Differential support of lake food webs by three types of terrestrial organic carbon

Organic carbon inputs from outside of ecosystem boundaries potentially subsidize recipient food webs. Four whole-lake additions of dissolved inorganic ¹³C were made to reveal the pathways of subsidies to lakes from terrestrial dissolved organic carbon (t-DOC), terrestrial particulate organic carbon (t-POC) and terrestrial prey items. Terrestrial DOC, the largest input, was a major subsidy of pelagic bacterial respiration, but little of this bacterial C was passed up the food web. Zooplankton received <2% of their C from the t-DOC to bacteria pathway. Terrestrial POC significantly subsidized the production of both zooplankton and benthic invertebrates, and was passed up the food web to Chaoborus and fishes. This route supplied 33–73% of carbon flow to zooplankton and 20–50% to fishes in non-fertilized lakes. Terrestrial prey, by far the smallest input, provided some fishes with >20% of their carbon. The results show that impacts of cross-ecosystem subsidies depend on characteristics of the imported material, the route of entry into the food web, the types of consumers present, and the productivity of the recipient system.     

How important are terrestrial organic carbon inputs for secondary production in freshwater ecosystems?

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The Influence of Hydrologic Residence Time on Lake Carbon Cycling Dynamics Following Extreme Precipitation Events

The frequency and magnitude of extreme events are expected to increase in the future, yet little is known about effects of such events on ecosystem structure and function. We examined how extreme precipitation events affect exports of terrestrial dissolved organic carbon (t-DOC) from watersheds to lakes as well as in-lake heterotrophy in three north-temperate lakes. Extreme precipitation events induced large influxes of t-DOC to our lakes, accounting for 45–58% of the seasonal t-DOC load. These large influxes of t-DOC influenced lake metabolism, resulting in lake net heterotrophy following 67% of the extreme precipitation events across all lakes. Hydrologic residence time (HRT) was negatively related to t-DOC load and heterotrophy; lakes with short HRT had higher t-DOC loads and greater net heterotrophy. The fraction of t-DOC mineralized within each lake following extreme precipitation events generally exhibited a positive relationship with lake HRT, similar to the previous studies of fractions mineralized at annual and supra-annual time scales. Event-associated turnover rate of t-DOC was higher than what is typically reported from laboratory studies and modeling exercises and was also negatively related to lake HRT. This study demonstrates that extreme precipitation events are ‘hot moments’ of carbon load, export, and turnover in lakes and that lake-specific characteristics (for example, HRT) interact with climatic patterns to set rates of important lake carbon fluxes.     

Carbon pathways to zooplankton: insights from the combined use of stable isotope and fatty acid biomarkers

1. Numerous studies have quantified the relative contribution of terrestrial‐ and phytoplankton‐derived carbon sources to zooplankton secondary production in lakes. However, few investigated the pathways along which allochthonous and autochthonous carbon (C) was actually conveyed to consumers. 2. We suggest that the combined use of fatty acid and stable isotope biomarkers could solve this issue. We conducted a field study on two oligotrophic lakes, in which primary production increased significantly between 2002 and 2004. We used modelling to estimate the contribution of terrestrial‐ and phytoplankton‐derived C to particulate organic C (POC) and zooplankton production from their δ¹³C values in 2002 and 2004. 3. According to the isotope model, phytoplankton‐derived C accounted for a major part of the POC pool in both lakes and supported more Daphnia sp. production in 2004 than in 2002. Fatty acid data revealed that increased contribution of algal‐C to Daphnia production, although common between both lakes, was achieved through C pathways that were different. In one lake, Daphnia grazed more intensively on phytoplankton, whereas in the other there was greater grazing on bacteria. In the latter case, the increased primary production resulted in greater release of algal‐derived dissolved organic C (DOC), which may have supported extra bacterial and eventually Daphnia, production. 4. This is the first study illustrating that the combination of fatty acid and stable isotope biomarkers could further our understanding of the factors controlling the relative magnitude of food webs pathways conveying organic matter to zooplankton.     

Habitat structure determines resource use by zooplankton in temperate lakes

While the importance of terrestrial linkages to aquatic ecosystems is well appreciated, the degree of terrestrial support of aquatic consumers remains debated. Estimates of terrestrial contributions to lake zooplankton have omitted a key food source, phytoplankton produced below the mixed layer. We used carbon and nitrogen stable isotope data from 25 Pacific Northwest lakes to assess the relative importance of particulate organic matter (POM) from the mixed layer, below the mixed layer and terrestrial detritus to zooplankton. Zooplankton and deep POM were depleted in 13C relative to mixed layer POM in lakes that can support deep primary production. A Bayesian stable isotope mixing model estimated that terrestrial detritus contributed <5% to zooplankton production, and confirms the role of lake optical and thermal properties; deep POM accounted for up to 80% of zooplankton production in the clearest lakes. These results suggest terrestrial support of lake zooplankton production is trivial.     

