Norbert Kamjunke

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.

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.

ALGAE AS COMPETITORS FOR GLUCOSE WITH HETEROTROPHIC BACTERIA

Dissolved organic carbon (DOC) constitutes the bulk of organic carbon in aquatic environments. The importance of DOC utilization by mixotrophic algae is unclear since heterotrophic bacteria are regarded as more efficient users. We tested the hypothesis that algae decrease the DOC concentration in the light to lower levels than in darkness resulting in competitive exclusion of heterotrophic bacteria according to the mechanistic competition theory. We investigated (a) the uptake kinetics of glucose as a model substrate by two cultured algae and mixed bacteria populations, (b) the competition for glucose between algae and bacteria in chemostats, (c) the effect of discontinuous glucose supply in chemostats, and (d) the minimum glucose concentrations achieved in cultures of algae and bacteria. Bacteria showed higher specific‐glucose‐uptake rates than algae. In chemostats, algae became extinct in the dark and coexisted in the light where they decreased bacteria to lower densities. Discontinuous glucose supply promoted the algae compared to continuous substrate addition. Several algae consumed glucose to lower concentrations in the dark than in the light and showed lower or equal residual glucose concentrations than bacteria. Residual concentrations were not related to allometric traits (cell volume) and photosynthetic potential (chl content). Overall, the hypothesis was not supported, and mechanisms of competition for DOC obviously differed from those for particulate prey. However, since some algae showed lower or equal residual glucose concentrations than bacteria, algal dark uptake of DOC may be important in deep layers of many waters.

Bacteria ingestion by Daphnia galeata in a biomanipulated reservoir: a mechanism stabilizing biomanipulation?

We determined clearance rates and ingestion rates of Daphnia galeata on bacteria and phytoplankton in order to test if bacteria are an important alternative food resource for daphnids during periods of low phytoplankton biomass in the biomanipulated Bautzen reservoir (Germany). D. galeata was able to feed on bacteria with the same efficiency as on algae during most of the time. In spite of similar clearance rates, bacteria ingestion was usually lower than phytoplankton ingestion due to lower bacterial biomass. Only at low biomass of algae in late fall and during the clear water phase, bacteria contributed up to 87% and 42%, respectively, to total carbon ingestion of D. galeata. However, even a short period of relatively high bacteria grazing by daphnids may be important for biomanipulation. Bacteria might bridge over periods of food limitation of daphnids thus promoting the maintenance of high Daphnia biomass. Therefore, ingestion of bacteria by daphnids is thought to stabilize biomanipulation and may hold a key position in the food web of biomanipulated lakes.

The Bode hydrological observatory: a platform for integrated, interdisciplinary hydro-ecological research within the TERENO Harz/Central German Lowland Observatory

This article provides an overview about the Bode River catchment that was selected as the hydrological observatory and main region for hydro-ecological research within the TERrestrial ENvironmental Observatories Harz/Central German Lowland Observatory. It first provides information about the general characteristics of the catchment including climate, geology, soils, land use, water quality and aquatic ecology, followed by the description of the interdisciplinary research framework and the monitoring concept with the main components of the multi-scale and multi-temporal monitoring infrastructure. It also shows examples of interdisciplinary research projects aiming to advance the understanding of complex hydrological processes under natural and anthropogenic forcings and their interactions in a catchment context. The overview is complemented with research work conducted at a number of intensive research sites, each focusing on a particular functional zone or specific components and processes of the hydro-ecological system.

Utilisation of terrestrial carbon by osmotrophic algae

Abstract.Terrestrial-derived dissolved organic carbon (DOC) contributes significantly to the energetic basis of many aquatic food webs. Although heterotrophic bacteria are generally considered to be the sole consumers of DOC, algae and cyanobacteria of various taxonomic groups are also capable of exploiting this resource. We tested the hypothesis that algae can utilise DOC in the presence of bacteria if organic resources are supplied in intervals by photolysis of recalcitrant DOC. In short-term uptake experiments, we changed irradiation in the range of minutes. As model substrates, polymers of radiolabelled coumaric acid (PCA) were used, which during photolysis are known to release aromatic compounds comparable to terrestrial-derived and refractory DOC. Three cultured freshwater algae readily assimilated PCA photoproducts equivalent to a biomass-specific uptake of 5–60% of the bacterial competitors present. Algal substrate acquisition did not depend on whether PCA was photolysed continuously or in intervals. However, the data show that photoproducts of terrestrial DOC can be a significant resource for osmotrophic algae. In long-term growth experiments, interval light was applied one hour per day. We allowed cultured Chlamydomonas to compete for ambient DOC of low concentration. We found higher abundances of Chlamydomonas when cultures were irradiated intermittently rather than continuously. These data suggest that photolysis of DOC supports algal heterotrophy, and potentially facilitates growth, when light fluctuations are large, as during the diurnal light cycle. We concluded that osmotrophic algae can efficiently convert terrestrial carbon into the biomass of larger organisms of aquatic food webs.

Quality of dissolved organic matter affects planktonic but not biofilm bacterial production in streams.

