Stöchiometrische Beschränkungen in Primärproduzenten beeiträchtigen Sekundärkonsumenten

This thesis investigates the effects of nutrient limitation in primary producers on higher trophic levels. To this aim the nutrient conditions and their effect on primary consumers in the North Sea were examined. Furthermore experiments were carried out to test the effect of nutrient limitations on tri-trophic food chains in controlled laboratory conditions. Despite the prevailing assumption that the herbivorous primary producers maintain strict homeostasis, thus buffering any nutrient imbalances at the base of the food web and providing their consumers with food of a high and constant quality, their nutrient stoichiometry and fitness was affected by the nutrient content of their food. The nutrient deficiency of the primary producers can thus be passed on through the food web and affect higher trophic levels. In a set of laboratory based experiments the nutrient contents of primary producers was manipulated to change their C:nutrient ratio and thereby their food quality. Primary consumers were reared on these producers and in turn were the food source for a higher consumer. The ctenophore Pleurobrachia pileus was exposed to copepods with manipulated C:P ratios along a gradient. The reaction of the ctenophore to food with a high C:P ratio, generally considered to be food of lower quality, was unexpected. P. pileus was negatively affected by nutrient replete food with a low C:P ratio and displayed higher levels of fitness when feeding on food with a high carbon:P ratio. This ctenophore is therefore more likely to be energy limited than nutrient limited. A possible explanation for this is the high body C:P ratio observed in P.pileus. The results are discussed in light of possible future scenarios in the aquatic environment. Freshly hatched larvae are very vulnerable and the mortality during this stage is particularly high. Therefore the effect of food with different C:N:P ratios was tested on larvae of the European lobster Homarus gammarus. Larvae were exposed to food with varying nutrient content either throughout their development or for the duration of one stage. The results confirm that the youngest larval stages are the most susceptible to a lack of nutrients in their diet, which had strong negative effects on their condition. The effect of P-limitation in particular was observed to change during ontogeny, with older larval stages being less affected. As nutrient-limitations reduce the fitness and reproductive output of primary consumers, this translates into a quantity effect for higher trophic levels by reducing the amount of food available to them. The combined effects of nutrient quality and nutrient quantity on a top predator were investigated in an experimental set-up. The consumer was negatively affected by the lack of nutrients in its diet even at very low nutrient quantities, indicating that quality of the food is more important than the quantity. Disentangling these two effects, the quality and quantity of food, remains a great challenge for future ecological studies in the marine environment. These findings have potentially far-reaching consequences for the trophic interactions and population dynamics of marine organisms.Diese Dissertation befasst sich mit Nährstofflimitationen bei Primärproduzenten und ihrer Auswirkungen auf höhere trophische Ebenen. Dazu wurden die Nährstoffbedingungen der Nordsee und ihre Auswirkungen auf Primärkonsumenten untersucht. Zusätzlich wurden Laborexperimente durchgeführt um unter kontrollierten Bedingungen die Auswirkungen von Nährstofflimitationen auf drei-trophische Nahrungsketten zu erforschen. Es ist eine weit verbreitete Annahme, dass herbivore Primärkonsumenten eine strenge Homöostase aufrechterhalten, wodurch sie sämtliche Unausgewogenheiten in der Nährstoffzusammensetzung ihres Futters puffern können. Somit würden sie eine gleichbleibend hohe Qualität als Nahrung für die nächst-höhere trophische Ebene bieten. Dennoch konnte in der vorliegenden Arbeit gezeigt werden, dass sowohl Stöchiometrie als auch Kondition dieser Primärkonsumenten beeinträchtigt wurden. Der Nährstoffmangel in Primärproduzenten kann also durch das Nahrungsnetz übermittelt werden und höhere trophische Ebenen beeinflussen. In einer Reihe von Experimenten wurde die Nährstoffzusammensetzung von Primärproduzenten manipuliert um das Kohlenstoff- zu Nährstoff-Verhältnis und somit ihre Qualität zu verändern. Primärproduzenten wurden mit diesem qualitativ veränderten Futter aufgezogen und dienten ihrerseits als Nahrung für Sekundärkonsumenten. Die Rippenqualle Pleurobrachia pileus wurde mit Copepoden gefüttert, deren C:P Verhältnis entlang eines Gradienten verlief. Die Reaktion der Qualle auf das Futter mit dem hohen C:P Verhältnis, das eigentlich als Futter von schlechterer Qualität angesehen wird, war überraschend. Pleurobrachia pileus wurde negativ beeinflusst von Futter mit ausgeglichenem Nährstoffgehalt und reagierte besser, wenn das Futter ein hohes Verhältnis von Kohlenstoff zu Phosphor aufwies. Dies bedeutet, dass die Qualle eher Energie- als Nährstofflimitiert ist, was möglicherweise im hohen CP-Verhältnis im Gewebe der Qualle begründet liegt. Die Ergebnisse werden im Zusammenhang mit den vorhergesagten Veränderungen in der aquatischen Umgebung, wie z.B. dem erhöhten Vorkommen von Quallen und der Oligotrophierung des marinen Systems diskutiert. Frisch geschlüpfte meroplanktonische Larven sind sehr verletzlich und die Mortalität während dieser Lebensphase ist besonders hoch. Deswegen wurde der Effekt von Nahrung mit unterschiedlichen C:N:P Verhältnissen auf Larven des europäischen Hummers Homarus gammarus untersucht. Larven wurden mit Futter unterschiedlicher Nährstoffzusammensetzung gefüttert. Dies wurde für den Zeitraum ihrer gesamten Entwicklung oder über die Dauer eines einzelnen Entwicklungsstadiums durchgeführt. Die Ergebnisse bestätigen, dass die jüngsten Larven am anfälligsten für Nährstoffmangel sind und ihre Kondition davon stark beeinflusst wird. Die Reaktion auf P-Limitationen änderte sich während der ontogenetischen Entwicklung wobei ältere Stadien weniger stark beeinträchtigt wurden. Da Nährstofflimitation die Kondition und die Reproduktion von Primärkonsumenten negativ beeinflusst, führt dies durch Reduktion der zu Verfügung stehenden Futtermenge zu einem Quantitätseffekt bei höheren trophischen Ebenen. Die Wirkung von Quantitäts – und Qualitätseffekten wurde in Kombination auf einen Top-Prädatoren in einem Experiment mit Hummerlarven untersucht. Die Larven wurden durch die geringe Menge an Nährstoffen sogar bei sehr geringer Futtermenge beeinträchtigt. Das ist ein Hinweis, dass die Futterqualität eine entscheidendere Rolle spielt als die Quantität. Eine der großen Herausforderungen für zukünftige ökologische Untersuchungen im marinen Bereich wird es sein, die relative Bedeutung von Qualität und Quantität aufzuschlüsseln. Die Ergebnisse der vorliegenden Studie sollten weitreichende Konsequenzen für das Verständnis von trophischen Interaktionen und der Populationsdynamik mariner Organismen haben

