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Interplay between energy limitation and nutritional deficiency: Empirical data and food web models
(2002)
Due to differences in the biochemical composition of autotrophs and their grazers, food quality can strongly influence herbivore population dynamics. Under nutrient depleted conditions the carbon to nutrient ratios of autotrophs 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 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 analyze the balance between energetic 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 supply of suspension-feeding zooplankton was 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 remineralization 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 herbivorous 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.
1. The polyunsaturated fatty acid eicosapentaenoic acid (EPA) plays an important role in aquatic food webs, in particular at the primary producerconsumer interface where keystone species such as daphnids may be constrained by its dietary availability. Such constraints and their seasonal and interannual changes may be detected by continuous measurements of EPA concentrations. However, such EPA measurements became common only during the last two decades, whereas long-term data sets on plankton biomass are available for many well-studied lakes. Here, we test whether it is possible to estimate EPA concentrations from abiotic variables (light and temperature) and the biomass of prey organisms (e.g. ciliates, diatoms and cryptophytes) that potentially provide EPA for consumers. 2. We used multiple linear regression to relate size- and taxonomically resolved plankton biomass data and measurements of temperature and light intensity to directly measured EPA concentrations in Lake Constance during a whole year. First, we tested the predictability of EPA concentrations from the biomass of EPA-rich organisms (diatoms, cryptophytes and ciliates). Secondly, we included the variables mean temperature and mean light intensity over the sampling depth (020 m) and depth (08 and 820 m) as factors in our model to check for large-scale seasonal- and depth-dependent effects on EPA concentrations. In a third step, we included the deviations of light and temperature from mean values in our model to allow for their potential influence on the biochemical composition of plankton organisms. We used the Akaike Information Criterion to determine the best models. 3. All approaches supported our proposition that the biomasses of specific plankton groups are variables from which seston EPA concentrations can be derived. The importance of ciliates as an EPA source in the seston was emphasised by their high weight in our models, although ciliates are neglected in most studies that link fatty acids to seston taxonomic composition. The large-scale seasonal variability of light intensity and its interaction with diatom biomass were significant predictors of EPA concentrations. The deviation of temperature from mean values, accounting for a depth-dependent effect on EPA concentrations, and its interaction with ciliate biomass were also variables with high predictive power. 4. The best models from the first and second approaches were validated with measurements of EPA concentrations from another year (1997). The estimation with the best model including only biomass explained 80%, and the best model from the second approach including mean temperature and depth explained 87% of the variability in EPA concentrations in 1997. 5. We show that it is possible to predict EPA concentrations reliably from plankton biomass, while the inclusion of abiotic factors led to results that were only partly consistent with expectations from laboratory studies. Our approach of including biotic predictors should be transferable to other systems and allow checking for biochemical constraints on primary consumers.
Seasonal changes of the impact of daphnids on the plankton biomass size distribution, the biomass within individual size ranges, the average predator-prey weight ratios, and the efficiency to transfer matter and energy from small to large organisms are analyzed in large and deep Lake Constance based on comprehensive long-term observations. A comparison of daphnid biomass and production with those of other herbivorous groups (i. e. ciliates, rotifers, herbivorous crustaceans) reveals that in early spring daphnids play a minor role in relative and absolute values as compared to small fast growing ciliates. During this time, small algae and ciliates dominate which gives rise to a decreasing Sheldon-type size spectrum, low predator-prey weight ratios, and a low transfer efficiency along the size gradient. Around June, daphnids reach maximum abundances and become keystone species for the shape of the biomass size distribution, the food web structure, and the energy flow. They accumulate biomass in their size range one order of magnitude above the average. The slope of the normalized biomass size spectrum is less negative and positively correlated with daphnid biomass if the latter exceeds about 200 mg C/m2. This indicates a more efficient transfer along the size gradient with high predator-prey weight ratios and high trophic transfer efficiencies. The coefficients of determination of regression lines fitted to size distributions decrease with daphnid abundance, i. e. the size spectra become more irregular when daphnids dominate. In midsummer, daphnids lose their dominance and coexist with other herbivores (especially ciliates) in a highly diverse plankton community. The latter gives rise to a relatively smooth and almost flat Sheldon-type size distribution, lower predator-prey weight ratios, and a slightly reduced transfer efficiency along the size gradient. In late spring/early summer, negative relationships are found between daphnid biomass and the biomasses in the size ranges of autotrophic picoplankton, small phytoplankton, heterotrophic flagellates, and small and medium sized ciliates (0.06 - 32 pg C and 100-30,000 pg C). In mid- and late summer or on annual average, hardly any of these relationships existed. This cannot solely be attributed to lower daphnid abundance but points also to a more diverse control of small plankton organisms including nutrient limitation in summer. Ciliates influence the slope and shape of the size distribution much less than daphnids although they are at least of equal importance as daphnids in respect to herbivory and related fluxes in Lake Constance on annual average. The findings on the impact of daphnids on the energy flow within the plankton food web derived from size distributions are compared to, and are consistent with results obtained by mass-balanced carbon flow diagrams.
We investigated the response of the microbial components of the pelagic food web to re-oligotrophication of large, deep Lake Constance where total phosphorus concentrations during mixing decreased from a maximum of 2.81 mu mol L- 1 in 1979 via 1.87 mu mol L-1 in 1987 to 0.26 mu mol L-1 in 2007. Measurements of heterotrophic bacteria, autotrophic picoplankton (APP) and heterotrophic nanoflagellates (HNF) in 2006 and 2007 were compared to values from 1987 to 1997. We hypothesized that the biomass and seasonal variability of all groups will decrease under more oligotrophic conditions due to reduced resource availability, particularly for APP and HNF but less for the competitively stronger bacteria. Average bacterial biomass between spring and autumn was unrelated to phosphorus, whereas the ratio of bacterial biomass to chlorophyll a concentration increased with decreasing trophy due to declining chlorophyll concentrations. In contrast, a unimodal relationship was found between APP and phosphorus with low biomass at low and high phosphorus concentrations and maximum biomass in between. Average HNF biomass decreased strongly by a factor of 10-30 with decreasing trophy, and chlorophyll-specific HNF biomass was unimodally related to phosphorus. The relative seasonal biomass variability did not change for any group during re-oligotrophication. To conclude, HNF responded much more strongly and bacteria less so than chlorophyll concentrations to oligotrophication, whereas APP exhibited a more complex pattern.