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This study examines a natural, rapid, fivefold increase in dissolved organic carbon (DOC) concentrations in a temperate shallow lake, describing the processes by which increased DOC resulted in anoxic conditions and altered existing carbon cycling pathways. High precipitation for two consecutive years led to rising water levels and the flooding of adjacent degraded peatlands. Leaching from the flooded soils provided an initial increase in DOC concentrations (from a 2010 mean of 12 +/- 1 mg L-1 to a maximum concentration of 53 mg L-1 by June 2012). Increasing water levels, DOC, and phytoplankton concentrations reduced light reaching the sediment surface, eliminating most benthic primary production and promoting anoxia in the hypolimnion. From January to June 2012 there was a sudden increase in total phosphorus (from 57 mg L-1 to 216 mg L-1), DOC (from 24.6 mg L-1 to 53 mg L-1), and iron (from 0.12 mg L-1 to 1.07 mg L-1) concentrations, without any further large fluxes in water levels. We suggest that anoxic conditions at the sediment surface and flooded soils produced a dramatic release of these chemicals that exacerbated brownification and eutrophication, creating anoxic conditions that persisted roughly 6 months below a water depth of 1 m and extended periodically to the water surface. This brownification-anoxia feedback loop resulted in a near-complete loss of macroinvertebrate and fish populations, and increased surface carbon dioxide (CO2) emissions by an order of magnitude relative to previous years.
Ecological regime shifts and carbon cycling in aquatic systems have both been subject to increasing attention in recent years, yet the direct connection between these topics has remained poorly understood. A four-fold increase in sedimentation rates was observed within the past 50 years in a shallow eutrophic lake with no surface in-or outflows. This change coincided with an ecological regime shift involving the complete loss of submerged macrophytes, leading to a more turbid, phytoplankton-dominated state. To determine whether the increase in carbon (C) burial resulted from a comprehensive transformation of C cycling pathways in parallel to this regime shift, we compared the annual C balances (mass balance and ecosystem budget) of this turbid lake to a similar nearby lake with submerged macrophytes, a higher transparency, and similar nutrient concentrations. C balances indicated that roughly 80% of the C input was permanently buried in the turbid lake sediments, compared to 40% in the clearer macrophyte-dominated lake. This was due to a higher measured C burial efficiency in the turbid lake, which could be explained by lower benthic C mineralization rates. These lower mineralization rates were associated with a decrease in benthic oxygen availability coinciding with the loss of submerged macrophytes. In contrast to previous assumptions that a regime shift to phytoplankton dominance decreases lake heterotrophy by boosting whole-lake primary production, our results suggest that an equivalent net metabolic shift may also result from lower C mineralization rates in a shallow, turbid lake. The widespread occurrence of such shifts may thus fundamentally alter the role of shallow lakes in the global C cycle, away from channeling terrestrial C to the atmosphere and towards burying an increasing amount of C.
Kettle holes are small inland waters formed from glacially-created depressions often situated in agricultural landscapes. Due to their high perimeter-to-area ratio facilitating a high aquatic-terrestrial coupling, kettle holes can accumulate high concentrations of organic carbon and nutrients, fueling microbial activities and turnover rates. Thus, they represent hotspots of carbon turnover in the landscape, but their bacterial activities and controlling factors have not been well investigated. Therefore, we aimed to assess the relative importance of various environmental factors on bacterial and biogeochemical processes in the water column of kettle holes and to disentangle their variations. In the water body of ten kettle holes in north-eastern Germany, we measured several physico-chemical and biological parameters such as carbon quantity and quality, as well as bacterial protein production (BP) and community respiration (CR) in spring, early summer and autumn 2014. Particulate organic matter served as an indicator of autochthonous production and represented an important parameter to explain variations in BP and CR. This notion is supported by qualitative absorbance indices of dissolved molecules in water samples and C: N ratios of the sediments, which demonstrate high fractions of autochthonous organic matter (OM) in the studied kettle holes. In contrast, dissolved chemical parameters were less important for bacterial activities although they revealed strong differences throughout the growing season. Pelagic bacterial activities and dynamics might thus be regulated by autochthonous OM in kettle holes implying a control of important biogeochemical processes by internal primary production rather than facilitated exchange with the terrestrial surrounding due to a high perimeter-to-area ratio.