Streams and rivers are important sites of organic carbon mineralization which is dependent on the land use within river catchments. Here we tested whether planktonic and epilithic biofilm bacteria differ in their response to the quality of dissolved organic carbon (DOC). Thus, planktonic and biofilm bacterial production was compared with patterns of DOC along a land-use gradient in the Bode catchment area (Germany). The freshness index of DOC was positively related to the proportion of agricultural area in the catchment. The humification index correlated with the proportion of forest area. Abundance and production of planktonic bacteria were lower in headwaters than at downstream sites. Planktonic production was weakly correlated to the total concentration of DOC but more strongly to quality-measures as revealed by spectra indexes, i.e. positively to the freshness index and negatively to the humification index. In contrast to planktonic bacteria, abundance and production of biofilm bacteria were independent of DOC quality. This finding may be explained by the association of biofilm bacteria with benthic algae and an extracellular matrix which represent additional substrate sources. The data show that planktonic bacteria seem to be regulated at a landscape scale controlled by land use, whereas biofilm bacteria are regulated at a biofilm matrix scale controlled by autochthonous production. Thus, the effects of catchment-scale land use changes on ecosystem processes are likely lower in small streams dominated by biofilm bacteria than in larger streams dominated by planktonic bacteria.

Utilisation of dissolved organic carbon from different sources by pelagic bacteria in an acidic mining lake

We compared growth rates and efficiencies of pelagic bacteria from an extremely acidic mining lake (pH 2.6, mean depth 4.6 m) supplied with different sources of carbon: (1) excreted by phytoplankton, (2) derived from benthic algae, (3) entering the lake via ground water, and (4) leached from leaf litter. Bacteria exhibited high growth rate and efficiency on exudates of pelagic and benthic algae. In contrast, they showed a lower growth rate and efficiency with organic carbon from ground water, and grew at a very high rate but a very low efficiency on leaf leachate. Results from stable isotope analyses indicate a greater importance of benthic exudates and leaf leachate for bacteria in the epilimnion, and a higher impact of ground water sources in the hypolimnion. Given the magnitude of differential source inputs into the lake, we suggest that benthic primary production was the most important carbon source for pelagic bacteria. The benthic-pelagic coupling seems to be more relevant in this shallow acidic lake with low pelagic carbon dioxide concentrations than in neutral lakes.

Tracing dissolved organic matter (DOM) from land-based aquaculture systems in North Patagonian streams.

Chile is the second largest producer of salmonids worldwide. The first step in the production of salmonids takes place in land-based aquacultures. However, the effects of the discharge from these aquacultures on stream dissolved organic matter (DOM) content, molecular composition and degradability are unknown. The aim of this study was thus to investigate the inputs of anthropogenic DOM from land-based aquaculture to the predominantly pristine river systems of North Patagonia. We hypothesized, that i) DOM exported from land-based aquaculture mainly consists of protein-like fluorescence (tyrosine and tryptophan) released from fish feces and food remains, and that ii) this DOM is highly degradable and therefore rapidly turned-over within the receiving streams. In the North Patagonian region we conducted a screening of ten land-based aquacultures and an intensive sampling campaign for one aquaculture. This was combined with longitudinal transects and a degradation experiment in order to couple the composition of DOM exported from land-based aquacultures to its degradability in streams. We measured dissolved organic carbon (DOC) concentration by high-temperature catalytic oxidation and DOM composition by fluorescence spectroscopy and parallel factor analysis. In the effluent of the ten screened aquacultures and in the repeated sampling of one aquaculture, we consistently found an increase of DOC concentrations and a dominance of protein-like fluorescence. The protein-like fluorescence rapidly disappeared downstream of the aquacultures, and in the degradation experiment. 21% of the DOC export from the repeatedly sampled aquaculture resulted from food addition and 76% from fish production. We conclude that large amounts of degradable DOM are exported from land-based aquacultures. This probably has strong effects on the ecological structure and function of North Patagonian streams, and similarly affected streams worldwide.

MIXOTROPHIC ALGAE CONSTRAIN THE LOSS OF ORGANIC CARBON BY EXUDATION1

Algae of various taxonomic groups are capable of assimilating dissolved organic carbon (DOC) from their environments (mixotrophy). Recently, we reported that, with increasing biomass of mixotrophs, heterotrophic bacteria did not increase. We hypothesized that algal uptake of external DOC may outweigh their release of DOC by exudation (H1). Here, we addressed an alternative hypothesis that algae did not assimilate external DOC but constrained the release of DOC (H2). In chemostat experiments, we cultured the mixotrophic Chlamydomonas acidophila Negoro together with heterotrophic bacteria. As external substrates, we used glucose, which was potentially available for both bacteria and algae, or fructose, which was available only for bacteria. We increased the biomass of algae by the stepwise addition of phosphorus. Bacterial biomass did not increase in experiments using glucose or when fructose was offered, suggesting that mechanisms other than algal mixotrophy (H1) kept concentrations of bacteria low. Measured exudation rates (percent extracellular release, PER) of mixotrophic algae (Cd. acidophila, Chlorella protothecoides W. Krüger) were very low and ranged between 1.0% and 3.5% at low and moderately high phosphorus concentrations. In contrast, an obligately phototrophic alga (Chlamydomonas segnis H. Ettl) showed higher exudation rates, particularly under phosphorus limitation (70%). The results support H2. If mixotrophy is considered as a mechanism to recycle organic exudates from near the cell surface, this would explain why algae retained mixotrophic capabilities although they cannot compete with bacteria for external organic carbon.