Ursula Gaedke

Lake ecosystems: Rapid evolution revealed by dormant eggs

Natural selection can lead to rapid changes in organisms, which can in turn influence ecosystem processes. A key factor in the functioning of lake ecosystems is the rate at which primary producers are eaten, and major consumers, such as the zooplankton Daphnia, can be subject to strong selection pressures when phytoplankton assemblages change. Lake Constance in central Europe experienced a period of eutrophication (the biological effects of an input of plant nutrients) during the 1960s–70s, which caused an increase in the abundance of nutritionally poor or even toxic cyanobacteria. By hatching long-dormant eggs of Daphnia galeata found in lake sediments, we show that the mean resistance of Daphnia genotypes to dietary cyanobacteria increased significantly during this eutrophication. This rapid evolution of resistance has implications for the ways that ecosystems respond to nutrient enrichment through the impact of grazers on primary production.

NATURAL SELECTION FOR GRAZER RESISTANCE TO TOXIC CYANOBACTERIA: EVOLUTION OF PHENOTYPIC PLASTICITY?

Abstract We studied the selection response of the freshwater grazing zooplankter, Daphnia galeata, to increased abundance of cyanobacteria in its environment. Cyanobacteria are a poor‐quality and often toxic food. Distinct genotypes of D. galeata were hatched from diapausing eggs extracted from three time horizons in the sediments of Lake Constance, Europe, covering the period 1962 to 1997, a time of change in both the prevalence of planktonic cyanobacteria and levels of phosphorus pollution. We assessed whether the grazers evolved to become more resistant to dietary cyanobacteria by exposing genetically distinct clones to two diets, one composed only of the nutritious green alga, Scenedesmus obliquus (good food), and the other a mixture of S. obliquus and the toxic cyanobacterium Microcystis aeruginosa (poor food). Genotype performance was measured as the specific rate of weight gain from neonate to maturity (gj).

Mixotrophs combine resource use to outcompete specialists: Implications for aquatic food webs

The majority of organisms can be grouped into those relying solely on photosynthesis (phototrophy) or those relying solely on the assimilation of organic substances (heterotrophy) to meet their requirements for energy and carbon. However, a special life history trait exists in which organisms combine both phototrophy and heterotrophy. Such “mixotrophy” is a widespread phenomenon in aquatic habitats and is observed in many protozoan and metazoan organisms. The strategy requires investment in both photosynthetic and heterotrophic cellular apparatus, and the benefits must outweigh these costs. In accordance with mechanistic resource competition theory, laboratory experiments revealed that pigmented mixotrophs combined light, mineral nutrients, and prey as substitutable resources. Thereby, they reduced prey abundance below the critical food concentration of competing specialist grazers [Rothhaupt, K. O. (1996) Ecology 77, 716–724]. Here, we demonstrate the important consequences of this strategy for an aquatic community. In the illuminated surface strata of a lake, mixotrophs reduced prey abundance steeply. The data suggest that, as a consequence, grazers from higher trophic levels, consuming both the mixotrophs and their prey, could not persist. Thus, the mixotrophs escaped from competition with and losses to higher grazers. Furthermore, the mixotrophs structured prey abundance along the vertical light gradient, creating low densities near the surface and a pronounced maximum of their algal prey at depth. Such deep algal accumulations are typical features of nutrient-poor aquatic habitats, previously explained by resource availability. We hypothesize instead that the mixotrophic grazing strategy is responsible for deep algal accumulations in many aquatic environments.

Challenges and Opportunities for Integrating Lake Ecosystem Modelling Approaches

A large number and wide variety of lake ecosystem models have been developed and published during the past four decades. We identify two challenges for making further progress in this field. One such challenge is to avoid developing more models largely following the concept of others (‘reinventing the wheel’). The other challenge is to avoid focusing on only one type of model, while ignoring new and diverse approaches that have become available (‘having tunnel vision’). In this paper, we aim at improving the awareness of existing models and knowledge of concurrent approaches in lake ecosystem modelling, without covering all possible model tools and avenues. First, we present a broad variety of modelling approaches. To illustrate these approaches, we give brief descriptions of rather arbitrarily selected sets of specific models. We deal with static models (steady state and regression models), complex dynamic models (CAEDYM, CE-QUAL-W2, Delft 3D-ECO, LakeMab, LakeWeb, MyLake, PCLake, PROTECH, SALMO), structurally dynamic models and minimal dynamic models. We also discuss a group of approaches that could all be classified as individual based: super-individual models (Piscator, Charisma), physiologically structured models, stage-structured models and trait-based models. We briefly mention genetic algorithms, neural networks, Kalman filters and fuzzy logic. Thereafter, we zoom in, as an in-depth example, on the multi-decadal development and application of the lake ecosystem model PCLake and related models (PCLake Metamodel, Lake Shira Model, IPH-TRIM3D-PCLake). In the discussion, we argue that while the historical development of each approach and model is understandable given its ‘leading principle’, there are many opportunities for combining approaches. We take the point of view that a single ‘right’ approach does not exist and should not be strived for. Instead, multiple modelling approaches, applied concurrently to a given problem, can help develop an integrative view on the functioning of lake ecosystems. We end with a set of specific recommendations that may be of help in the further development of lake ecosystem models.

