Trophic state changes can affect the importance of methane-derived carbon in aquatic food webs.
ABSTRACT: Methane-derived carbon, incorporated by methane-oxidizing bacteria, has been identified as a significant source of carbon in food webs of many lakes. By measuring the stable carbon isotopic composition (?13C values) of particulate organic matter, Chironomidae and Daphnia spp. and their resting eggs (ephippia), we show that methane-derived carbon presently plays a relevant role in the food web of hypertrophic Lake De Waay, The Netherlands. Sediment geochemistry, diatom analyses and ?13C measurements of chironomid and Daphnia remains in the lake sediments indicate that oligotrophication and re-eutrophication of the lake during the twentieth century had a strong impact on in-lake oxygen availability. This, in turn, influenced the relevance of methane-derived carbon in the diet of aquatic invertebrates. Our results show that, contrary to expectations, methane-derived relative to photosynthetically produced organic carbon became more relevant for at least some invertebrates during periods with higher nutrient availability for algal growth, indicating a proportionally higher use of methane-derived carbon in the lake's food web during peak eutrophication phases. Contributions of methane-derived carbon to the diet of the investigated invertebrates are estimated to have ranged from 0-11% during the phase with the lowest nutrient availability to 13-20% during the peak eutrophication phase.
Project description:Small humic forest lakes often have high contributions of methane-derived carbon in their food webs but little is known about the temporal stability of this carbon pathway and how it responds to environmental changes on longer time scales. We reconstructed past variations in the contribution of methanogenic carbon in the pelagic food web of a small boreal lake in Finland by analyzing the stable carbon isotopic composition (?13C values) of chitinous fossils of planktivorous invertebrates in sediments from the lake. The ?13C values of zooplankton remains show several marked shifts (approx. 10 ‰), consistent with changes in the proportional contribution of carbon from methane-oxidizing bacteria in zooplankton diets. The results indicate that the lake only recently (1950s) obtained its present state with a high contribution of methanogenic carbon to the pelagic food web. A comparison with historical and palaeobotanical evidence indicates that this most recent shift coincided with agricultural land-use changes and forestation of the lake catchment and implies that earlier shifts may also have been related to changes in forest and land use. Our study demonstrates the sensitivity of the carbon cycle in small forest lakes to external forcing and that the effects of past changes in local land use on lacustrine carbon cycling have to be taken into account when defining environmental and ecological reference conditions in boreal headwater lakes.
Project description:During past decades, many lakes underwent drastic human-caused changes in trophic state with strong implications for population dynamics and food web processes. We investigated the influence of trophic state on nutrient allocation into Daphnia resting eggs. The production of resting eggs is an important survival strategy, allowing Daphnia to cope with unfavorable environmental conditions. Allocation of essential nutrients into resting eggs may crucially influence embryonic development and offspring survival and thus is of great ecological and evolutionary interest. The capacity of Daphnia to adjust the allocation of nutrients into resting eggs may depend on the dietary nutrient supply, which may vary with trophic state-related changes in the phytoplankton community composition. Resting eggs were isolated from sediment cores taken from Lake Constance, a large prealpine lake with a distinct eutrophication and reoligotrophication history, and analyzed for elemental (carbon, nitrogen, and phosphorus) and biochemical (sterols and fatty acids) nutrients. Carbon allocation into Daphnia resting eggs continuously decreased over time, irrespective of changes in trophic state. The allocation of nitrogen into Daphnia resting eggs followed the changes in trophic state, that is, nitrogen concentrations in resting eggs increased with eutrophication and decreased again with reoligotrophication. The allocation of phosphorus, sterols and long-chain polyunsaturated fatty acids, such as eicosapentaenoic acid, into Daphnia resting eggs did not change significantly over time. Changes in trophic state strikingly influenced all trophic levels in Lake Constance. However, nutrient allocation into Daphnia resting eggs was mostly resilient to changes in lake trophic state.