Weak Response of Animal Allochthony and Production to Enhanced Supply of Terrestrial Leaf Litter in Nutrient-Rich Lakes

Ecosystems are generally linked via fluxes of nutrients and energy across their boundaries. For example, freshwater ecosystems in temperate regions may receive significant inputs of terrestrially derived carbon via autumnal leaf litter. This terrestrial particulate organic carbon (POC) is hypothesized to subsidize animal production in lakes, but direct evidence is still lacking. We divided two small eutrophic lakes each into two sections and added isotopically distinct maize litter to the treatment sections to simulate increased terrestrial POC inputs via leaf litter in autumn. We quantified the reliance of aquatic consumers on terrestrial resources (allochthony) in the year subsequent to POC additions by applying mixing models of stable isotopes. We also estimated lake-wide carbon (C) balances to calculate the C flow to the production of the major aquatic consumer groups: benthic macroinvertebrates, crustacean zooplankton, and fish. The sum of secondary production of crustaceans and benthic macroinvertebrates supported by terrestrial POC was higher in the treatment sections of both lakes. In contrast, total secondary and tertiary production (supported by both autochthonous and allochthonous C) was higher in the reference than in the treatment sections of both lakes. Average aquatic consumer allochthony per lake section was 27–40%, although terrestrial POC contributed less than about 10% to total organic C supply to the lakes. The production of aquatic consumers incorporated less than 5% of the total organic C supply in both lakes, indicating a low ecological efficiency. We suggest that the consumption of terrestrial POC by aquatic consumers facilitates a strong coupling with the terrestrial environment. However, the high autochthonous production and the large pool of autochthonous detritus in these nutrient-rich lakes make terrestrial POC quantitatively unimportant for the C flows within food webs.     

流溪河水库颗粒有机物及浮游动物碳、氮稳定同位素特征

为了解影响流溪河水库颗粒有机物(POM)碳和氮稳定同位素(δ¹³C和δ¹⁵N)变化的主要因素,及其与浮游动物δ¹³C和δ¹⁵N之间的关系,于2008年5月至12月份对POM及浮游动物的δ¹³C和δ¹⁵N进行了研究。颗粒有机物碳稳定同位素(δ¹³C_POM)和氮稳定同位素(δ¹⁵N_POM)的季节性变化幅度分别为5.1‰和2.2‰,5月和7月份δ¹³C_POM较高,而在10月和12月份降低,这主要与降雨将大量外源有机物带入水库而引起的外源及内源有机物在POM组成上发生变化有关。δ¹⁵N_POM总体呈上升趋势,可能是由降雨引起的外源负荷、初级生产力、生物固氮等因素共同作用的结果。浮游动物的δ¹³C及δ¹⁵N总的变化趋势与POM的相似,也具有明显的季节性变化,食物来源的季节变化可能是造成其变化的主要原因。在5月份,浮游动物的食物来源为POM中δ¹³C较高的部分,也就是外源有机物,而在10月及12月份,其食物则可能主要为浮游植物。     

Essential fatty acids and phosphorus in seston from lakes with contrasting terrestrial dissolved organic carbon content

1. It is often assumed that lakes highly influenced by terrestrial organic matter (TOM) have low zooplankton food quality because of elemental and/or biochemical deficiencies of the major particulate organic carbon pools. We used the biochemical [polyunsaturated fatty acids, especially eicosapentaenoic acid (EPA) – 20:5ω3] and elemental (C : P ratio) composition of particulate matter (PM) as qualitative measures of potential zooplankton food in two categories of lakes of similar primary productivity, but with contrasting TOM influence (clear water versus humic lakes). 2. C : P ratios (atomic ratio) in PM were similar between lake categories and were above 400. The concentration (μg L⁻¹) and relative content (μg mg C⁻¹) of EPA, as well as the particulate organic carbon concentration, were higher in the humic lakes than in the clear‐water lakes. 3. Our results show high fatty acid quality of PM in the humic lakes. The differences in the biochemical quality of the potential zooplankton food between lake categories can be attributed to the differences in their phytoplankton communities. 4. High biochemical quality of the food can result in high efficiency of energy transfer in the food chain and stimulate production at higher trophic levels, assuming that zooplankton are able to ingest and digest the resource available.     

