PLANKTON DYNAMICS

Phytoplankton growth is controlled by the balance between reproduction and mortality. Phytoplankton reproduction is determined by environmental factors (such as temperature and pH) and by essential resources (such as light and nutrients). In my thesis, I investigated the importance of the essential resources light and nutrients for phytoplankton dynamics in laboratory and field experiments. Research questions involved topics such as: the resource use efficiency of phytoplankton communities, the role of resources for phytoplankton stoichiometry, aspects of phytoplankton food quality and grazing by zooplankton, costs of behavioural strategies of mobile phytoplankton species and the establishment of new methods to quantify growth and loss processes of phytoplankton in situ. EFFECTS OF DIVERSITY ON PHYTOPLANKTON RESOURCE UPTAKE AND GROWTH The resource use efficiency of terrestrial plant communities has been related to taxonomic diversity and a recent metaanalysis of freshwater and brackish phytoplankton communities shows that this relationship also exists in phytoplankton communities. Our experiments with natural and assembled phytoplankton communities showed a clear effect of phytoplankton biodiversity on carbon incorporation. Phytoplankton functional groups differ in their resource use attributes and exhibit different constituents of photosynthetic active pigments. We have shown that the diversity of wavelength specific photosynthetically active pigments was a function of the taxonomic diversity of the phytoplankton communities. The effect of biodiversity on carbon incorporation was related to the functional (biochemical) diversity of phytoplankton communities (Paper 1). Increasing biodiversity and thereby increasing pigment diversity resulted in a higher absorbance of light within the photosynthetic active radiation spectrum and thereby higher carbon assimilation. EFFECTS OF DIVERSITY ON PHYTOPLANKTON RESOURCE UPTAKE AND BIOMASS COMPOSITION (STOICHIOMETRY) Phytoplankton carbon assimilation and nutrient uptake are not tightly coupled. As a result of fluctuating resources, autotrophs can exhibit variable biomass compositions (biomass carbon to nutrient ratios). The increased efficiency of resource use in highly diverse phytoplankton communities (Paper 1) also has consequences for the biomass composition of those communities (Paper 2). Increasing biodiversity resulted in increasing carbon assimilation, but not in a comparable increase of phosphorus uptake. This resulted in increasing biomass carbon to phosphorous ratios. Phytoplankton with high biomass carbon to phosphorus ratios are considered to be low quality food for cladoceran zooplankton such as Daphnia. Although the stoichiometry of Daphnia varies somewhat with algae and diet, they maintain a relatively homeostatic composition with low carbon to nutrient (phosphorus) biomass composition compared to their food. Phytoplankton biodiversity could therefore also have consequences for freshwater phytoplankton-zooplankton interactions. The mismatch in the biomass composition between phytoplankton and Daphnia could lead to changed trophic transfer efficiencies between phytoplankton and zooplankton and hence affect the entire pelagic food web. THE SUPPLY OF LIGHT AND NUTRIENTS AND ITS CONSEQUENCES FOR PHYTOPLANKTON-ZOOPLANKTON INTERACTIONS Both, low and high light to nutrient (phosphorus) ratios in the environment can restrict herbivore growth rates by either the quantity (photosynthetically fixed carbon) of phytoplankton at low light to nutrient ratios or the nutritional quality (biomass carbon to phosphorus ratios) of phytoplankton at high light to nutrient ratios. This can result in an unimodal relationship between light intensity and zooplankton growth. In mesocosm experiments with natural phytoplankton communities from different lakes, we established gradients of light to nutrient ratios by manipulating the light availability for phytoplankton. After two weeks we added the herbivorous zooplankter Daphnia magna to the mesocosms. Indeed, in treatments from phosphorus limited oligotrophic and mesotrophic lakes we found unimodal relationships between light intensity and Daphnia growth rates (Paper 3). At low light levels Daphnia growth rates were limited by food quantity and at high light levels they were limited by food quality. Light dependent variations of natural phytoplankton biomass carbon to phosphorus ratios can effect zooplankton growth. COSTS OF BEHAVIOURAL STRATEGIES FOR PHYTOPLANKTON RESOURCES UPTAKE In pelagic environments, light and nutrients are not equally distributed within the water column and show vertical gradients of availability. While light intensity is higher in upper water layers, nutrient concentrations are, during periods of stratification, generally higher in deeper water layers. A possibility for phytoplankton species to optimize resource uptake is mobility. Mobile species can (at least to a certain degree) migrate within the water column to choose an optimal position for nutrient uptake and photosynthesis. Mobility involves costs in terms of energy to develop, maintain and operate mobility structures. We conducted laboratory growth experiments with mobile and non-mobile green algal species along a gradient of light availability (Paper 4). Phytoplankton biomass (determined as particulate organic carbon) and biomass carbon to phosphorus ratios of non-mobile species were higher than those of mobile species. This indicates that the efficiency of resource use of mobile species was worse than that of non-mobile species. Mobile species had higher energy requirements to balance the costs of basic metabolism. Thus, the advantages of mobility are restricted to specific environmental conditions. NEW METHODS TO ESTIMATE GROWTH AND MORTALITY OF PHYTOPLANKTON COMMUNITIES It is difficult to measure phytoplankton growth and mortality (grazing by micro- and mesozooplankton) in situ in natural phytoplankton communities. However, these are important parameters to understand the dynamics of natural phytoplankton communities. We established a new method to estimate phytoplankton growth and mortality by combining existing dilution (to measure mortality) and dialysis (to measure growth) techniques (Paper 5). Experiments showed that the combination of these methods can be successfully used to quantify phytoplankton gross growth rates and micro- and mesozooplankton grazing in situ