Project description:Methanogens are the major contributors of greenhouse gas methane and play significant roles in the degradation and transformation of organic matter. These organisms are particularly abundant in Swan Lake, which is a shallow lagoon located in Rongcheng Bay, Yellow Sea, northern China, where eutrophication from overfertilization commonly results in anoxic environments. High organic phosphorus content is a key component of the total phosphorus in Swan Lake and is possibly a key factor affecting the eutrophication and carbon and nitrogen cycling in Swan Lake. The effects of organic phosphorus on eutrophication have been well-studied with respect to bacteria, such as cyanobacteria, unlike the effects of organic phosphorus on methanogenesis. In this study, different sediment layer samples of seagrass-vegetated and unvegetated areas in Swan Lake were investigated to understand the effects of organic phosphorus on methylotrophic methanogenesis. The results showed that phytate phosphorus significantly promoted methane production in the deepest sediment layer of vegetated regions but suppressed it in unvegetated regions. Amplicon sequencing revealed that methylotrophic Methanococcoides actively dominated in all enrichment samples from both regions with additions of trimethylamine or phytate phosphorus, whereas methylotrophic Methanolobus and Methanosarcina predominated in the enrichments obtained from vegetated and unvegetated sediments, respectively. These results prompted further study of the effects of phytate phosphorus on two methanogen isolates, Methanolobus psychrophilus, a type strain, Methanosarcina mazei, an isolate from Swan Lake sediments. Cultivation experiments showed that phytate phosphorus could inhibit methane production by M. psychrophilus but promote methane production by M. mazei. These culture-based studies revealed the effects of organic phosphorus on methylotrophic methanogenesis in coastal lagoon sediments and improves our understanding of the mechanisms of organic carbon cycling leading to methanogenesis mediated by organic phosphorus dynamics in coastal wetlands.
Project description:To assess whether and how zooplankton communities respond to variations in temperature and how these assemblages change with eutrophication, we performed a large-scale, monthly survey from August 2011 to July 2012 to determine the seasonal and spatial variations in these communities in a high-altitude lake. A detrended correspondence analysis and a path analysis demonstrated that temperature and chlorophyll a were important factors influencing zooplankton. The path diagram showed that Daphnia was negatively affected directly by chlorophyll a and indirectly by temperature, whereas Bosmina was directly and positively affected by temperature. Daphnia spp. decreased in both absolute and relative biomass during warm seasons, whereas Bosmina spp. showed the opposite trend. Moreover, the lowest Daphnia spp. biomass was observed in the southern region, which was the most eutrophic. Our results indicate that increasing temperatures will continue to shift the dominant genus from Daphnia to Bosmina, and this change will be exacerbated by eutrophication. In addition, the zooplankton of Lake Erhai have shifted to smaller species over time as temperature and eutrophication have increased, which implies that zooplankton succession to small cladocerans may be markedly accelerated under further climate change and the increased eutrophication that has been observed in recent decades.
Project description:Freshwater lakes emit large amounts of methane, some of which is produced in oxic surface waters. Two potential pathways for aerobic methane production exist: methanogenesis in oxygenated water, which has been observed in some lakes, or demethylation of small organic molecules. Although methane is produced via demethylation in oxic marine environments, this mechanism of methane release has not yet been demonstrated in freshwater systems. Genes related to the C-P lyase pathway, which cleaves C-P bonds in phosphonate compounds, were found in a metagenomic survey of the surface water of Lake Matano, which is chronically P-starved and methane-rich. We demonstrate that four bacterial isolates from Lake Matano obtain P from methylphosphonate and release methane, and that this activity is repressed by phosphate. We further demonstrate that expression of phnJ, which encodes the enzyme that releases methane, is higher in the presence of methylphosphonate and lower when both methylphosphonate and phosphate are added. This gene is also found in most of the metagenomic data sets from freshwater environments. These experiments link methylphosphonate degradation and methane production with gene expression and phosphate availability in freshwater organisms, and suggest that some of the excess methane in the Lake Matano surface water, and in other methane-rich lakes, may be produced by P-starved bacteria. IMPORTANCE:Methane is an important greenhouse gas, and contributes substantially to global warming. Although freshwater environments are known to release methane into the atmosphere, estimates of the amount of methane emitted by freshwater lakes vary from 8 to 73 Tg per year. Methane emissions are difficult to predict in part because the source of the methane can vary: it is the end product of the energy-conserving pathway in methanogenic archaea, which predominantly live in anoxic sediments or waters, but have also been identified in some oxic freshwater environments. More recently, methane release from small organic molecules has been observed in oxic marine environments. Here we show that demethylation of methylphosphonate may also contribute to methane release from lakes, and that phosphate can repress this activity. Since lakes are typically phosphorus-limited, some methane release in these environments may be a byproduct of phosphorus metabolism, rather than carbon or energy metabolism. Methane emissions from lakes are currently predicted using primary production, eutrophication status, extent of anoxia, and the shape and size of the lake; to improve prediction of methane emissions, phosphorus availability and sources may also need to be included in these models.