Reducing dissolved phosphorus loading to the Salton Sea with aluminum sulfate

Terrestrial support of aquatic food webs is becoming well established in the science of ecology. However, while terrestrial subsidies of energy have been shown to exert strong effects on aquatic food webs, it is less clear how variations in these subsidies, via natural or anthropogenic factors, will affect recipient ecosystems. To assess the influence of variations in terrestrial subsidies on an aquatic food web, we manipulated leaf-litter inputs in artificial ponds. Decreasing litter inputs did not affect any of the response variables in artificial ponds. This may be because the minimal amount of terrestrial carbon present combined with autochthonous production was enough to sustain the food web and/or the food web was altered in ways not detected by the experimental design. However, increasing leaf-litter inputs increased the percent survival and developmental rate of larval wood frogs (Rana sylvatica). Conversely, increasing litter input appeared to have no influence on zooplankton or salamander larvae. Increasing litter inputs also increased the dissolved organic carbon content and decreased the percent saturation of dissolved oxygen in artificial ponds. As system respiration in aquatic systems is frequently dominated by microbial respiration, we hypothesize that the effects of increasing litter input on wood frogs were the result of an increase food resources (i.e., microbes) for tadpoles. The lack of a response by salamander larvae and zooplankton may be due to the densities of zooplankton in tanks providing enough food for salamanders in all treatments, variation among specific zooplankton species in their ability to exploit these resources and transfer energy to salamanders, or omnivory among zooplankton offsetting the affects of leaf-litter inputs. Additional work is needed to determine the influence of litter inputs on zooplankton and salamanders in this community. These data demonstrate that variations in leaf-litter inputs can influence food web structure; however, the importance of these variations will likely be dependent upon the trophic position of various consumers. Handling editor: J. Cole     

Carbon dioxide supersaturation promotes primary production in lakes

A majority of the world's lakes are supersaturated with respect to carbon dioxide (CO(2) ). By experimental manipulation of the CO(2) concentration in supersaturated boreal lakes, we demonstrate that phytoplankton primary production was up to 10 times higher in supersaturated lake water in comparison with water with CO(2) at equilibrium concentrations and that CO(2) , together with nutrients, explained most of the variation in pelagic primary production and phytoplankton biomass over a wide variety of unproductive lakes. These results suggest that phytoplankton can be co-limited by CO(2) and nutrients in unproductive lakes. As import of terrestrial organic carbon and its subsequent microbial mineralisation in lakes is a driving force of CO(2) -supersaturation our results suggest that lake productivity and carbon cycling may respond to variations in terrestrial organic carbon export, (e.g. caused by land use or climate change) in ways not described before.     

Bacterial chitin hydrolysis in two lakes with contrasting trophic statuses

Chitin, which is a biopolymer of the amino sugar glucosamine (GlcN), is highly abundant in aquatic ecosystems, and its degradation is assigned a key role in the recycling of carbon and nitrogen. In order to study the significance of chitin decomposition in two temperate freshwater lakes with contrasting trophic and redox conditions, we measured the turnover rate of the chitin analog methylumbelliferyl-N,N'-diacetylchitobioside (MUF-DC) and the presence of chitinase (chiA) genes in zooplankton, water, and sediment samples. In contrast to the eutrophic and partially anoxic lake, chiA gene fragments were detectable throughout the oligotrophic water column and chiA copy numbers per ml of water were up to 15 times higher than in the eutrophic waters. For both lakes, the highest chiA abundance was found in the euphotic zone--the main habitat of zooplankton, but also the site of production of easily degradable algal chitin. The bulk of chitinase activity was measured in zooplankton samples and the sediments, where recalcitrant chitin is deposited. Both, chiA abundance and chitinase activity correlated well with organic carbon, nitrogen, and concentrations of particulate GlcN. Our findings show that chitin, although its overall contribution to the total organic carbon is small (~0.01 to 0.1%), constitutes an important microbial growth substrate in these temperate freshwater lakes, particularly where other easily degradable carbon sources are scarce.     