Food Quality Affects Secondary Consumers Even at Low Quantities: An Experimental Test with Larval European Lobster

The issues of food quality and food quantity are crucial for trophic interactions. Although most research has focussed on the primary producer – herbivore link, recent studies have shown that quality effects at the bottom of the food web propagate to higher trophic levels. Negative effects of poor food quality have almost exclusively been demonstrated at higher food quantities. Whether these negative effects have the same impact at low food availability in situations where the majority if not all of the resources are channelled into routine metabolism, is under debate. In this study a tri-trophic food chain was designed, consisting of the algae Rhodomonas salina, the copepod Acartia tonsa and freshly hatched larvae of the European lobster Homarus gammarus. The lobster larvae were presented with food of two different qualities (C∶P ratios) and four different quantities to investigate the combined effects of food quality and quantity. Our results show that the quality of food has an impact on the condition of lobster larvae even at very low food quantities. Food with a lower C∶P content resulted in higher condition of the lobster larvae regardless of the quantity of food. These interacting effects of food quality and food quantity can have far reaching consequences for ecosystem productivity

Increased carbon dioxide availability alters phytoplankton stoichiometry and affects carbon cycling and growth of a marine planktonic herbivore

Rising levels of CO2 in the atmosphere have led to increased CO2 concentrations in the oceans. This enhanced carbon availability to the marine primary producers has the potential to change their nutrient stoichiometry, and higher carbon to nutrient ratios are expected. As a result, the quality of the primary producers as food for herbivores may change. Here, we present experimental work showing the effect of feeding Rhodomonas salina grown under different pCO2 (200, 400 and 800 µatm) on the copepod Acartia tonsa. The rate of development of copepodites decreased with increasing CO2 availability to the algae. The surplus carbon in the algae was excreted by the copepods, with younger stages (copepodites) excreting most of their surplus carbon through respiration, and adult copepods excreting surplus carbon mostly as DOC. We consider the possible consequences of different excretory pathways for the ecosystem. A continued increase in the CO2 availability for primary production, together with changes in the nutrient loading of coastal ecosystems, may cause changes in the trophic links between primary producers and herbivores