Project description:Denitrification is a critical process that can alleviate the effects of excessive nitrogen availability in aquatic ecosystems subject to eutrophication. An important part of denitrification occurs in benthic systems where bioturbation by meiofauna (invertebrates <1 mm) and its effect on element cycling are still not well understood. Here we study the quantitative impact of meiofauna populations of different abundance and diversity, in the presence and absence of macrofauna, on nitrate reduction, carbon mineralization and methane fluxes. In sediments with abundant and diverse meiofauna, denitrification is double that in sediments with low meiofauna, suggesting that meiofauna bioturbation has a stimulating effect on nitrifying and denitrifying bacteria. However, high meiofauna densities in the presence of bivalves do not stimulate denitrification, while dissimilatory nitrate reduction to ammonium rate and methane efflux are significantly enhanced. We demonstrate that the ecological interactions between meio-, macrofauna and bacteria are important in regulating nitrogen cycling in soft-sediment ecosystems.
Project description:The first few months of life is the most vulnerable period for fish and their optimal hatching time with zooplankton prey is favored by natural selection. Traditionally, however, prey abundance (i.e., zooplankton density) has been considered important, whereas prey nutritional composition has been largely neglected in natural settings. High-quality zooplankton, rich in both essential amino acids (EAAs) and fatty acids (FAs), are required as starting prey to initiate development and fast juvenile growth. Prey quality is dependent on environmental conditions, and, for example, eutrophication and browning are two major factors defining primary producer community structures that will directly determine the nutritional quality of the basal food sources (algae, bacteria, terrestrial matter) for zooplankton. We experimentally tested how eutrophication and browning affect the growth and survival of juvenile rainbow trout (Oncorhynchus mykiss) by changing the quality of basal resources. We fed the fish on herbivorous zooplankton (Daphnia) grown with foods of different nutritional quality (algae, bacteria, terrestrial matter), and used GC-MS, stable isotope labeling as well as bulk and compound-specific stable isotope analyses for detecting the effects of different diets on the nutritional status of fish. The content of EAAs and omega-3 (?-3) polyunsaturated FAs (PUFAs) in basal foods and zooplankton decreased in both eutrophication and browning treatments. The decrease in ?-3 PUFA and especially docosahexaenoic acid (DHA) was reflected to fish juveniles, but they were able to compensate for low availability of EAAs in their food. Therefore, the reduced growth and survival of the juvenile fish was linked to the low availability of DHA. Fish showed very low ability to convert alpha-linolenic acid (ALA) to DHA. We conclude that eutrophication and browning decrease the availability of the originally phytoplankton-derived DHA for zooplankton and juvenile fish, suggesting bottom-up regulation of food web quality.
