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«Tag der mündlichen Prüfung: 24.11.2005 Environmental variables and plankton communities in the pelagic of lakes: enclosure experiment and ...»

-- [ Page 1 ] --

Erstgutachter: Prof. Dr. Sebastian Diehl

Zweitgutachter: Prof. Dr. Wilfried Gabriel

Tag der mündlichen Prüfung: 24.11.2005

Environmental variables

and plankton communities in the pelagic of lakes:

enclosure experiment and comparative lake survey

Stella A. Berger

Dissertation

zur Erlangung des Doktorgrades

der Fakultät für Biologie

der Ludwig-Maximilians-Universität München

März 2005

Table of contents 1 Table of contents Table of contents

Summary

Zusammenfassung

Introduction

Summary of the articles

Article 1 Effects of mixing depth and background turbidity on phytoplankton biomass, light and nutrients

Article 2 Light supply, plankton biomass and seston stoichiometry in a gradient of lake mixing depths

Article 3

Phytoplankton taxonomic composition in relation to environmental variables:

a comparative lake study using pigment analysis

Synopsis

Outlook

References

Articles

Article 1 Effects of mixing depth and background turbidity on phytoplankton biomass, light and nutrients

Article 2 Light supply, plankton biomass and seston stoichiometry in a gradient of lake mixing depths

Article 3

Phytoplankton taxonomic composition in relation to environmental variables:

a comparative lake study using pigment analysis

Acknowledgements

Curriculum vitae

Summary 2

Summary

Most primary production of lakes and oceans occurs in the well-mixed surface layer that is subject to strong seasonal and geographical variation. With increasing mixed surface layer depth average light supply and specific nutrient supply decrease and so do light-dependent production rates and depth-dependent sinking loss rates of phytoplankton. Changes in mixing depth are expected to have important consequences for the dynamics of phytoplankton biomass, algal nutrient stoichiometry, light availability and nutrient retention in the mixed layer. Light absorption by enhanced concentrations of abiotic substances (humic substances, clay particles) furthermore negatively affects light availability and production.

I tested the predictions of a dynamical “closed system” model concerning the effects of mixing depth and background turbidity (Kbg) on phytoplankton biomass, light climate and nutrients in a field enclosure experiment. The natural phytoplankton community was exposed to high and low background turbidity along a gradient of mixing depth. For sinking algae, the model predicts that phytoplankton biomass should be most strongly limited by sedimentation losses in shallow mixed layers, by mineral nutrients at intermediate mixing depths and by a lack of light in deep mixed layers. As predicted, phytoplankton volumetric and areal biomasses showed a unimodal relationship to mixing depth and were negatively affected by background attenuation. With increasing Kbg the biomass peak shifted towards shallower mixing depth. The concentrations of dissolved and total nutrients were positively affected by increasing mixing depth but only marginally related to Kbg most likely due to a variable carbon to phosphorus cell quota.

For thermally stratified lakes I derived the following predictions from a dynamical “open system” model which includes variable algal cell quota: within a realistic mixing depth range (3-12m) light availability, phytoplankton density, and the carbon:phosphorus ratio of algal biomass should all be negatively related to mixing depth, while algal standing stock should be unimodally related, and total and dissolved nutrients be horizontally or positively related to mixing depth. All these prediction were in qualitatively good agreement with data from 65 central European lakes sampled during summer stratification. Notably, I observed the predicted negative relationship between phytoplankton density and mixing depth in spite of the rather limited range of mixing depths typical for medium sized temperate lakes.

Summary 3 Furthermore, I found a strong negative relationship among zooplankton biomass and mixing depth.

In a comprehensive comparative lake study of 40 northern German lakes, I sampled the surface mixed layers for a set of variables and focused on the taxonomic composition of phytoplankton and the relationships of taxonomic classes to environmental variables. I used high performance liquid chromatography to analyse the phytoplankton samples for 13 photosynthetic pigments and calculated the contributions of seven algal classes with distinct pigment signatures to total chlorophyll a using CHEMTAX, a matrix factorisation program. In multiple regression analyses, I examined the relationships of phytoplankton biomass and composition to total nitrogen (TN), total phosphorus (TP), total silica (TSi), mixing depth, water temperature, and zooplankton biomass. Total Chl-a was positively related to TN and TP and unimodally related to mixing depth. TN was the factor most strongly related to the biomasses of single taxa. I found positive relationships of chrysophytes, chlorophytes, cryptophytes, and euglenophytes to TN, and of diatoms and chrysophytes to TSi. Diatoms were negatively related to TN. Cryptophytes and chlorophytes were negatively and cyanobacteria positively related to zooplankton.





Finally, the relative biomasses of chrysophytes and cryptophytes were negatively related to mixing depth. Most results were consistent with theoretical expectations.

