Arne M. Malzahn

Differential effects of nutrient-limited primary production on primary, secondary or tertiary consumers

Nutritional imbalances between predator and prey are the rule rather than the exception at the lower end of food webs. We investigated the role of different grazers in the propagation of nutritionally imbalanced primary production by using the same primary producers in a three-trophic-level food chain and a four-trophic-level food chain experimental setup. The three-trophic-level food chain consisted of a classic single-cell primary producer (Rhodomonas salina), a metazoan grazer (the copepod Acartia tonsa) and a top predator (the jellyfish Gonionemus vertens), while we added a protozoan grazer (Oxyrrhis marina) as primary consumer to the food chain to establish the four-trophic-level food chain. This setup allowed us to investigate how nutrient-limitation effects change from one trophic level to another, and to investigate the performance of two components of our experimental food chains in different trophic positions. Stoichiometry and fatty acid profiles of the algae showed significant differences between the nutrient-depleted [no N and no P addition (−P), respectively] and the nutrient-replete (f/2) treatments. The differences in stoichiometry could be traced when O. marina was the first consumer. Copepods feeding on these flagellates were not affected by the nutritional imbalance of their prey in their stoichiometry, their respiration rates nor in their developmental rates. In contrast, when copepods were the primary consumer, those reared on the −P algae showed significantly higher respiration rates along with significantly lower developmental rates. In neither of our two experimental food chains did the signals from the base of the food chains travel up to jelly fish, our top predator.

The first occurrence of the ctenophore Mnemiopsis leidyi in the North Sea

After the discovery of large densities of Mnemiopsis leidyi in the Baltic Sea near Kiel by Javidpour et al. (First record of Mnemiopsis leidyi A. Agassiz 1865 in the Baltic Sea, 2006) in October 2006, we investigated the gelatinous zooplankton in the North Sea near Helgoland and recorded Mnemiopsis leidyi for the first time in the North Sea, albeit in much lower densities than those recorded in the Baltic Sea.

Recruitment variability in Baltic Sea sprat (Sprattus sprattus) is tightly coupled to temperature and transport patterns affecting the larval and early juvenile stages

Recruitment patterns of Baltic Sea sprat (Sprattus sprattus) were correlated to time series of (i) month- and depth-specific temperature conditions and (ii) larval drift patterns inferred from long-term Lagrangian particle simula- tions. From the latter, we derived an index that likely reflected the variable degree of annual larval transport from the central, deep spawning basins to the shallow coastal areas of the Baltic Sea. The drift index was significantly (P < 0.001) correlated to sprat recruitment success and explained, together with sprat spawning stock biomass, 82% of the overall variability between 1979 and 2003. Years of strong larval displacement towards southern and eastern Baltic coasts corresponded to relative recruitment failure, while years of retention within the deep basins were associated with relative recruitment success. The strongest correlation between temperature and recruitment occurred during August in surface waters, explaining 73% of the overall variability. Together, the two approaches advocate that new year classes of Baltic sprat are predominantly composed of individuals born late in the season and are determined in strength mainly by processes acting during the late larval and early juvenile stages. However, prior to be included in recruit- ment predictions, the biological mechanisms underlying these strong correlations may need to be better resolved.

Interspecific and nutrient-dependent variations in stable isotope fractionation: experimental studies simulating pelagic multitrophic systems

Stable isotope signatures of primary producers display high inter- and intraspecific variation. This is assigned to species-specific differences in isotope fractionation and variable abiotic conditions, e.g., temperature, and nutrient and light availability. As consumers reflect the isotopic signature of their food source, such variations have direct impacts on the ecological interpretation of stable isotope data. To elucidate the variability of isotope fractionation at the primary producer level and the transfer of the signal through food webs, we used a standardised marine tri-trophic system in which the primary producers were manipulated while the two consumer levels were kept constant. These manipulations were (1) different algal species grown under identical conditions to address interspecific variability and (2) a single algal species cultivated under different nutrient regimes to address nutrient-dependent variability. Our experiments resulted in strong interspecific variation between different algal species (Thalassiosira weissflogii, Dunaliella salina, and Rhodomonas salina) and nutrient-dependent shifts in stable isotope signatures in response to nutrient limitation of R. salina. The trophic enrichment in 15N and 13C of primary and secondary consumers (nauplii of Acartia tonsa and larval herring) showed strong deviations from the postulated degree of 1.0‰ enrichment in δ13C and 3.4‰ enrichment in δ15N. Surprisingly, nauplii of A. tonsa tended to keep “isotopic homeostasis” in terms of δ15N, a pattern not described in the literature so far. Our results suggest that the diets’ nutritional composition and food quality as well as the stoichiometric needs of consumers significantly affect the degree of trophic enrichment and that these mechanisms must be considered in ecological studies, especially when lower trophic levels, where variability is highest, are concerned.