Project description:We examined stable carbon and nitrogen isotope ratios for a large variety of consumers in intertidal and subtidal habitats, and their potential primary food sources [i.e., microphytobenthos (MPB), phytoplankton, and Phragmites australis] in a coastal bay system, Yeoja Bay of Korea, to test the hypothesis that the transfer of intertidal MPB-derived organic carbon to the subtidal food web can be mediated by motile consumers. Compared to a narrow ?13C range (-18 to -16‰) of offshore consumers, a broad ?13C range (-18 to -12‰) of both intertidal and subtidal consumers indicated that 13C-enriched sources of organic matter are an important trophic source to coastal consumers. In the intertidal areas, ?13C of most consumers overlapped with or was 13C-enriched relative to MPB. Despite the scarcity of MPB in the subtidal, highly motile consumers in subtidal habitat had nearly identical ?13C range with many intertidal foragers (including crustaceans and fish), overlapping with the range of MPB. In contrast, ?13C values of many sedentary benthic invertebrates in the subtidal areas were similar to those of offshore consumers and more 13C-depleted than motile foragers, indicating high dependence on phytoplankton-derived carbon. The isotopic mixing model calculation confirms that the majority of motile consumers and also some of subtidal sedentary ones depend on intertidal MPB for more than a half of their tissue carbon. Finally, although further quantitative estimates are needed, these results suggest that direct foraging by motile consumers on intertidal areas, and thereby biological transport of MPB-derived organic carbon to the subtidal areas, may provide important trophic connection between intertidal production and the nearshore shallow subtidal food webs.
Project description:Terrestrial paleoclimate archives such as lake sediments are essential for our understanding of the continental climate system and for the modeling of future climate scenarios. However, quantitative proxies for the determination of paleotemperatures are sparse. The relative abundances of certain bacterial lipids, i.e., branched glycerol dialkyl glycerol tetraethers (brGDGTs), respond to changes in environmental temperature, and thus have great potential for climate reconstruction. Their application to lake deposits, however, is hampered by the lack of fundamental knowledge on the ecology of brGDGT-producing microbes in lakes. Here, we show that brGDGTs are synthesized by multiple groups of bacteria thriving under contrasting redox regimes in a deep meromictic Swiss lake (Lake Lugano). This niche partitioning is evidenced by highly distinct brGDGT inventories in oxic vs. anoxic water masses, and corresponding vertical patterns in bacterial 16S rRNA gene abundances, implying that sedimentary brGDGT records are affected by temperature-independent changes in the community composition of their microbial producers. Furthermore, the stable carbon isotope composition (?13C) of brGDGTs in Lake Lugano and 34 other (peri-)Alpine lakes attests to the widespread heterotrophic incorporation of 13C-depleted, methane-derived biomass at the redox transition zone of mesotrophic to eutrophic lake systems. The brGDGTs produced under such hypoxic/methanotrophic conditions reflect near-bottom water temperatures, and are characterized by comparatively low ?13C values. Depending on climate zone and water depth, lake sediment archives predominated by deeper water/low-13C brGDGTs may provide more reliable records of climate variability than those where brGDGTs derive from terrestrial and/or aquatic sources with distinct temperature imprints.
Project description:Terrestrial organic matter inputs have long been thought to play an important role in aquatic food web dynamics. Results from recent whole lake (13)C addition experiments suggest terrestrial particulate organic carbon (t-POC) inputs account for a disproportionate portion of zooplankton production. For example, several studies concluded that although t-POC only represented approximately 20% of the flux of particulate carbon available to herbivorous zooplankton, this food source accounted for approximately 50% of the C incorporated by zooplankton. We tested the direct dietary impact of t-POC (from the leaves of riparian vegetation) and various phytoplankton on Daphnia magna somatic growth, reproduction, growth efficiency, and lipid composition. By itself, t-POC was a very poor quality resource compared to cryptophytes, diatoms, and chlorophytes, but t-POC had similar food quality compared to cyanobacteria. Small additions of high quality Cryptomonas ozolinii to t-POC-dominated diets greatly increased Daphnia growth and reproduction. When offered alone, t-POC resulted in a Daphnia growth efficiency of 5 +/- 1%, whereas 100% Cryptomonas and Scenedesmus obliquus diets resulted in growth efficiencies of 46 +/- 8% (+/- SD) and 36 +/- 3%, respectively. When offered in a 50:50 mixed diet with Cryptomonas or Scenedesmus, the t-POC fraction resulted in a partial growth efficiency of 22 +/- 9% and 15 +/- 6%, respectively. Daphnia that obtained 80% of their available food from t-POC assimilated 84% of their fatty acids from the phytoplankton component of their diet. Overall, our results suggest Daphnia selectively allocate phytoplankton-derived POC and lipids to enhance somatic growth and reproduction, while t-POC makes a minor contribution to zooplankton production.