Phytoplankton community responses to temperature fluctuations under different nutrient concentrations and stoichiometry

Nutrient availability and temperature are important drivers of phytoplankton growth and stoichiometry. However, the interactive effects of nutrients and temperature on phytoplankton have been analyzed mostly by addressing changes in average temperature, whereas recent evidence suggests an important role of temperature fluctuations. In a laboratory experiment, we grew a natural phytoplankton community under fluctuating and constant temperature regimes across 25 combinations of nitrogen (N) and phosphorus (P) supply. Temperature fluctuations decreased phytoplankton growth rate (rmax), as predicted by nonlinear averaging along the temperature–growth relationship. rmax increased with increasing P supply, and a significant temperature × P × N interaction reflected that the shape of the thermal reaction norm depended on nutrients. By contrast, phytoplankton carrying capacity increased with N supply and in fluctuating rather than constant temperature. Higher phytoplankton N:P ratios under constant temperature showed that temperature regimes affected cellular nutrient incorporation. Minor differences in species diversity and composition existed. Our results suggest that temperature variability interacts with nutrient supply to affect phytoplankton physiology and stoichiometry at the community level

“Unifying” the Concept of Resource Use Efficiency in Ecology

Resource use efficiency (RUE) is an ecological concept that measures the proportion of supplied resources, which is converted into new biomass, i.e., it relates realized to potential productivity. It is also commonly perceived as one of the main mechanisms linking biodiversity to ecosystem functioning based on the assumption that higher species numbers lead to more complementary and consequently more efficient use of the available resources. While there exists a large body of literature lending theoretical and experimental support to this hypothesis, there are a number of inconsistencies regarding its application: First, empirical tests use highly divergent approaches to calculate RUE. Second, the quantification of RUE is commonly based on measures of standing stock instead of productivity rates and total pools of nutrients instead of their bioavailable fractions, which both vary across systems and therefore can introduce considerable bias. Third, conceptual studies suggest that the relationship between biodiversity, productivity and RUE involves many more mechanisms than complementary resource use, resulting in variable magnitude and direction of biodiversity effects on productivity. Moreover, RUE has mainly been applied to single elements, ignoring stoichiometric, or metabolic constraints that lead to co-limitation by multiple resources. In this review we illustrate and discuss the use of RUE within and across systems and highlight how the various drivers of RUE affect the diversity-productivity relationship with increasing temporal and spatial scales as well as under anthropogenic global change. We illustrate how resource supply, resource uptake and RUE interactively determine ecosystem productivity. In addition, we illustrate how in the context of biodiversity and ecosystem functioning, the addition of a species will only result in more efficient resource use, and consequently, higher community productivity if the species' traits related to resource uptake and RUE are positively correlated

The importance of phytoplankton trait variability in spring bloom formation

About 60 years ago, the critical depth hypothesis was proposed to describe the occurrence of spring phytoplankton blooms and emphasized the role of stratification for the timing of onset. Since then, several alternative hypotheses appeared focusing on the role of grazing and mixing processes such as turbulent convection or wind activity. Surprisingly, the role of community composition—and thus the distribution of phytoplankton traits—for bloom formation has not been addressed. Here, we discuss how trait variability between competing species might influence phytoplankton growth during the onset of the spring bloom. We hypothesize that the bloom will only occur if there are species with a combination of traits fitting to the environmental conditions at the respective location and time. The basic traits for formation of the typical spring bloom are high growth rates and photoadaptation to low light conditions, but other traits such as nutrient kinetics and grazing resistance might also be important. We present concise ideas on how to test our theoretical considerations experimentally. Furthermore, we suggest that future models of phytoplankton blooms should include both water column dynamics and variability of phytoplankton traits to make realistic projections instead of treating the phytoplankton bloom as an aggregate community phenomenon