SPECTRAL ANALYSIS UNMASKS SYNCHRONOUS AND COMPENSATORY DYNAMICS IN PLANKTON COMMUNITIES

Community biomass is often less variable than the biomasses of populations within the community, yet attempts to implicate compensatory dynamics between populations as a cause of this relationship often fail. In part, this may be due to the lack of appropriate metrics for variability, but there is also great potential for large-scale processes such as seasonality or longer-term environmental change to obscure important dynamics at other temporal scales. In this study, we apply a scale-resolving method to long-term plankton data, to identify the specific temporal scales at which community-level variability is influenced by synchrony or compensatory dynamics at the population level. We show that variability at both the population and community level is influenced strongly by a few distinct temporal scales: in phytoplankton, ciliate, rotifer, and crustacean communities, synchronous dynamics are predominant at most temporal scales. However, in phytoplankton and crustacean communities, compensatory dynamics occur at a sub-annual scale (and at the annual scale in crustaceans) leading to substantial reductions in community-level variability. Aggregate measures of population and community variability do not detect compensatory dynamics in these communities; thus, resolving their scale dependence unmasks dynamics that are important for community stability in this system. The methods and results presented herein will ultimately lead to a better understanding of how stability is achieved in communities.

Interplay between energy limitation and nutritional deficiency: Empirical data and food web models

Food quality may play an important role in consumer population dynamics. The frequently large differences in elemental and biochemical composition observed be- tween autotrophs and their grazers suggest that food quality may be of particular importance for herbivores. Under nutrient-depleted conditions the carbon-to-nutrient ratios of auto- trophs can increase to such an extent that consumers become nutrient rather than energy limited. Estimating the importance of this effect in situ in pelagic food webs is complicated by the omnivory of many consumers and by rapid nutrient recycling. Isolated predator- prey studies inadequately represent this interaction; instead, an ecosystem perspective is required. We used seven years of data from large, deep Lake Constance to develop seasonally resolved flux models of the pelagic food web and analyzed the balance between energy and nutrient constraints. The carbon (C) and phosphorus (P) flows were simultaneously quantified and balanced. C represented food quantity/energy. P was taken as a surrogate of food quality, because algal C:P ratios exceeded the threshold above which P limitation of herbivores is predicted by stoichiometric theory throughout summer and autumn. Primary production exceeded bacterial C production by a factor of 3, but autotrophs and bacteria took up approximately equal amounts of P during summer and autumn. As a consequence, the C and P supplies of suspension-feeding zooplankton were decoupled: Consumer C demands were largely met by phytoplankton whereas P was mostly obtained from bacteria and their protist predators. The degree of consumer P deficiency varied according to supplementation of their algal diet with P-enriched bacteria or bacterivores. This favored the occurrence of omnivores, i.e., organisms that minimized P deficiencies at the cost of enhanced energy limitation. In contrast with previous perceptions, P reminer- alization during P-depleted summer conditions was dominated by bacterivorous flagellates, carnivorous crustaceans, and fish, which fed on prey with an elemental composition similar to their own, whereas herbivores contributed only 30% of P cycling despite their large biomass and C production. Our results suggested a co-limitation of predominantly herbiv- orous consumers by C and P and a mutual dependence of the two types of deficiency at the individual and system level. This pattern is not specific to pelagic systems but appears to be applicable across ecosystem types.

The first decade of oligotrophication of Lake Constance

In Lake Constance, after several decades of cutrophication, a decrease in phosphorus loading over the last decade has lead to a partial recovery from eutrophication. Here we analyse the shift in the taxonomic composition of phytoplankton during the first decade of oligotrophication in Lake Constance. During the 1980s, spring total P concentrations decreased from ca. 130 to less than 50 μ·l−1. This decrease was reflected by an approximately proportional decrease in summer phytoplankton biomass while spring phytoplankton biomass seemed unresponsive. Major taxonomic changes occured during both growth seasons. In spring, the proportion of diatoms, green algae and Chrysophyta increased while the proportion of Cryptophyta decreased. The summer trend was very different: the relative importance of diatoms decreased and Cryptophyta and Chrysophyta increased, while Chlorophyta reached their peak around 1985. These trends are also analysed at the genus level. Comparison with taxonomic trends during the eutrophication period shows the expected reversals in most cases. Comparison with other lakes shows general similarities, with the notable exception that Planktothrix rubescens has never been important in Lake Constance. The increase of diatoms during spring is attributed to their improved competitive performance with increasing Si:P ratios. Their decrease during summer is explained by the increasing silicate removal from the epilimnion by increasing spring populations.