Low Levels of Allochthony in Consumers Across Three High-Elevation Lake Types

The integration of lakes into watershed-scale energy budgets remains a major goal of aquatic ecosystem ecology. However, this enterprise has focused almost exclusively on temperate and boreal systems and on zooplankton as representatives of system-wide energy flow. We investigated the proportion of consumer biomass derived from terrestrial sources, allochthony, in three classes of high-elevation lakes—alpine, large and small montane—of varying geometry and watershed ecosystem development, and across five taxa, including macrobenthic invertebrates and fish. We used stable isotopes of carbon (¹³C:¹²C), nitrogen (¹⁵N:¹⁴N), and hydrogen (²H:¹H) to fit a modular Bayesian mixing model, which estimated proportional assimilation of phytoplankton, algal periphyton, and terrestrial organic matter by each consumer. The stable isotope analysis was supplemented with a comparison of fatty acid profiles between consumers and producers, and with a Daphnia magna rearing study involving aquatic and terrestrial nutrient sources. The most probable estimate of allochthony across consumer taxa was 41% in small montane lakes (< 0.1 ha) with high terrestrial C loading. For large montane (3–11 ha) and alpine lakes (0.8–3 ha), with substantially less terrestrial influence, allochthony was just 4 and 3%, respectively. Allochthony was also lower on average for benthic grazers than for pelagic consumers. Our results corroborate previous findings that lake size, depth, and light penetration are dominant physical controls on allochthony, but add that it sharply declines at high elevation due to changes in terrestrial primary production near or above tree line.     

Nutrients associated with terrestrial dissolved organic matter drive changes in zooplankton:phytoplankton biomass ratios in an alpine lake

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Effects of algal and terrestrial carbon on methane production rates and methanogen community structure in a temperate lake sediment

1. Sources of atmospheric CH₄ are both naturally occurring and anthropogenic. In fact, some anthropogenic activities may influence the production of CH₄ from natural sources, such as lakes. 2. Ongoing changes in the catchment of lakes, including eutrophication and increased terrestrial organic carbon export, may affect CH₄ production rates as well as shape methanogen abundance and community structure. Therefore, inputs from catchments to lakes should be examined for their effects on CH₄ production. 3. We added algal and terrestrial carbon separately to lake sediment cores and measured CH₄ production. We also used quantitative polymerase chain reaction and terminal restriction fragment length polymorphism to determine the effects of these carbon additions on methanogen abundance and community composition. 4. Our results indicate that CH₄ production rates were significantly elevated following the addition of algal biomass. Terrestrial carbon addition also appeared to increase methanogenesis rates; however, the observed increase was not statistically significant. 5. Interestingly, increased CH₄ production rates resulted from increases in per‐cell activity rather than an increase in methanogen abundance or community compositional shifts, as indicated by our molecular analyses. 6. Overall, anthropogenic impacts on aquatic ecosystems can influence methanogenesis rates and should be considered in models of global methane cycling and climate.     

Different carbon support for respiration and secondary production in unproductive lakes

This study investigates the allocation of allochthonous organic carbon (AlloOC) to pelagic respiration and biomass production in unproductive lakes. Metabolic process rates and stable isotopic composition (δ¹³C) of crustacean zooplankton and respired CO₂ were measured in the epilimnion of 13 forest lakes in northern Sweden. The δ¹³C of zooplankton was low (−31.2 to −38.0‰) compared to that of respired CO₂ (−28.4 to −30.6‰), implying that the relative importance of AlloOC was lower for zooplankton (ca 40%) than for respiration (ca 80%). Combining δ¹³C and carbon flux data revealed that a large amount of metabolized AlloOC was lost in respiration, compared to the amount transferred to zooplankton (<3%). Thus, despite large respiratory losses, AlloOC was still important for zooplankton growth, implying a high supply of AlloOC in comparison to phytoplankton generated organic carbon in the lakes.     

Bottom‐up and top‐down effects of browning and warming on shallow lake food webs

Productivity and trophic structure of aquatic ecosystems result from a complex interplay of bottom‐up and top‐down forces that operate across benthic and pelagic food web compartments. Projected global changes urge the question how this interplay will be affected by browning (increasing input of terrestrial dissolved organic matter), nutrient enrichment and warming. We explored this with a process‐based model of a shallow lake food web consisting of benthic and pelagic components (abiotic resources, primary producers, grazers, carnivores), and compared model expectations with the results of a browning and warming experiment in nutrient‐poor ponds harboring a boreal lake community. Under low nutrient conditions, the model makes three major predictions. (a) Browning reduces light and increases nutrient supply; this decreases benthic and increases pelagic production, gradually shifting productivity from the benthic to the pelagic habitat. (b) Because of active habitat choice, fish exert top‐down control on grazers and benefit primary producers primarily in the more productive of the two habitats. (c) Warming relaxes top‐down control of grazers by fish and decreases primary producer biomass, but effects of warming are generally small compared to effects of browning and nutrient supply. Experimental results were consistent with most model predictions for browning: light penetration, benthic algal production, and zoobenthos biomass decreased, and pelagic nutrients and pelagic algal production increased with browning. Also consistent with expectations, warming had negative effects on benthic and pelagic algal biomass and weak effects on algal production and zoobenthos and zooplankton biomass. Inconsistent with expectations, browning had no effect on zooplankton and warming effects on fish depended on browning. The model is applicable also to nutrient‐rich systems, and we propose that it is a useful tool for the exploration of the consequences of different climate change scenarios for productivity and food web dynamics in shallow lakes, the worldwide most common lake type.     

