish 86 Contents PDOC pool 86 Food web 86 Results 87 Biomass patterns and carbon fluxes between food web components 87 Pelagic vs. benthic carbon fluxes 89 Pelagic, benthic and food web efficiencies 91 Discussion 92 Conclusion 95 Acknowledgements 96 References 97 Supporting Information 102 GENERAL DISCUSSION 103 Conclusion 111 SUMMARY 113 ZUSAMMENFASSUNG 115 REFERENCES (GENERAL INTRODUCTION AND DISCUSSION) 117 DANKSAGUNG 125 ERKLÄRUNG 127 CURRICULUM VITAE 129 List of Publications 130 Reviewed publications 130 Manuscripts in preparation 130 Scientific Contributions 131 General Introduction General Introduction Living organisms grow and reproduce based on autotrophic or heterotrophic assimilation and they are subject to the consumption by other organisms. These trophic interactions form predator-prey pairs, food chains and food webs, with an increasing degree of complexity regarding the underlying regulating processes. The food web regulation characterizes processes limiting the biomass or production of its components. The dominant processes are the top-down and bottom-up control, which describes the regulation of the prey through predator feeding and the limited availability of resources or prey for the predator, respectively. Thus, in predator-prey systems the prey is usually top-down and the predator bottom-up controlled. In contrast to biotic predator-prey pairs, the utilization of abiotic resources, such as nutrients and light, may form consumer-resource interactions with bottom- up regulated consumers. A bottom-up regulated population increases in biomass if more resources or prey production is available and decreases if less is available. A top-down regulated population is in general characterized by low biomasses and high production to biomass ratios. Their biomass remains stable if the amount of resources or prey production available to them increases. Solely the production of the top-down regulated population can increase up to their physiologically determined maximum production to biomass ratio. A further increase of resources would remain unconsumed. The concept of top-down and bottom-up regulation is continuously extended e.g. to the trophic cascade concept (Carpenter et al., 1985), by including omnivory, leading to apparent competition or apparent mutualism (Abrams et al., 1998) and intraguild predation (Polis et al., 1989), and by considering a weaker or stronger linked parallel food chain (Wollrab et al., 2012). These extensions of the concept of bottom-up regulated predators and top-down regulated prey enhance its utility for food web analyses. Trophic interactions are ubiquitous, but they not necessarily regulate a population. Beyond trophic interactions also non-trophic interactions are relevant for the food web regulation, e.g. the competition for light between autotrophs, the production of allelopathic substances by macrophytes, which hamper the phytoplankton growth (Hilt and Gross, 2008) and macrophytes providing shelter from fish predation (Jeppesen et al., 1997; Timms and Moss, 1984). Finally, also abiotic conditions limit the production of organisms as e.g. well known for crustaceans in spring. A large amount of food is available during the phytoplankton spring bloom, but crustacean growth is limited by low temperatures which diminishes the trophic regulation of phytoplankton (Straile, 2000). Thus, a variety of processes determines the regulation of the food web components, which consequently results in a specific food web structure. Alterations of the top-down and bottom-up regulation under different forcing regimes have presumably consequences at the species, community and ecosystem scale, such as the dominant species, the community biomass and size spectrum and the prevalent ecosystem state (e.g. turbid or clear-water state). Forcing regimes may arise from external and internal, 1 General Introduction abiotic and biotic processes and may strengthen, reduce or even reverse the regulating forces of food web components, as exemplified for aquatic ecosystems (Table 1). Effects of the enhanced input of terrestrial organic matter into aquatic ecosystems (chapter I) and persistent low temperatures in winter (chapter II & III) are categorized as external, abiotic forcing regimes. Western civilization is already aware of the problems regarding large nutrient fluxes, e.g. from agriculture into aquatic ecosystems, as another external, abiotic forcing regime and manage to regulate the fluxes for several ecosystems. However, developing countries still face the major problems of eutrophication e.g. for the stable supply of drinking water. In a tri- trophic food chain higher nutrient availability may cause increased phytoplankton production which is not utilized by their top-down controlled predators. Food web theory predicts that the top-predator of this system accumulates biomass until it is sufficient to sustain a further trophic level. Then, this fourth trophic level leads to control changes at each trophic level, i.e. top-down becomes bottom-up and vice versa (Oksanen et al., 1981). Biomanipulation as an ecosystem management tool relies on this concept and aims to enhance the water quality by reducing the phytoplankton biomass with the introduction of a fourth trophic level, namely piscivorous fish (Benndorf, 1995). Biotic, external processes, as feeding by waterfowls, might also regulate trophic food web interactions (Table 1). The predation pressure by waterfowls on a specific ecosystem food web may strongly vary in time, as they are mobile and thus have access to prey from different ecosystems. Waterfowls feeding from aquatic food webs export biomass and therefore, either strengthen the bottom-up control of the organisms’ predator or release its prey from top-down pressure. The waterfowls’ excrements and organic matter or even living organisms transported within their feathers are an import to aquatic ecosystems, which may again alter the ecosystem food web regulation. Besides external, also internal, abiotic forcing regimes such as the stratification of lakes may affect the food web regulation. Stratification hampers the access to nutrients for phytoplankton and thus their production especially in oligotrophic systems, which may consequently lead to bottom-up regulated predators. Additionally, internal, biotic processes may strongly alter the trophic food web interactions, for example the formation of defense strategies against predation, which can be morphological, chemical or realized by predator avoidance.