Seasonal changes of trophic transfer efficiencies in a plankton food web derived from biomass size distributions and network analysis

Abstract The trophic transfer efficiencies in the planktonic food web of large, deep, and mesoeutrophic Lake Constance were derived independently from biomass size distributions and from mass-balanced carbon flow diagrams based on comprehensive data for biomass, production, and food web structure. The main emphasis was on the transfer of primary production to herbivores since this process dominates the flow of matter within the food web. Biomass size distributions offer an ecosystem approach which relies only on measurements of biomass and a few general assumptions, whereas network analysis is predominantly based on production estimates and requires more detailed knowledge of the ecosystem. Despite these differences, both approaches give consistent results for both the absolute values of the transfer efficiencies and seasonal trends. Estimates of the seasonally averaged transfer efficiency (dominated by the utilization of primary production by herbivores) range from 0.20 to 0.27. They are considerably lower in late winter and spring (0.05 to 0.21) than in summer and autumn (0.25 to 0.38, extreme values: 0.20 and 0.42).

Strong vertical differences in the plankton composition of an extremely acidic lake

Vertical differences in food web structure were examined in an extremely acidic, iron-rich mining lake in Germany (Lake 111; pH 2.6, total Fe 150 mg L -1 ) during the period of stratification. We tested whether or not the seasonal variation of the plankton composition is less pronounced than the differences observed over depth. The lake was strongly stratified in summer, and concentrations of dissolved organic carbon and inorganic carbon were consistently low in the epilimnion but high in the hypolimnion. Oxygen concentrations declined in the hypolimnion but were always above 2 mg L -1 . Light attenuation did not change over depth and time and was governed by dissolved ferric iron. The plankton consisted mainly of single-celled and filamentous bacteria, the two mixotrophic flagellates Chlamydomonas sp. and Ochromonas sp., the two rotifer species Elosa worallii and Cephalodella hoodi, and Heliozoa as top predators. We observed very few ciliates and rhizopods, and no heterotrophic flagellates, crustaceans or fish. Ochromonas sp., bacterial filaments, Elosa and Heliozoa dominated in the epilimnion whereas Chlamydomonas sp., single-celled bacteria and Cephalodella dominated in the hypolimnion. Single-celled bacteria were controlled by Ochromonas sp. whereas the lack of large consumers favoured a high proportion of bacterial filaments. The primarily phototrophic Chlamydomas sp. was limited by light and CO 2 and may have been reduced due to grazing by Ochromonas sp. in the epilimnion. The distribution of the primarily phagotrophic Ochromonas sp. and of the animals seemed to be controlled by prey availability. Differences in the plankton composition were much higher between the epilimnion and hypolimnion than within a particular stratum over time. The food web in Lake 111 was extremely species-poor enabling no functional redundancy. This was attributed to the direct exclusion of species by the harsh environmental conditions and presumably enforced by competitive exclusion. The latter was promoted by the low diversity at the first trophic level which, in turn was attributed to relatively stable growth conditions and the independence of resource availability (inorganic carbon and light) from algal density. Ecological theory suggests that low functional redundancy promotes low stability in ecosystem processes which was not supported by our data.

Trophic structure and carbon flow dynamics in the pelagic community of a large lake

Understanding the flow and cycling of matter within food webs is a major objective of contemporary ecosystem research (e.g., Wulff et al. (1989) and literature cited therein). A number of investigations on carbon (C) cycling in pelagic ecosystems focused on the role of the microbial loop (e.g., Ducklow et al. (1986), Jackson and Eldridge (1992), and Stone et al. (1993)). The present case study from large and deep Lake Constance aims to contribute to this partially controversial issue by evaluating separately the contribution of the microbial community to the nutrition of large zooplankton (i.e., the link-sink issue), and to the overall C flow dynamics. This is done by aggregating all species from the entire food web into two separate chains, one based directly on phytoplankton (called grazing chain in the following), and one relying energetically on dead organic matter taken up by osmotrophic bacteria (detritus chain). The organismal composition and the relative quantitative significance of both chains will be compared. Perceiving the food web as being composed of these two chains approximates the concept of distinguishing between a classical pelagic food chain (going from phytoplankton via crustaceans to fish) and a microbial loop. However, in contrast to the latter concept, we account explicitly for flows into and from the pool of dead organic material. Second, we do not allocate each plankton group to one of the chains entirely but compute the fractional contribution of each group to both chains according to its diet composition. For example, ciliates belong mostly to the grazing chain as they are predominantly herbivorous. However, additional grazing on bacteria and flagellates results in the allocation of some ciliate fraction to the detritus chain.