Love Handles in Aquatic Ecosystems: The Role of Dissolved Organic Carbon Drawdown, Resuspended Sediments, and Terrigenous Inputs in the Carbon Balance of Lake Michigan

During the unstratified (winter) and stratified (summer) periods of 1999 and 2000, we examined carbon (C) dynamics in the upper water column of southern Lake Michigan. We found that (a) bacterial respiration (BR) and planktonic respiration (PR) were major sinks for C, (b) C flux through bacteria (CFTB) was diminished in winter because of reduced bacterial production (BP) and increased bacterial growth efficiency (BGE) at colder temperatures, and (c) PR exceeded primary production (PP) during the spring–summer transition. Drawdown of dissolved organic C (DOC), resuspended organic matter from the lake floor, and riverine organic matter likely provided organic C to compensate for this temporal deficit. DOC in the water column decreased between winter and summer (29–91 mg C m² d⁻¹) and accounted for 20%–53% of CFTB and 11%–33% of PR. Sediment resuspension events supported elevated winter heterotrophy in the years that they occurred with greatest intensities (1998 and 2000) and may be important to interannual variability in C dynamics. Further, riverine discharge, containing elevated DOC (5×) and dissolved P (10×) relative to lake water, peaked in the winter–spring season in southern Lake Michigan. Collectively, terrigenous inputs (river, stream, and groundwater discharges; storm water runoff; and atmospheric precipitation) may support approximately 10%–20% of annual in-lake heterotrophy as well as autotrophy. Terrestrial subsidies likely play a key role in the C balance of even very large lakes, representing a critical linkage between terrestrial and aquatic ecosystems. Received 11 June 2001; Accepted 14 December 2001.     

Links between Terrestrial Primary Production and Bacterial Production and Respiration in Lakes in a Climate Gradient in Subarctic Sweden

We compared terrestrial net primary production (NPP) and terrestrial export of dissolved organic carbon (DOC) with lake water heterotrophic bacterial activity in 12 headwater lake catchments along an altitude gradient in subarctic Sweden. Modelled NPP declined strongly with altitude and annual air temperature decreases along the altitude gradient (6°C between the warmest and the coldest catchment). Estimated terrestrial DOC export to the lakes was closely correlated to NPP. Heterotrophic bacterial production (BP) and respiration (BR) were mainly based on terrestrial organic carbon and strongly correlated with the terrestrial DOC export. Excess respiration over PP of the pelagic system was similar to net emission of CO₂ in the lakes. BR and CO₂ emission made up considerably higher shares of the terrestrial DOC input in warm lakes than in cold lakes, implying that respiration and the degree of net heterotrophy in the lakes were dependant not only on terrestrial export of DOC, but also on characteristics in the lakes which changed along the gradient and affected the bacterial metabolization of allochthonous DOC. The study showed close links between terrestrial primary production, terrestrial DOC export and bacterial activity in lakes and how these relationships were dependant on air temperature. Increases in air temperature in high latitude unproductive systems might have considerable consequences for lake water productivity and release of CO₂ to the atmosphere, which are ultimately determined by terrestrial primary production.     

Response of plankton to nutrients,planktivory and terrestrial organic matter: a model analysis of whole‐lake experiments

Terrestrial organic matter can be assimilated by aquatic consumers but implications for biomass and production are unresolved. An ecosystem model was fit to estimate effects of phosphorus (P) load, planktivory, and supply rate of terrestrial particulate organic carbon (TPOC) on phytoplankton and zooplankton in five whole‐lake experiments. Phytoplankton biomass increased with P load and planktivory and decreased with TPOC supply rate. Zooplankton biomass increased with P load and responded weakly to planktivory and TPOC supply rate. Zooplankton allochthony (proportion of carbon from terrestrial sources) decreased with P load and planktivory and increased with TPOC supply rate. Lakes with low allochthony (< 0.3) had wide ranges of phytoplankton and zooplankton biomass and production, depending on P load and planktivory. Lakes with high allochthony (> 0.3) had low biomass and production of both phytoplankton and zooplankton. In summary, terrestrial OC inhibits primary production and is a relatively low‐quality food source for zooplankton.     

Interactive effects of higher temperature and dissolved organic carbon on planktonic communities in fishless mountain lakes

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