Decomposing multiple dimensions of stability in global change experiments

Ecological stability is the central framework to understand an ecosystem’s ability to absorb or recover from environmental change. Recent modelling and conceptual work suggests that stability is a multidimensional construct comprising different response aspects. Using two freshwater mesocosm experiments as case studies, we show how the response to single perturbations can be decomposed in different stability aspects (resistance, resilience, recovery, temporal stability) for both ecosystem functions and community composition. We find that extended community recovery is tightly connected to a nearly complete recovery of the function (biomass production), whereas systems with incomplete recovery of the species composition ranged widely in their biomass compared to controls. Moreover, recovery was most complete when either resistance or resilience was high, the latter associated with low temporal stability around the recovery trend. In summary, no single aspect of stability was sufficient to reflect the overall stability of the system

Sea surface phytoplankton community response to nutrient and light changes

The sea surface microlayer (SML) is the boundary layer between the ocean and the atmosphere and plays a unique role in marine biogeochemistry. Phytoplankton communities in this uppermost surface layer are exposed to extreme ultraviolet (UV) radiation and potentially high nutrient supplies. In order to understand the response of SML communities to such contrasting conditions, we conducted experiments at three different sites, the North Sea (open ocean) and two sites, outer and middle fjord, in the Sognefjord, Norway, with differing physical and chemical parameters. We manipulated light, nitrogen (N) and phosphorus (P) supply to natural communities collected from the SML and compared their response to that of the underlying water (ULW) communities at 1-m depth. Phytoplankton communities in both SML and ULW responded significantly to N addition, suggesting the upper 1-m surface phytoplankton communities were N-limited. While phytoplankton growth rates were higher with high N and high light supply, biomass yield was higher under low light conditions and with a combined N and P supply. Furthermore, biomass yield was generally higher in the ULW communities compared to SML communities. Nutrient and light effects on phytoplankton growth rates, particulate organic carbon (POC) and stoichiometry varied with geographical location. Phytoplankton growth rates in both SML and ULW at the open ocean station, the site with highest salinity, did not respond to light changes, whereas the communities in the middle fjord, characterized by high turbidity and low salinity, did experience light limitation. This work on the upper surface phytoplankton communities provides new insights into possible effects of coastal darkening and increases understanding of oceanic biogeochemical cycling

“Unifying” the Concept of Resource Use Efficiency in Ecology

Resource use efficiency (RUE) is an ecological concept that measures the proportion of supplied resources, which is converted into new biomass, i.e., it relates realized to potential productivity. It is also commonly perceived as one of the main mechanisms linking biodiversity to ecosystem functioning based on the assumption that higher species numbers lead to more complementary and consequently more efficient use of the available resources. While there exists a large body of literature lending theoretical and experimental support to this hypothesis, there are a number of inconsistencies regarding its application: First, empirical tests use highly divergent approaches to calculate RUE. Second, the quantification of RUE is commonly based on measures of standing stock instead of productivity rates and total pools of nutrients instead of their bioavailable fractions, which both vary across systems and therefore can introduce considerable bias. Third, conceptual studies suggest that the relationship between biodiversity, productivity and RUE involves many more mechanisms than complementary resource use, resulting in variable magnitude and direction of biodiversity effects on productivity. Moreover, RUE has mainly been applied to single elements, ignoring stoichiometric, or metabolic constraints that lead to co-limitation by multiple resources. In this review we illustrate and discuss the use of RUE within and across systems and highlight how the various drivers of RUE affect the diversity-productivity relationship with increasing temporal and spatial scales as well as under anthropogenic global change. We illustrate how resource supply, resource uptake and RUE interactively determine ecosystem productivity. In addition, we illustrate how in the context of biodiversity and ecosystem functioning, the addition of a species will only result in more efficient resource use, and consequently, higher community productivity if the species' traits related to resource uptake and RUE are positively correlated

Warming and oligotrophication cause shifts in freshwater phytoplankton communities

