Food quantity and quality together determine growth rates of consumers and the utilisation efficiencies of available resources in aquatic and terrestrial ecosystems. The effect of food quality on the performance of consumers is dependent on both, its direct influence on ingestion and assimilation rates, and on the behavioural and physiological adjustments of consumers to their food environment. The main target of this thesis was to investigate the nature and scope of behavioural and physiological adjustments in consumers and assess the resulting consequences for consumers’ fitness and ecosystem-wide nutrient flows.
In paper I, we investigated the extent of elemental homeostasis across several taxonomic groups of planktonic herbivores. We found that adjustments in elemental ratios (C:N:P) in body tissues are an important physiological response of heterotrophic flagellates, but that in ciliates and multi-cellular organisms C:N:P ratios varied much less than in their algal prey. Hence, alternative regulatory mechanisms determine the reactions of metazoan zooplankton to decreases in food quality. In paper II, we developed a theoretical model to explore regulation in behaviour and digestive physiology of consumers to changes in the food environment. Our results demonstrate that feeding and digestion of consumers are determined by trade-offs between benefits and costs of investments in these processes. We revealed that the flexibility in consumers’ behaviour and physiology had strong influences on assimilation rates and efficiencies and thereby affected growth rates and a wide range of ecosystem functions. In paper III, we investigated the scope and consequences of adjustments in feeding and assimilation rates of copepods exposed to different diets. An important finding was that consumers can use resources, which are available in surplus, to increase the uptake of a limiting nutrient. Such nutrient interconversion led to co-limitation, the simultaneous limitation of copepods by two different nutrients. Finally, in paper IV, we aimed to test the effect of food quality on population dynamics in the field. We investigated zooplankton populations in tropical soda-lakes, an environment with a surplus of planktonic food sources that thus provides an ideal setting for investigations of food quality. However, we found that the hatching of resting eggs from lake sediments was the main driver of zooplankton bloom formation resulting in non-cyclical dynamics that were not related to food quality.
These findings contributed to our understanding under which circumstance and by which mechanisms food quality affects the performance of consumers. My results highlight that food quality has not only direct effects on consumers’ growth but also triggers behavioral and physiological responses in consumers to maximize their fitness.
The analysis of functional groups with a resolution to the individual species level is a basic requirement to better understand complex interactions in aquatic food webs. Species-specific stable isotope analyses are currently applied to analyse the trophic role of large zooplankton or fish species, but technical constraints complicate their application to smaller-sized plankton. We investigated rotifer food assimilation during a short-term microzooplankton bloom in the East African soda lake Nakuru by developing a method for species-specific sampling of rotifers. The two dominant rotifers, Brachionus plicatilis and Brachionus dimidiatus, were separated to single-species samples (purity >95%) and significantly differed in their isotopic values (4.1 parts per thousand in delta C-13 and 1.5 parts per thousand in delta N-15). Bayesian mixing models indicated that isotopic differences were caused by different assimilation of filamentous cyanobacteria and particles A main difference was that the filamentous cyanobacterium Arthrospira fusiformis, which frequently forms blooms in African soda lakes, was an important food source for the larger-sized B.plicatilis (48%), whereas it was hardly ingested by B.dimidiatus. Overall, A.fusiformis was, relative to its biomass, assimilated to small extents, demonstrating a high grazing resistance of this species. In combination with high population densities, these results demonstrate a strong potential of rotifer blooms to shape phytoplankton communities and are the first in situ demonstration of a quantitatively important direct trophic link between rotifers and filamentous cyanobacteria.
Compound-specific isotope analyses (CSIA) of fatty acids (FA) constitute a promising tool for tracing energy flows in food-webs. However, past applications of FA-specific carbon isotope analyses have been restricted to a relatively coarse food-source separation and mainly quantified dietary contributions from different habitats. Our aim was to evaluate the potential of FA-CSIA to provide high-resolution data on within-system energy flows using algae and zooplankton as model organisms. First, we investigated the power of FA-CSIA to distinguish among four different algae groups, namely cyanobacteria, chlorophytes, haptophytes and diatoms. We found substantial within-group variation but also demonstrated that delta C-13 of several FA (e.g. 18:3 omega 3 or 18:4 omega 3) differed among taxa, resulting in group-specific isotopic fingerprints. Second, we assessed changes in FA isotope ratios with trophic transfer. Isotope fractionation was highly variable in daphnids and rotifers exposed to different food sources. Only delta C-13 of nutritionally valuable poly-unsaturated FA remained relatively constant, highlighting their potential as dietary tracers. The variability in fractionation was partly driven by the identity of food sources. Such systematic effects likely reflect the impact of dietary quality on consumers' metabolism and suggest that FA isotopes could be useful nutritional indicators in the field. Overall, our results reveal that the variability of FA isotope ratios provides a substantial challenge, but that FA-CSIA nevertheless have several promising applications in food-web ecology. This article is part of the theme issue 'The next horizons for lipids as 'trophic biomarkers': evidence and significance of consumer modification of dietary fatty acids'.