Food web effects of ocean acidification

Increased CO2 availability to primary producers changes the nutrient stoichiometry of these organisms. As a result, the quality of the primary producers as food for herbivores is affected. Here, we present experimental work showing that the copepod Acartia tonsa feeding on differently grown Rhodomonas salina is indeed affected by the CO2 availability to the algae. We discuss the potential pathways of excreting the carbon that is in excess in high CO2 algae, and consider the possible consequences of different excretory pathways for the ecosystem. Most likely, a continued increase in the CO2 availability for primary production, together with changes in the nutrient loading of coastal ecosystems will cause strong changes in the trophic link between primary producers and herbivores, which in turn will have consequences to higher trophic levels

Dietary and seasonal variability in trophic relations at the base of the North Sea pelagic food web revealed by stable isotope and fatty acid analysis

A two-dimensional biomarker approach including fatty acids and stable isotopes of seston and copepods was applied to examine how the variability at the base of the food web affects trophic interactions between primary producers and copepod consumers over a sampling period of two years. We investigated how the composition of the seston affected feeding behaviour by analysing the fatty acid and stable isotope signals of the copepods Calanus helgolandicus, Acartia spp., Centropages spp. and Temora longicornis at Helgoland Roads, North Sea. Our results indicate that the relative contributions of autotrophic and heterotrophic fractions in the seston determined the stable isotope signal of the seston and hence the δ15N of copepods. Our findings show that the combination of stable isotope and fatty acid analyses provides an ideal tool to address the complexity of trophic relations in planktonic food-webs and to define relative trophic position and feeding preferences of e.g. copepods. Defining accurate baselines from bulk seston samples containing a mixture of auto- and heterotroph protist communities still remains a challenge when defining lower food-web dynamics in natural plankton communities.Dietary and seasonal variability in trophic relations at the base of the North Sea pelagic food web revealed by stable isotope and fatty acid analysisacceptedVersio

The reaction of European lobster larvae (Homarus gammarus) to different quality food: effects of ontogenetic shifts and pre-feeding history

Young larval stages of many organisms represent bottlenecks in the life-history of many species. The high mortality commonly observed in, for example, decapod larvae has often been linked to poor nutrition, with most studies focussing on food quantity. Here, we focus instead on the effects of quality and have investigated its effects on the nutritional condition of lobster larvae. We established a tri-trophic food chain consisting of the cryptophyte Rhodomonas salina, the calanoid copepod Acartia tonsa and larvae of the European lobster Homarus gammarus. In a set of experiments, we manipulated the C:N:P stoichiometry of the primary producers, and accordingly those of the primary consumer. In a first experiment, R. salina was grown under N- and P-limitation and the nutrient content of the algae was manipulated by addition of the limiting nutrient to create a food quality gradient. In a second experiment, the effect on lobster larvae of long- and short-term exposure to food of varying quality during ontogenetic development was investigated. The condition of the lobster larvae was negatively affected even by subtle N- and P-nutrient limitations of the algae. Furthermore, younger lobster larvae were more vulnerable to nutrient limitation than older ones, suggesting an ontogenetic shift in the capacity of lobster larvae to cope with low quality food. The results presented here might have substantial consequences for the survival of lobster larvae in the field, as, in the light of future climate change and re-oligotrophication of the North Sea, lobster larvae might face marked changes in temperature and nutrient conditions, thus significantly altering their condition and growth

Direct and indirect effects of elevated CO2 are revealed through shifts in phytoplankton, copepod development, and fatty acid accumulation.

Change in the nutritional quality of phytoplankton is a key mechanism through which ocean acidification can affect the function of marine ecosystems. Copepods play an important role transferring energy from phytoplankton to higher trophic levels, including fatty acids (FA)-essential macronutrients synthesized by primary producers that can limit zooplankton and fisheries production. We investigated the direct effects of pCO2 on phytoplankton and copepods in the laboratory, as well as the trophic transfer of effects of pCO2 on food quality. The marine cryptophyte Rhodomonas salina was cultured at 400, 800, and 1200 μatm pCO2 and fed to adult Acartia hudsonica acclimated to the same pCO2 levels. We examined changes in phytoplankton growth rate, cell size, carbon content, and FA content, and copepod FA content, grazing, respiration, egg production, hatching, and naupliar development. This single-factor experiment was repeated at 12°C and at 17°C. At 17°C, the FA content of R. salina responded non-linearly to elevated pCO2 with the greatest FA content at intermediate levels, which was mirrored in A. hudsonica; however, differences in ingestion rate indicate that copepods accumulated FA less efficiently at elevated pCO2. A. hudsonica nauplii developed faster at elevated pCO2 at 12°C in the absence of strong food quality effects, but not at 17°C when food quality varied among treatments. Our results demonstrate that changes to the nutritional quality of phytoplankton are not directly translated to their grazers, and that studies that include trophic links are key to unraveling how ocean acidification will drive changes in marine food webs