The sum of benthic autotrophic and bacterial production often exceeds the sum of pelagic autotrophic and bacterial production, and hence may contribute substantially to whole-lake carbon fluxes, especially in shallow lakes. Furthermore, both benthic and pelagic autotrophic and bacterial production are highly edible and of sufficient nutritional quality for animal consumers. We thus hypothesised that pelagic and benthic transfer efficiencies (ratios of production at adjacent trophic levels) in shallow lakes should be similar. We performed whole ecosystem studies in two shallow lakes (3.5ha, mean depth 2m), one with and one without submerged macrophytes, and quantified pelagic and benthic biomass, production and transfer efficiencies for bacteria, phytoplankton, epipelon, epiphyton, macrophytes, zooplankton, macrozoobenthos and fish. We expected higher transfer efficiencies in the lake with macrophytes, because these provide shelter and food for macrozoobenthos and may thus enable a more efficient conversion of basal production to consumer production. In both lakes, the majority of the whole-lake autotrophic and bacterial production was provided by benthic organisms, but whole-lake primary consumer production mostly relied on pelagic autotrophic and bacterial production. Consequently, transfer efficiency of benthic autotrophic and bacterial production to macrozoobenthos production was an order of magnitude lower than the transfer efficiency of pelagic autotrophic and bacterial production to rotifer and crustacean production. Between-lake differences in transfer efficiencies were minor. We discuss several aspects potentially causing the unexpectedly low benthic transfer efficiencies, such as the food quality of producers, pelagic-benthic links, oxygen concentrations in the deeper lake areas and additional unaccounted consumer production by pelagic and benthic protozoa and meiobenthos at intermediate or top trophic levels. None of these processes convincingly explain the large differences between benthic and pelagic transfer efficiencies. Our data indicate that shallow eutrophic lakes, even with a major share of autotrophic and bacterial production in the benthic zone, can function as pelagic systems with respect to primary consumer production. We suggest that the benthic autotrophic production was mostly transferred to benthic bacterial production, which remained in the sediments, potentially cycling internally in a similar way to what has previously been described for the microbial loop in pelagic habitats. Understanding the energetics of whole-lake food webs, including the fate of the substantial benthic bacterial production, which is either mineralised at the sediment surface or permanently buried, has important implications for regional and global carbon cycling.
Most studies of aquatic plankton focus on either macroscopic or microbial communities, and on either eukaryotes or prokaryotes. This separation is primarily for methodological reasons, but can overlook potential interactions among groups. Here we tested whether DNA metabarcoding of unfractionated water samples with universal primers could be used to qualitatively and quantitatively study the temporal dynamics of the total plankton community in a shallow temperate lake. Significant changes in the relative proportions of normalized sequence reads of eukaryotic and prokaryotic plankton communities over a 3-month period in spring were found. Patterns followed the same trend as plankton estimates measured using traditional microscopic methods. The bloom of a conditionally rare bacterial taxon belonging to Arcicella was characterized, which rapidly came to dominate the whole lake ecosystem and would have remained unnoticed without metabarcoding. The data demonstrate the potential of universal DNA metabarcoding applied to unfractionated samples for providing a more holistic view of plankton communities.
In aquatic systems, terrestrial dissolved organic matter (t-DOM) is known to stimulate bacterial activities in the water column, but simultaneous effects of autumnal leaf input on water column and sediment microbial dynamics in littoral zones of lakes remain largely unknown. The study's objective was to determine the effects of leaf litter on bacterial metabolism in the littoral water and sediment, and subsequently, the consequences for carbon cycling and food web dynamics. Therefore, in late fall, we simultaneously measured water and sediment bacterial metabolism in the littoral zone of a temperate shallow lake after adding terrestrial particulate organic matter (t-POM), namely, maize leaves. To better evaluate bacterial production (BP) and community respiration (CR) in sediments, we incubated sediment cores with maize leaves of different quality (nonleached and leached) under controlled laboratory conditions. Additionally, to quantify the incorporated leaf carbon into microbial biomass, we determined carbon isotopic ratios of fatty acids from sediment and leaf-associated microbes from a laboratory experiment using C-13-enriched beech leaves. The concentrations of dissolved organic carbon (DOC) increased significantly in the lake after the addition of maize leaves, accompanied by a significant increase in water BP. In contrast, sediment BP declined after an initial peak, showing no positive response to t-POM addition. Sediment BP and CR were also not stimulated by t-POM in the laboratory experiment, either in short-term or in long-term incubations, except for a short increase in CR after 18 hours. However, this increase might have reflected the metabolism of leaf-associated microorganisms. We conclude that the leached t-DOM is actively incorporated into microbial biomass in the water column but that the settling leached t-POM (t-POML) does not enter the food web via sediment bacteria. Consequently, t-POML is either buried in the sediment or introduced into the aquatic food web via microorganisms (bacteria and fungi) directly associated with t-POML and via benthic macroinvertebrates by shredding of t-POML. The latter pathway represents a benthic shortcut which efficiently transfers t-POML to higher trophic levels.
