Effects of Macrophytes, Fish and Metazooplankton on a Microbial Food Web
Total Page：16
File Type：pdf, Size：1020Kb
EFFECTS OF MACROPHYTES, FISH AND METAZOOPLANKTON ON A MICROBIAL FOOD WEB Veetaimestiku, kalade ja metazooplanktoni mõju mikroobsele toiduahelale KATRIT KARUS A Thesis For applying for the degree of Doctor of Philosophy in Hydrobiology Väitekiri Filosoofiadoktori kraadi taotlemiseks hüdrobioloogia erialal Tartu 2014 Eesti Maaülikooli doktoritööd Doctoral Thesis of the Estonian University of Life Sciences EFFECTS OF MACROPHYTES, FISH AND METAZOOPLANKTON ON A MICROBIAL FOOD WEB Veetaimestiku, kalade ja metazooplanktoni mõju mikroobsele toiduahelale KATRIT KARUS A Thesis For applying for the degree of Doctor of Philosophy in Hydrobiology Väitekiri Filosoofi adoktori kraadi taotlemiseks hüdrobioloogia erialal Tartu 2014 Institute of Agricultural and Environmental Sciences Estonian University of Life Sciences According to verdict No 195 of July 4, 2014 the Doctoral Committee for Agricultural and Natural Sciences of the Estonian University of Life Sciences has accepted the thesis for the defence of the degree of Doctor of Philosophy in Hydrobiology. Opponent: Jouko Sarvala, Professor Emeritus Department of Biology, University of Turku, Finland Supervisor: Priit Zingel, PhD Centre for Limnology, Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences Reviewer: Priit Zingel, PhD Centre for Limnology, Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences Defence of the thesis: Estonian University of Life Sciences, Kreutzwaldi 5 (room 1A5), Tartu, on August 28, 2014, at 10:00. The English language was edited by T M B G Editing, United Kingdom and Estonian language by Priit Zingel. Copyrighted papers in this dissertation are reproduced by courtesy of the Elsevier; John Wiley & Sons Inc. and Association for the Sciences of Limnology and Oceanography, Inc. Publication of this dissertation is granted by the Doctoral School of Earth Sciences and Ecology created under the auspices of European Social Fund. © Katrit Karus, 2014 ISSN 2382-7076 ISBN 978-9949-536-38-2 (trükis) ISBN 978-9949-536-39-9 (pdf) CONTENTS LIST OF ORIGINAL PUBLICATIONS .................................................7 1. INTRODUCTION ...................................................................................9 2. OBJECTIVES OF THE STUDY .......................................................12 3. REVIEW OF THE LITERATURE ..................................................13 3.1. Brief history of protozoology ........................................................13 3.2. Main groups of protozoa ...............................................................16 3.2.1. Ciliates .................................................................................16 3.2.2. Flagellates ............................................................................17 3.2.3. Amoebae ..............................................................................18 3.2.4. Sporozoa ..............................................................................19 3.3. Concept of microbial loop and its formation .............................20 3.4. Microbial loop as sink or link in pelagic food webs .................23 3.5. Top-down versus bottom-up control and microbial loops ......24 4. MATERIALS AND METHODS .......................................................31 4.1. Description of the study areas ......................................................31 4.2. Experimental design, sampling and sample analysis ................32 4.3. Statistical analysis ............................................................................35 5. RESULTS .................................................................................................36 5.1. Aquatic biota in study areas ..........................................................36 5.2. The infl uence of polarized macrovegetation on the central link of the microbial loop (V) .........................................37 5.3. Trophic cascade from fi sh to bacteria (I) ...................................39 5.4. The feeding infl uence of the fi sh stock on ciliated protozoans (III) ..............................................................................42 5.5. The infl uence of zp-removal and zp-enrichment treatments on microbial communities (II & IV) ......................................... 