While there is a lot of data on interactive effects of eutrophication and warming, to date, we lack data to generate reliable predictions concerning possible effects of nutrient decrease and temperature increase on community composition and functional responses. In recent years, a wide‐ranging trend of nutrient decrease (re‐oligotrophication) was reported for freshwater systems. Small lakes and ponds, in particular, show rapid responses to anthropogenic pressures and became model systems to investigate single as well as synergistic effects of warming and fertilization in situ and in experiments. Therefore, we set up an experiment to investigate the single as well as the interactive effects of nutrient reduction and gradual temperature increase on a natural freshwater phytoplankton community, using an experimental indoor mesocosm setup. Biomass production initially increased with warming but decreased with nutrient depletion. If nutrient supply was constant, biomass increased further, especially under warming conditions. Under low nutrient supply, we found a sharp transition from initially positive effects of warming to negative effects when resources became scarce. Warming reduced phytoplankton richness and evenness, whereas nutrient reduction at ambient temperature had positive effects on diversity. Our results indicate that temperature effects on freshwater systems will be altered by nutrient availability. These interactive effects of energy increase and resource decrease have major impacts on biodiversity and ecosystem function and thus need to be considered in environmental management plans

Anti-Fouling Effects of Saponin-Containing Crude Extracts from Tropical Indo-Pacific Sea Cucumbers

Sea cucumbers are bottom dwelling invertebrates, which are mostly found on subtropical and tropical sea grass beds, sandy reef flats, or reef slopes. Although constantly exposed to fouling communities in these habitats, many species are surprisingly free of invertebrate epibionts and microfouling algae such as diatoms. In our study, we investigated the anti-fouling (AF) activities of different crude extracts of tropical Indo-Pacific sea cucumber species against the fouling diatom Cylindrotheca closterium. Nine sea cucumber species from three genera (i.e., Holothuria, Bohadschia, Actinopyga) were selected and extracted to assess their AF activities. To verify whether the sea cucumber characteristic triterpene glycosides were responsible for the observed potent AF activities, we tested purified fractions enriched in saponins isolated from Bohadschia argus, representing one of the most active anti-fouling extracts. Saponins were quantified by vanillin-sulfuric acid colorimetric assays and identified by LC-MS and LC-MS/MS analyses. We were able to demonstrate that AF activities in sea cucumber extracts were species-specific, and growth inhibition as well as attachment of the diatom to surfaces is dependent on the saponin concentration (i.e., Actinopyga contained the highest quantities), as well as on the molecular composition and structure of the present saponins (i.e., Bivittoside D derivative was the most bioactive compound). In conclusion, the here performed AF assay represents a promising and fast method for selecting the most promising bioactive organism as well as for identifying novel compounds with potent AF activities for the discovery of potentially novel pharmacologically active natural products

Cell size as driver and sentinel of phytoplankton community structure and functioning

Body size is a decisive functional trait in many organisms, especially for phytoplankton, which span several orders of magnitude in cell volume. Therefore, the analysis of size as a functional trait driving species’ performance has received wide attention in aquatic ecology, amended in recent decades by studies documenting changes in phytoplankton size in response to abiotic or biotic factors in the environment. We performed a systematic literature review to provide an overarching, partially quantitative synthesis of cell size as a driver and sentinel of phytoplankton ecology. We found consistent and significant allometric relationships between cell sizes and the functional performance of phytoplankton species (cellular rates of carbon fixation, respiration and exudation as well as resource affinities, uptake and content). Size scaling became weaker, absent or even negative when addressing C- or volume-specific rates or growth. C-specific photosynthesis and population growth rate peaked at intermediate cell sizes around 100 µm3. Additionally, we found a rich literature on sizes changing in response to warming, nutrients and pollutants. Whereas small cells tended to dominate under oligotrophic and warm conditions, there are a few notable exceptions, which indicates that other environmental or biotic constraints alter this general trend. Grazing seems a likely explanation, which we reviewed to understand both how size affects edibility and how size structure changes in response to grazing. Cell size also predisposes the strength and outcome of competitive interactions between algal species. Finally, we address size in a community context, where size-abundance scaling describes community composition and thereby the biodiversity in phytoplankton assemblages. We conclude that (a) size is a highly predictive trait for phytoplankton metabolism at the cellular scale, with less strong and nonlinear implications for growth and specific metabolism and (b) size structure is a highly suitable sentinel of phytoplankton responses to changing environments. A free Plain Language Summary can be found within the Supporting Information of this article