The fate of allochthonous dissolved organic carbon (DOC) in aquatic systems is primarily controlled by the turnover of heterotrophic bacteria. However, the roles that abiotic and biotic factors such as light and DOC release by aquatic primary producers play in the microbial decomposition of allochthonous DOC is not well understood. We therefore tested if light and autochthonous DOC additions would increase allochthonous DOC decomposition rates and change bacterial growth efficiencies and community composition (BCC). We established continuous growth cultures with different inocula of natural bacterial communities and alder leaf leachates (DOCleaf) with and without light exposure before amendment. Furthermore, we incubated DOCleaf together with autochthonous DOC from lysed phytoplankton cultures (DOCphyto). Our results revealed that pretreatments of DOCleaf with light resulted in a doubling of bacterial growth efficiency (BGE), whereas additions of DOCphyto or combined additions of DOCphyto and light had no effect on BGE. The change in BGE was not accompanied by shifts in the phylogenetic structure of the BCC, but BCC was influenced by the DOC source. Our results highlight that a doubling of BGE is not necessarily accompanied by a shift in BCC and that BCC is more strongly affected by resource properties.
The density of organisms declines with size, because larger organisms need more energy than smaller ones and energetic losses occur when larger organisms feed on smaller ones. A potential expression of density-size distributions are Normalized Biomass Size Spectra (NBSS), which plot the logarithm of biomass independent of taxonomy within bins of logarithmic organismal size, divided by the bin width. Theoretically, the NBSS slope of multi-trophic communities is exactly - 1.0 if the trophic transfer efficiency (TTE, ratio of production rates between adjacent trophic levels) is 10% and the predator-prey mass ratio (PPMR) is fixed at 10(4). Here we provide evidence from four multi-trophic lake food webs that empirically estimated TTEs correspond to empirically estimated slopes of the respective community NBSS. Each of the NBSS considered pelagic and benthic organisms spanning size ranges from bacteria to fish, all sampled over three seasons in 1 yr. The four NBSS slopes were significantly steeper than -1.0 (range -1.14 to -1.19, with 95% CIs excluding -1). The corresponding average TTEs were substantially lower than 10% in each of the four food webs (range 1.0% to 3.6%, mean 1.85%). The overall slope merging all biomass-size data pairs from the four systems (-1.17) was almost identical to the slope predicted from the arithmetic mean TTE of the four food webs (-1.18) assuming a constant PPMR of 10(4). Accordingly, our empirical data confirm the theoretically predicted quantitative relationship between TTE and the slope of the biomass-size distribution. Furthermore, we show that benthic and pelagic organisms can be merged into a community NBSS, but future studies have yet to explore potential differences in habitat-specific TTEs and PPMRs. We suggest that community NBSS may provide valuable information on the structure of food webs and their energetic pathways, and can result in improved accuracy of TTE-estimates.
Dissolved organic carbon (DOC) concentrations - mainly of terrestrial origin - are increasing worldwide in inland waters. Heterotrophic bacteria are the main consumers of DOC and thus determine DOC temporal dynamics and availability for higher trophic levels. Our aim was to study bacterial carbon (C) turnover with respect to DOC quantity and chemical quality using both allochthonous and autochthonous DOC sources. We incubated a natural bacterial community with allochthonous C (C-13-labeled beech leachate) and increased concentrations and pulses (intermittent occurrence of organic matter input) of autochthonous C (phytoplankton lysate). We then determined bacterial C consumption, activities, and community composition together with the C flow through bacteria using stable C isotopes. The chemical analysis of single sources revealed differences in aromaticity and low-and high-molecular-weight substance fractions (LMWS and HMWS, respectively) between allochthonous and autochthonous C sources. Both DOC sources (allochthonous and autochthonous DOC) were metabolized at a high bacterial growth efficiency (BGE) around 50%. In treatments with mixed sources, rising concentrations of added autochthonous DOC resulted in a further, significant increase in bacterial DOC consumption of up to 68% when nutrients were not limiting. This rise was accompanied by a decrease in the humic substance (HS) fraction and an increase in bacterial biomass. Changes in DOC concentration and consumption in mixed treatments did not affect bacterial community composition (BCC), but BCC differed in single vs. mixed incubations. Our study highlights that DOC quantity affects bacterial C consumption but not BCC in nutrient-rich aquatic systems. BCC shifted when a mixture of allochthonous and autochthonous C was provided simultaneously to the bacterial community. Our results indicate that chemical quality rather than source of DOC per se (allochthonous vs. autochthonous) determines bacterial DOC turnover.