Some relationships may, however, have been masked by strong cross-correlations among several environmental variables.

Zusammenfassung 4

Zusammenfassung

Der Großteil der Primärproduktion in Seen und Ozeanen findet in der gut durchmischten Oberflächendeckschicht statt, die starken saisonalen und geographischen Schwankungen unterliegt. Zunehmende vertikale Ausdehnung der durchmischten Oberflächendeckschicht (Durchmischungstiefe) führt zu verringertem mittleren Licht- und Nährstoffangebot und damit zu abnehmender lichtabhängiger Produktionsrate, sowie zu verringerter Sedimentationverlustsrate des Phytoplanktons.

Veränderungen der Durchmischungstiefe beeinflussen somit die Dynamik der Phytoplanktonbiomasse, der Nährstoff-Stoichiometrie der Algen, der Lichtverfügbarkeit und der Nährstoffretention in der durchmischen Schicht. Zusätzlich verringert eine erhöhte Konzentration an Licht absorbierenden abiotischen Substanzen im Wasser (Huminstoffe, Tonpartikel) die Lichtverfügbarkeit und damit die Produktion des Phytoplanktons.

Ich überprüfte die Vorhersagen eines dynamischen Modells, das die Auswirkungen von Durchmischungstiefe und Hintergrundtrübung (Kbg) auf Phytoplanktonbiomasse, Lichtklima und Nährstoffverteilung in einem „geschossenen System“ beschreibt, mit einem Enclosure-Experiment. Entlang eines Gradienten zunehmender Durchmischungstiefe wurde die natürliche Phytoplanktongemeinschaft hoher und niedriger Hintergrundtrübung ausgesetzt. Für sinkendes Phytoplankton sagt das Modell vorher, dass die Phytoplanktonbiomasse stark durch Sedimentationsverluste in geringen Durchmischungstiefen limitiert ist, durch mineralische Nährstoffe in mittleren Durchmischungstiefen und durch Lichtmangel in einer tief durchmischen Wasserschicht.

Wie vorhergesagt zeigten Algenkonzentration und Gesamtbiomasse eine unimodale Beziehung zur Durchmischungstiefe und waren beide negativ durch erhöhte Hintergrundattenuation beeinflusst. Mit erhöhter Hintergrundtrübung verschoben sich, wie vorausgesagt, die Maxima der Algenbiomassen in Richtung geringerer Durchmischungstiefe. Die Konzentrationen an gelöstem und Gesamtphosphor zeigten, wie erwartet, eine positive Beziehung zur Durchmischungstiefe und wurden nur marginal von der Hintergrundtrübung beeinflusst, höchstwahrscheinlich bedingt durch ein variables Kohlenstoff zu Phosphor Verhältnis in den Zellen.

Für thermisch geschichtete Seen („offenes System“) konnte ich aus einem dynamischen Modell mit integriertem variablen Kohlenstoff zu Phosphor Verhältnis der Algen folgende Vorhersagen ableiten: innerhalb realistischer DurchmischungsZusammenfassung 5 tiefenbereiche (3-12m) sollte mit zunehmender Durchmischungstiefe die mittlere Lichtverfügbarkeit, die Phytoplanktonkonzentration und das Kohlenstoff zu Phosphor Verhältnis der Algenbiomasse abnehmen. Die Gesamtalgenbiomasse sollte unimodal zur Durchmischungstiefe stehen und die gelösten und Gesamtnährstoffe sollten einen leicht ansteigenden Verlauf zeigen bzw. unbeeinflusst von der Durchmischungstiefe sein. Diese Modellvorhersagen konnten in einer vergleichenden Seenstudie, die eine Beprobung von 65 zentraleuropäischen Seen während der sommerlichen Schichtung umfasste, weitgehend bestätigt werden. Besonders hervorzuheben ist die negative Beziehung zwischen Phytoplanktonbiomasse und Durchmischungstiefe trotz der relativ geringen Durchmischungstiefenspanne, die typisch für Seen mittlerer Größe der gemäßigten Zone ist. Darüber hinaus konnte ich einen stark negativen Zusammenhang zwischen Zooplanktonbiomasse und Durchmischungstiefe aufdecken.