Intraspecific selectivity, compensatory feeding and flexible homeostasis in the phagotrophic flagellate Oxyrrhis marina: three ways to handle food quality fluctuations

The phagotrophic flagellate Oxyrrhis marina shows a strong stoichiometric plasticity when fed differently grown Rhodomonas salina. We tested whether differently pre-conditioned O. marina displayed selective feeding behaviour from a mixture of nitrogen and phosphorus depleted R. salina. We observed selective feeding of O. marina, always selecting phosphorus rich R. salina independent of the pre-conditioning of the protists. In a second experiment, O. marina was again pre-conditioned either with nitrogen- or phosphorus-depleted R. salina and was refed with either of the differently limited R. salina in single food treatments (not in a mixture). The phagotrophic flagellate displayed compensatory feeding which means that O. marina feed more on the food source which they were not given before. Due to its stoichiometric plasticity, O. marina might handle bad quality food by following the stoichiometry of its prey and additionally by active selective feeding towards P-rich algae to enhance growth. Post-ingestion selection might as well be an important feature which means that ingested elements in excess are quickly excreted and scarce elements are ingested through accelerated food uptake.

Does the nutrient stoichiometry of primary producers affect the secondary consumer Pleurobrachia pileus

We investigated whether phosphorus limitations of primary producers propagate upwards through the food web, not only to the primary consumer level but also onto the secondary consumers’ level. A tri-trophic food chain was used to assess the effects of phosphorus-limited phytoplankton (the cryptophyte Rhodomonas salina) on herbivorous zooplankters (the copepod Acartia tonsa) and finally on zooplanktivores (the ctenophore Pleurobrachia pileus). The algae were cultured in phosphorus-replete and phosphorus-limited media before being fed to two groups of copepods. The copepods in turn were fed to the top predator, P. pileus, in a mixture resulting in a phosphorus-gradient, ranging from copepods having received only phosphorus-replete algae to copepods reared solely on phosphorus-limited algae. The C:P ratio of the algae varied significantly between the two treatments, resulting in higher C:P ratios for those copepods feeding on phosphorus-limited algae, albeit with a significance of 0.07. The differences in the feeding environment of the copepods could be followed to Pleurobrachia pileus. Contrary to our expectations, we found that phosphorus-limited copepods represented a higher quality food source for P. pileus, as shown by the better condition (expressed as nucleic acid content) of the ctenophore. This could possibly be explained by the rather high C:P ratios of ctenophores, their resulting low phosphorus demand and relative insensitivity to P deficiency. This might potentially be an additional explanation for the observed increasing abundances of gelatinous zooplankton in our increasingly phosphorus-limited coastal seas.

A New Approach to Homeostatic Regulation: Towards a Unified View of Physiological and Ecological Concepts

Stoichiometric homeostasis is the ability of an organism to keep its body chemical composition constant, despite varying inputs. Stoichiometric homeostasis therefore constrains the metabolic needs of consumers which in turn often feed on resources not matching these requirements. In a broader context, homeostasis also relates to the capacity of an organism to maintain other biological parameters (e.g. body temperature) at a constant level over ambient environmental variations. Unfortunately, there are discrepancies in the literature and ecological and physiological definitions of homeostasis are disparate and partly contradictory. Here, we address this matter by reviewing the existing knowledge considering two distinct groups, regulators and conformers and, based on examples of thermo- and osmoregulation, we propose a new approach to stoichiometric homeostasis, unifying ecological and physiological concepts. We suggest a simple and precise graphical way to identify regulators and conformers: for any given biological parameter (e.g. nutrient stoichiometry, temperature), a sigmoidal relation between internal and external conditions can be observed for conformers while an inverse sigmoidal response is characteristic of regulators. This new definition and method, based on well-studied physiological mechanisms, unifies ecological and physiological approaches and is a useful tool for understanding how organisms are affected by and affect their environment.

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.

Food chain effects of nutrient limitation in primary producers

The propagation of mineral limitation in primary producers to the second consumer level has rarely been investigated. Recently, it has been shown that limitation effects do travel up the food chain, not only quantitatively, but also qualitatively, and also that these quality effects affect the nutritional condition and growth of secondary consumers. The present study experimentally investigated the effect of phosphorus limitation in combination with fatty acid addition in primary producers (Scenedesmus obliquus) channelled through a primary consumer (Daphnia magna) on the condition of larval rainbow trout (Oncorhynchus mykiss). The C : P ratio and the fatty acid concentrations of the primary producers varied significantly with the phosphorus concentration of the culture media. These differences were also visible in the primary consumers (D. magna) feeding on the algae. The significantly different stoichiometry and fatty acid concentrations of the daphnids fed to larval trout did not lead to significant differences in growth, but the additional supplementation of fatty acid emulsions caused a significant increase in the condition of the fish. It was found that in the case of Daphnia as the primary prey for fish, with its relatively high phosphorus content even under phosphorus limitation, it is unlikely that phosphorus limitation affects fish condition and growth.

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.