Food quantity-quality interactions determine growth rates and reproductive success of consumers and thereby regulate community dynamics and food web structure. Predator-prey models that shape our conceptual understanding of foraging ecology typically rely on the parametrization of fixed consumer responses to either food quantity or food quality. In nature, however, consumers optimize their fitness by responding simultaneously to changes in food quantity and quality. Therefore, we assessed consumer responses to changing food environments using a new fitness optimization model that accounted for food quality-quantity interactions to better capture the regulatory flexibility of consumers. Our simulations demonstrated that the impact of food quality on important consumer traits can be altered or even reversed by changes in food quality. Low food quality, for example, affected feeding rates negatively at low food concentrations but triggered surplus feeding at high food concentrations. The scope of surplus feeding was thereby mainly dependent on dynamics of nutrient digestion and in contrast to previous assumptions, energy costs of feeding played a minor role. Further, the regulation of digestive enzyme production, a crucial factor determining assimilation efficiencies, was strongly dependent on whether nonessential or essential nutrients were limiting growth. Consequently, not only the degree but also the type of nutrient limitation mediated the impact of the food environment on consumers' fitness. At the community level, food quality was key in shaping predator-prey biomass ratios. High food qualities resulted in top-heavy systems with larger consumer than prey biomass. Decreases of prey digestibility or the availability of essential nutrients, however, triggered a switch from inverted to classical pyramid shapes of bi-trophic systems. The impact of food quantity on trophic transfer and emerging structural ecosystem properties thus critically hinges on behavioral and physiological responses of consumers. The inclusion of the regulatory flexibility of consumers is therefore an essential next step to improve predator-prey models and our conceptual understanding of trophic interactions.
Zooplankton blooms are a frequent phenomenon in tropical systems. However, drivers of bloom formation and the contribution of emerging resting eggs are largely unexplored. We investigated the dynamics and the triggers of rotifer blooms in African soda-lakes and assessed their impact on other trophic levels. A meta-analysis of rotifer peak densities including abundances of up to 6 × 105 individuals L−1 demonstrated that rotifer bloom formation was uncoupled from the food environment and the seasonality of climatic conditions. A time series with weekly sampling intervals from Lake Nakuru (Kenya) revealed that intrinsic growth factors (food quality and the physicochemical environment) significantly affected rotifer population fluctuations, but were of minor importance for bloom formation. Instead, rotifer bloom formation was linked to sediment resuspension, a prerequisite for hatching of resting-eggs. Population growth rates exceed pelagic birth rates and simulations of rotifer dynamics confirmed the quantitative importance of rotifer emergence from the sediment egg-bank and signifying a decoupling of bloom formation from pelagic reproduction. Rotifer blooms led to a top-down control of small-sized algae and facilitated a switch to more grazing-resistant, filamentous cyanobacteria. This shift in phytoplankton composition cascaded up the food chain and triggered the return of filter-feeding flamingos. Calculations of consequent changes in the lake's energy budget and export of aquatic primary production to terrestrial ecosystems demonstrated the large potential impact of nonseasonal disturbances on the functioning of shallow tropical lakes.
Aquatic ecosystems experience large natural variation in elemental composition of carbon (C), nitrogen (N) and phosphorus (P), which is further enhanced by human activities. Primary producers typically reflect the nutrient ratios of their resource, whose stoichiometric composition can vary widely in conformity to environmental conditions. In contrast, C to nutrient ratios in consumers are largely constrained within a narrow range, termed homeostasis. In comparison to crustacean zooplankton, less is known about the ability of protozoan grazers and rotifer species to maintain stoichiometric balance. In this study, we used laboratory experiments with a primary producer (Nannochloropsis sp.), three different species of protozoan grazers and one mesozooplankton species: two heterotrophic dinoflagellates (Gyrodinium dominans and Oxyrrhis marina), a ciliate (Euplotes sp.) and a rotifer (Brachionus plicatilis) to test the stoichiometric response to five nutrient treatments. We showed that the dependency of zooplankton C: N: P ratios on C: nutrient ratios of their food source varies among species. Similar to the photoautotroph, the two heterotrophic dinoflagellates weakly regulated their internal stoichiometry. In contrast, the strength of stoichiometric regulation increased to strict homeostasis in both the ciliate and the rotifer, similar to crustacean zooplankton. Our study further shows that ciliate and rotifer growth can be constrained by imbalanced resource supply. It also indicates that these key primary consumers have the potential to trophically upgrade poor stoichiometric autotrophic food quality for higher trophic levels.
beta-N-Methylamino-l-alanine (BMAA), a neurotoxin reportedly produced by cyanobacteria, diatoms and dinoflagellates, is proposed to be linked to the development of neurological diseases. BMAA has been found in aquatic and terrestrial ecosystems worldwide, both in its phytoplankton producers and in several invertebrate and vertebrate organisms that bioaccumulate it. LC-MS/MS is the most frequently used analytical technique in BMAA research due to its high selectivity, though consensus is lacking as to the best extraction method to apply. This study accordingly surveys the efficiency of three extraction methods regularly used in BMAA research to extract BMAA from cyanobacteria samples. The results obtained provide insights into possible reasons for the BMAA concentration discrepancies in previous publications. In addition and according to the method validation guidelines for analysing cyanotoxins, the TCA protein precipitation method, followed by AQC derivatization and LC-MS/MS analysis, is now validated for extracting protein-bound (after protein hydrolysis) and free BMAA from cyanobacteria matrix. BMAA biological variability was also tested through the extraction of diatom and cyanobacteria species, revealing a high variance in BMAA levels (0.0080-2.5797 mu g g(-1) DW).
Soda lakes are simple in biodiversity, but due to their highly stochastic environmental dynamics unexpected shifts in species composition do occur. We studied key drivers for structuring phytoplankton communities and identified variables significantly influencing changes of Arthrospira fusiformis abundance in the Kenyan soda lakes, Nakuru and Bogoria. In both lakes, Arthrospira fusiformis dominated algal biomass, but in Nakuru, crashes of this taxon were recorded. The three variables sodium, pH and dry mass significantly contributed to the phytoplankton taxa pattern. Arthrospira was absent at highest turbidity and salinity levels, being outcompeted by the small, single-celled chlorophyte Picocystis salinarium. Picoplankton was in general connected to higher pH values and tended to occur anti-cyclic to Arthrospira. Overall, the abundance of A. fusiformis was influenced by the boundaries of habitat suitability, light penetration, grazers and cyanophages attacks.