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«Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften Dr. rer. nat. der Fakultät für Biologie der Ludwig-Maximilians-Universität ...»

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Selected interactions between phytoplankton, zooplankton and the microbial

food web: Microcosm experiments in marine and limnic habitats

Dissertation

zur Erlangung des Doktorgrades der Naturwissenschaften

Dr. rer. nat.

der Fakultät für Biologie der Ludwig-Maximilians-Universität München

by

Alexis Katechakis

München 2005

Selected interactions between phytoplankton, zooplankton and the microbial

food web: Microcosm experiments in marine and limnic habitats

Dissertation

zur Erlangung des Doktorgrades der Naturwissenschaften Dr. rer. nat.

der Fakultät für Biologie der Ludwig-Maximilians-Universität München by Alexis Katechakis Eingereicht am: 24. November 2005

1. Gutachter: PD Dr. Herwig Stibor

2. Gutachter: Prof. Dr. Sebastian Diehl Tag der mündlichen Prüfung: 17. März 2006 A L'ANNA

CONTENTS

Summary / Key words …………………………………………………………………………………1

1. Introduction ……….……….………………………………………………………………………4

1.1. Thesis objectives, approach and outline……………………………………………………….5

1.2. The pelagic food web ………………………………………………………………………….7

1.3. Bottom-up vs. top-down control ………………………………………………………………9

1.4. Natural vs. cultural enrichment ………………………………………………………………10

2. Study backgrounds ………………………………………………………………………………11

2.1. Backgrounds Study A – Copepods, cladocerans, doliolids…………………………………..11

2.2. Backgrounds Study B – Mixotrophs …………………………………………………………13

3. Paper summaries…………………………………………………………………………………15 A1 Feeding selectivities and food niche separation of Acartia clausi, Penilia avirostris (Crustacea) and Doliolum denticulatum (Thaliacea) in Blanes Bay (Catalan Sea, NW Mediterranean). Journal of Plankton Research (2004) 26:589–603 ….………………15 A2 Changes in the phytoplankton community and microbial food web of Blanes Bay (Catalan Sea, NW Mediterranean) under prolonged grazing pressure by doliolids (Tunicata), cladocerans or copepods (Crustacea). Marine Ecology Progress Series (2002) 234:55–69 ………………………………………….…………………………………17 A3 Feeding selectivities of the marine cladocerans Penilia avirostris, Podon intermedius and Evadne nordmanni. Marine Biology (2004) 145:529–539l ………………..19 B1 Mixotrophic vs. obligately autotrophic algae as food for zooplankton – the light:nutrient hypothesis might not hold for mixotrophs. Limnology and Oceanography (2005) 50:1290–1299 ………………………….……………………………21 B2 The mixotroph Ochromonas tuberculata may invade and suppress specialist phagoand phototroph plankton communities depending on nutrient conditions. Oecologia (2005), submitted ………………………………………………………………………….…24

4. Conclusions …………………………………………………………………………………….…27

5. Research outlook ……………….……………….………………………………………………28

6. References …………………………….……………………….…………………………………31 Attachments ● Paper reprints ● Personal notes Curriculum vitae – Publication list / Grants – Acknowledgements – Declaration 1 · Summary SUMMARY The experiments presented in this thesis elucidate selected interactions between the phytoplankton, the zooplankton and the microbial food web in aquatic ecosystems. The objective is to provide a mechanistic understanding of classic general ecology topics including competition, predator-prey relations, food web structure, succession, and transfer of matter and energy. Special relevance is attributed to the role of mixotrophic organisms, marine cladocerans, and gelatinous mesozooplankton.

Although they may contribute substantially to plankton composition they have thus far been neglected in common ecosystem models. All experiments were based on enrichment with nutrients and organic compounds. Enrichment with nutrients and organic compounds that influence overall system productivity is one of the most pervasive human alterations of the environment and profoundly affects species composition, food web structure, and ecosystem functioning. In order to predict the consequences of such enrichment, a better understanding of the impact that trophic structure has on community dynamics and ecosystem processes is required.

The presented thesis consists of two studies. The first study includes three experiments in which I investigated the role copepods, cladocerans and doliolids play in plankton interactions. Copepods, cladocerans and doliolids are major mesozooplankton groups in marine systems. The first experiment (Katechakis et al. 2004) showed that copepods, cladocerans and doliolids have different food size spectra and different assimilation efficiencies. According to my experiment, copepods actively select for larger food items, whereas cladocerans and doliolids passively filter medium-sized and small food items, respectively, with doliolids being the only group that feeds efficiently on bacteria and picoplankton. The results illustrate that food niche separation enables copepods, cladocerans and doliolids to coexist. In addition, they emphasize the fact that doliolids are favored in low nutrient environments, characterized by small food items, whereas cladocerans and copepods have competitive advantages at moderate and high nutrient supplies, respectively. Furthermore, copepods obviously utilize ingested food best, gauged in terms of produced biomass, followed by cladocerans and doliolids, which suggests that the different mesozooplankton have different impacts on energy transfer efficiency within the food web.





In the second experiment (Katechakis et al. 2002), I investigated how copepods, cladocerans and doliolids directly influence the phytoplankton and the microbial food web over a longer period of time by grazing. Furthermore, I investigated how they indirectly influence the system's nutrient dynamics through "sloppy feeding" and their excretions. According to my experiment, in the long run, doliolids and cladocerans promote the growth of large algae whereas copepods shift the size spectrum towards small sizes with different consequences for food chain length. Doliolids, cladocerans and copepods also affect the microbial food web in different ways. Size-selective grazing may lead to differences in the nanoplankton concentrations. These in turn can affect bacterial concentrations in a trophic cascade.