In einer sehr umfangreich beprobten Seenstudie 40 norddeutscher Seen untersuchte ich die taxonomische Zusammensetzung des Phytoplanktons und die Beziehungen einzelner Phytoplanktonklassen zu verschiedenen Umweltfaktoren. Ich verwendete eine moderne Methode zur Analyse der Phytoplanktonproben, die Hochdruckflüssigkeitschromatographie (HPLC) und konnte 13 photosynthetisch aktive Pigmente extrahieren. Ich ermittelte den jeweiligen Chorophyll-a Anteil von 7 Algenklassen am Gesamtchlorophyll-a - Gehalt durch eindeutige Pigmentsignaturen mit Hilfe von CHEMTAX, einem Matrix-Faktorisierungs-Programm. Durch Regressionsanalysen untersuchte ich die Zusammenhänge zwischen Phytoplanktonbiomasse bzw. einzelner Taxa und den ´unabhängigen´ Variablen Gesamtstickstoff (TN), Gasamtphosphor (TP), Gasamtsilikat (TSi), Durchmischungstiefe, Wassertemperatur, und Zooplanktonbiomasse. Der Gesamtchlorophyll a-Gehalt stand in positiver Beziehung zu TN und TP und zeigte eine unimodale Beziehung zur Durchmischungs-tiefe. TN schien der wichtigste Faktor zu sein und stand zu den meisten Algentaxa in Beziehung.

Chrysophyten, Chlorophyten, Cryptophyten und Euglenophyten zeigten eine positive Beziehung zu TN, Diatomeen und Chrysophyceen eine positive zu TSi und Diatomeen eine negative zu TN. Cryptophyten und Chlorophyten zeigte eine negative, Cyanobakterien dagegen eine positive Beziehung zum Zooplankton. Die relativen Biomasseanteile von Chrysophyten und Cryptophyten hingen negativ mit der Durchmischungstiefe zusammen. Ein Großteil der Ergebnisse stimmte mit den theoretischen Erwartungen überein. Manche Beziehungen jedoch waren möglicherweise durch starke Korrelationen zwischen einigen Umweltfaktoren verdeckt.

Introduction 6

Introduction

As all plants, phytoplankton requires light for photosynthesis and nutrients for growth, reproduction and metabolism. The supply of resources limiting algal production (light and nutrients) is highly variable depending on their environment. A major part of primary production in the pelagic of lakes and oceans occurs in the well-mixed surface layer. Light and nutrients fundamentally differ in their distribution within a well-mixed water column. While nutrients are relatively homogenously distributed, light decreases exponentially with depth due to absorption by water molecules. The vertical extension of the surface mixed layer (mixing depth) has strong negative effects on the mean light availability for passively entrained phytoplankton (Kirk 1994). The underwater light climate, particularly of lakes and estuaries is also affected by the concentration of light absorbing substances. Light attenuation by, e.g., humic substances or clay particles can be enormous and is summarised as background turbidity (Kbg) (Cuker 1987; Carpenter et al. 1998;

Guildford et al. 1987). In many lakes, however, a major part of the available light may be absorbed by primary producers themselves (Tilzer 1983; Kirk et al. 1986). Thus, changes in phytoplankton biomass have direct feedback effects on the light climate in the mixed layer.

While increased background turbidity and mixing depth both negatively affect mean light intensity and, consequently, light-limited production of phytoplankton (Sverdrup 1953; Huisman 1999; Diehl et al. 2002) mixing depth also affects the sedimentation loss rates of phytoplankton. The sedimentation loss rate of negativelybuoyant algae is inversely related to mixing depth (Reynolds et al. 1984; Visser et al.

1996; Diehl et al. 2002; Ptacnik et al. 2003) and thus becomes most relevant to phytoplankton biomass in shallow mixed layers.

The vertical extension of the mixed surface layer can vary seasonally within lakes and geographically among lakes (Guildford et al. 1994; Soto 2002; Kunz and Diehl 2003). Furthermore, mixing depth depends on lake size and orientation to the dominating wind direction, water clarity and has been related to overall climate (Sterner 1990; Fee et al. 1996). It should therefore be regarded as an important environmental driver affecting phytoplankton biomass in a variety of ways.

Since the onset of widespread anthropogenic eutrophication limnologists have focused mainly on the effects of nutrient enrichment on phytoplankton and later Introduction 7 became interested in effects of zooplankton grazing on food web structure in lakes (Sarnelle 1992; Persson et al. 1992; Mazumder et al. 1994). The strong positive relationship between chlorophyll a (Chl-a) and total phosphorus content (TP) became a dogma in freshwater ecosystems research (e.g. Dillon et al. 1974; Schindler 1978), while nitrogen (and silica) seemed to be more important as limiting nutrients in marine ecosystems and were rarely examined in freshwater ecosystems. The supply of light was examined to a lesser extent. Still, light and nutrients are interactively essential resources for phytoplankton growth sensu Tilman (1982); i.e., within limits an increase in either resource can overcome limitation by the other. As a consequence, increases in nutrient supply should ultimately increase the attenuation of light caused by phytoplankton biomass (Huisman et al. 1995; Scheffer 1998).

Mechanistic understanding of the complex interrelationships and feedback mechanisms among mixing depth, nutrient supply, phytoplankton and light climate requires a dynamical modeling approach.



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