44 6. DISCUSSION ..........................................................................................48 6.1. The infl uence of polarized macrovegetation on the central link of the microbial loop (V) .........................................48 6.2. Trophic cascade from fi sh to bacteria (I) ...................................53 6.3. The feeding infl uence of the fi sh stock on ciliated protozoans (III) ..............................................................................58 6.4. The infl uence of zp-removal and zp-enrichments on microbial communities (II & IV) ..................................................................60 7. CONCLUSIONS .....................................................................................66 REFERENCES ............................................................................................69 SUMMARY IN ESTONIAN ....................................................................90 ACKNOWLEDGEMENTS......................................................................95 ORIGINAL PUBLICATIONS .................................................................97 CURRICULUM VITAE...........................................................................184 ELULOOKIRJELDUS ............................................................................190 6 LIST OF ORIGINAL PUBLICATIONS The present thesis is based on the following papers, which are referred to by Roman numerals in the dissertation. I. Karus, K., Paaver, T., Agasild, H. & Zingel, P. 2014. The effects of predation by planktivorous juvenile fi sh on the microbial food web. European Journal of Protistology, 50: 109–121. II. Agasild, H., Zingel, P., Karus, K., Kangro, K., Salujõe, J. & Nõges, T. 2013. Does metazooplankton regulate the ciliate community in a shallow eutrophic lake? Freshwater Biology, 58: 183–191. III. Zingel, P., Paaver, T., Karus, K., Agasild, H. & Nõges, T. 2012. Ciliates as the crucial food source of larval fi sh in a shallow eutrophic lake. Limnology and Oceanography, 57: 1049–1056. IV. Zingel, P., Agasild, H., Karus, K., Kangro, K., Tammert, H., Tõnno, I., Feldmann, T. & Nõges, T. The infl uence of zooplankton enrichment on the microbial loop in a shallow, eutrophic lake. Submitted to Freshwater Biology. V. Karus, K., Feldmann, T., Nõges, P. & Zingel, P. 2014. Ciliate communities of a large shallow lake: association with macrophyte beds. European Journal of Protistology, 50: 382–394. 7 Author’s contribution to the papers: I II III IV V Concept * * * Study design * * Data collection * Data analysis ***** Manuscript preparation***** 8 1. INTRODUCTION Up to the 1980s, or more precisely before the formulation of microbial loop theory, it was thought that all primary production is channelled through a classical grazing food web from phytoplankton to zooplankton to fi sh (Steele, 1974). However, several decades of studies have demonstrated that this simple idea of orderly trophic level nutrient transfers and energy fl uxes from phytoplankton to zooplankton and fi nally to fi sh is inadequate and misleading because approximately half of algal production can bypass the traditional food web and directly channel through a microbial loop (Berman, 1990; Fenchel, 1988; Pomeroy & Wiebe, 1988; Sherr & Sherr, 1991). In this loop, a crucial part of the primary production is not directly consumed by zooplankton but is channelled through a supply of organic matter before it becomes available via bacterial production to protozoans. More particularly, the loop describes a trophic pathway in a food web, where phytoplankton-derived dissolved organic matter is absorbed by heterotrophic bacteria, their production is grazed by ciliates and heterotrophic nanofl agellates, and this “dissolved organic matter- bacteria-protozoa” loop is then coupled with a classical grazing food web by metazoan grazing on protozoans. Therefore, it follows that protozoans form a trophic nexus in microbial food webs. The effi ciency with which zooplankton communities consume primary production and their own suitability as food for larger zooplankton and/or fi sh determines the effi cacy of the food web. As the microbial loop usually consists of more trophic levels and the energy loss is higher owing to respiration at each level, this kind of food web is considered a less effi cient pathway for energy and nutrients than the classical grazing food web (Pomeroy & Wiebe, 1988). Moreover, this loop theory has long been a debating issue because it implicates another system, which can be separated from the classical grazing food web. However, the microbial loop should be considered an integral part of the pelagic food webs as there is no separate loop or appendage beside the classical food web and no fi rm border between them; they are connected to each other in many direct and indirect ways (Porter et al., 1988; Riemann & Christoffersen, 1993). For these various reasons, the importance of microbial loop in the functioning of ecosystems as well as food webs in lakes is underestimated. Consequently, most food web studies have focused on classical grazing food webs, studying interactions from fi sh and macrophytes to zooplankton and phytoplankton. The cascading effects of fi sh on whole microbial loop 9 organisms have been