My findings offered the first experimental evidence for the occurrence of top-down effects in marine Summary · 2 systems. Although top-down explanations of phytoplankton size structure had been acknowledged for limnic systems before, they had not been attempted for marine systems.

In the last experiment of this series (Katechakis and Stibor 2004) I sought to complement the knowledge about the feeding behavior of marine cladocerans. Marine cladocerans are difficult to cultivate in the laboratory. Therefore, the three cladoceran genera found in marine systems, Penilia, Podon and Evadne, had never before been compared under similar conditions. Existing studies with single cladoceran genera were to some extent contradictory. My experiments indicate similar feeding characteristics for Penilia, Podon and Evadne, that is to say, similar food size spectra, clearance and ingestion rates. However, Evadne obviously has problems feeding on motile prey organisms.

The results generated by my first study have been summarized and their importance has been hypothetically extended to ecosystem level by Sommer et al. (2002) and by Sommer and Stibor (2002).

My second study includes two experiments that refer to the ecological role of mixotrophs in aquatic systems. Mixotrophic organisms combine phototrophic and phagotrophic production dependent on the availability of light and nutrients. Although they are common in aquatic systems, their function for nutrient cycling and as a link to higher trophic levels has never before been examined.

In my first experiment (Katechakis et al. 2005) I investigated if mixotrophs influence energy transfer efficiency to higher trophic levels differently than predicted for purely phototrophic organisms. My results indicate that compared to phototrophic specialists mixotrophs may enhance transfer efficiency towards herbivores at low light conditions and in situations when limiting nutrients are linked to bacteria and to the picoplankton. Additionally, the results suggest that mixotrophs may have a stabilizing effect on variations in trophic cascade strength caused by perturbations to light and nutrient supply ratios.

My second experiment (Katechakis and Stibor 2005a) served as a first step towards analyzing if the results gained from the first experiment have any ecological relevance in situ, that is, if mixotrophs in nature-like communities can gain enough importance to relevantly influence transfer efficiency and system stability. Competition experiments revealed that mixotrophs may invade and suppress plankton communities that consist of purely phototrophic and purely phagotrophic specialists at low nutrient conditions while high nutrient supplies prevent mixotrophs from successfully invading such communities. In systems where mixotrophs suppressed their specialist competitors they indeed had a habitat-ameliorating effect for higher trophic levels, gauged in terms of plankton food quality.

In the meantime, the results gained from my experiments have inspired various other studies in marine and limnic systems.

3 · Key Words

KEY WORDS

aquatic food web • assimilation efficiency • autotrophy • bottom-up control • cladocerans • clearance rate • coexistence • competition • copepods • doliolids • ecological stoichiometry (ES) • effective food concentration (EFC) • energy transfer efficiency • enrichment • eutrophication • feeding selectivity • food niche separation • food quality • food quantity • food web dynamics • food web model • food web theory • gelatinous plankton • generalist • grazing • herbivory • heterotrophy • indirect effects • ingestion rate • invasion • light-nutrient hypothesis (LNH) • limnic food web • marine food web • mechanistic resource competition theory • microbial food web • microcosm • mixotrophy • niche overlap • nutrient stoichiometry • omnivory • pelagic food web • phagotrophy • phototrophy • phytoplankton • plankton composition • plankton ecology • plankton size structure • predation • primary production • productivity • secondary production • specialization • top-down control • trophic cascade • trophic structure • tunicates • zooplankton

Introduction · 4

CHAPTER 1 – INTRODUCTION

Pelagic food webs are the most common type of food webs on earth and planktonic organisms involved in pelagic food webs may possibly be the most abundant on earth. Regarding solely protozoa, more than 1500 million tons of them exist in the Southern Ocean alone. In contrast, all vertebrates together, including fish, penguins, seals and whales make up only 16 million tons (Beaumont 2003).

Hence, it is not surprising, that the dynamics of planktonic food webs have powerful impacts on important issues such as world climate (e.g. Beaumont et al. 1998, Toole and Siegel 2004), global biogeochemical cycling (e.g. Dachs et al. 2002, Valdes et al. 2004) and the world food production (e.g. Meadows et al. 2004). For example, plankton influences climate and biogeochemical cycling by absorbing carbon dioxide (e.g. Beaumont 1998), releasing cloud-forming compounds such as dimethylsulfoniopropionate (DMSP) (Toole and Siegel 2004) and drawing huge amounts of nitrogen from the air (Capone and Carpenter 1982). Drastic changes in plankton abundances affecting food web production have recently been reported from the waters of Northern California. Oceanic plankton have largely disappeared there, followed by a general decline in near-shore oceanic life, with far fewer fish, birds and marine mammals. Reasons for the absence of the plankton have yet to be fully understood.

However, a recent study indicates that it may be a long term phenomenon linked to global warming (Gregg et al. 2003), that may, on the other hand, enhance plankton growth in other regions of the world (Goes et al. 2005).

These few examples demonstrate that despite their critical relevance for our planet, we are still only in the early stages of understanding the interactions in planktonic food webs that take place among species at different trophic levels and under changing environmental conditions. The main difficulty lies in that even relatively simple food webs have such complicated structures thus one cannot intuitively understand how a change in one variable might ultimately affect each of the others.

Therefore, ecosystem models play an ever more important role in the understanding of applied and theoretical problems in food web ecology. The question regarding what features should be incorporated into these models is fundamental for improving them. Information on physiological and community structuring properties of functional key species are essential within this context.

5 · Thesis objectives, approach and outline

1.1. Thesis objectives, approach and outline

In this thesis I focus on selected interactions such as competition, predator-prey relations, and the transfer of matter and energy between the phytoplankton, the zooplankton and the microbial food web.



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