Effects of Eutrophication on Sedimentary Organic Carbon Cycling in five Temperate Lakes
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Biogeosciences, 16, 3725–3746, 2019 https://doi.org/10.5194/bg-16-3725-2019 © Author(s) 2019. This work is distributed under the Creative Commons Attribution 4.0 License. Effects of eutrophication on sedimentary organic carbon cycling in five temperate lakes Annika Fiskal1, Longhui Deng1, Anja Michel1, Philip Eickenbusch1, Xingguo Han1, Lorenzo Lagostina1, Rong Zhu1, Michael Sander1, Martin H. Schroth1, Stefano M. Bernasconi3, Nathalie Dubois2,3, and Mark A. Lever1 1Institute of Biogeochemistry and Pollutant Dynamics (IBP), ETH Zurich, Universitätstrasse 16, 8092 Zurich, Switzerland 2Surface Waters Research – Management, Eawag, Swiss Federal Institute of Aquatic Science and Technology, Überlandstrasse 133, 8600 Dübendorf, Switzerland 3Department of Earth Sciences, ETH Zurich, Sonneggstrasse 5, 8092 Zurich, Switzerland Correspondence: Annika Fiskal (annika.fi[email protected]) and Mark A. Lever ([email protected]) Received: 25 March 2019 – Discussion started: 27 March 2019 Revised: 2 September 2019 – Accepted: 4 September 2019 – Published: 30 September 2019 Abstract. Even though human-induced eutrophication has rate. Instead, data from one eutrophic lake suggest that artifi- severely impacted temperate lake ecosystems over the last cial ventilation, which has been used to prevent water column centuries, the effects on total organic carbon (TOC) burial anoxia in this lake for 35 years, may help sustain high rates and mineralization are not well understood. We study these of TOC burial and accumulation in sediments despite water effects based on sedimentary records from the last 180 years column P concentrations being strongly reduced. Our study in five Swiss lakes that differ in trophic state. We compare provides novel insights into the influence of human activi- changes in TOC content and modeled TOC accumulation ties in lakes and lake watersheds on lake sediments as carbon rates through time to historical data on algae blooms, water sinks and habitats for diverse microbial respiration processes. column anoxia, wastewater treatment, artificial lake ventila- tion, and water column phosphorus (P) concentrations. We furthermore investigate the effects of eutrophication on rates of microbial TOC mineralization and vertical distributions of 1 Introduction microbial respiration reactions in sediments. Our results in- dicate that the history of eutrophication is well recorded in Lake sediments play an important role in the global carbon the sedimentary record. Overall, eutrophic lakes have higher cycle despite covering only about 1 % of the Earth’s sur- TOC burial and accumulation rates, and subsurface peaks face area (Cole et al., 2007; Battin et al., 2009). Estimates in TOC coincide with past periods of elevated P concentra- of global carbon dioxide (CO2) net fluxes from lake systems − tions in lake water. Sediments of eutrophic lakes, moreover, range from 60 to 580 Tg C yr 1 (Raymond et al., 2013; Hol- have higher rates of total respiration and higher contributions gerson and Raymond, 2016). Methane (CH4) fluxes are much of methanogenesis to total respiration. However, we found smaller (6 to 36 Tg C; Bastviken et al., 2004), but are also strong overlaps in the distributions of respiration reactions globally important given that CH4 has a 28 to 36 times higher involving different electron acceptors in all lakes regardless global warming potential than CO2 on a timescale of about of lake trophic state. Moreover, even though water column 100 years (Cubasch et al., 2014). Besides being important P concentrations have been reduced by ∼ 50 %–90 % since sources of CO2 and CH4, lakes are also important sinks of the period of peak eutrophication in the 1970s, TOC burial organic C (OC). Global storage of C in lake sediments for and accumulation rates have only decreased significantly, by the entire Holocene is estimated to be ∼ 820 Pg C (Einsele et ∼ 20 % and 25 %, in two of the five lakes. Hereby there is no al., 2001; Mendonca et al., 2017). clear relationship between the magnitude of the P concentra- Whether OC in lake sediments is buried and preserved tion decrease and the change in TOC burial and accumulation over geologic time or degraded to CO2 and CH4 is par- tially controlled by sediment microorganisms, which break Published by Copernicus Publications on behalf of the European Geosciences Union. 3726 A. Fiskal et al.: Effects of eutrophication on sedimentary organic carbon cycling down OC for energy conservation and biosynthesis (Ned- tion and structure of the OC also affect OC preservation. OC well, 1984). In a first step, microorganisms enzymatically of terrestrial plants is typically more resistant to microbial hydrolyze organic macromolecules, e.g., proteins, nucleic attack than OC of phytoplankton due to the presence of bio- acids, lipids, and polysaccharides, extracellularly into suffi- logically resistant polymers, e.g., lignin, waxes, and resins, ciently small components that can be taken up across the cell that are absent in phytoplankton (Burdige, 2007). Abiotic membrane (Canfield et al., 2005). If oxygen (O2) is available processes, e.g., condensation reactions (e.g., Burdige, 2007), as an electron acceptor, organisms performing initial hydrol- incorporation of sedimentary Fe(III) (Lalonde et al., 2012) ysis are often capable of oxidizing hydrolysis products all or sulfur compounds (Werne et al., 2000, 2008; Hebting et the way to CO2. In the absence of O2, OC is degraded to al., 2006), and physical protection by adsorption or encapsu- CO2 or CH4 by multiple groups of more specialized microor- lation can also significantly decrease rates of microbial OC ganisms (Canfield et al., 2005). Primary fermenters carry out degradation (reviewed in Hedges et al., 2000). the initial extracellular hydrolysis and subsequently gain en- Besides these natural factors, the burial of C in lake sed- ergy from the intracellular disproportionation of hydrolysis iment is also largely influenced by anthropogenic activi- products to smaller molecules such as H2, short-chain or- ties, such as agriculture, wastewater input, and urbanization ganic acids, and alcohols. In some cases, an intermediary (Heathcote and Downing, 2012; Anderson et al., 2013). OC secondary fermentation step takes place whereby the organic burial rates may increase due to increased water column pri- acids and alcohols produced by primary fermenters are dis- mary production resulting from increased nutrient input, es- proportionated to H2, acetate, and C1 compounds (Capone pecially P (Dean and Gorham, 1998; Maerki et al., 2009; and Kiene, 1988; Schink, 1997). The products of primary Heathcote and Downing, 2012; Anderson et al., 2013, 2014), and secondary fermentation are subsequently converted to which is the limiting nutrient for primary production in most CO2 or CH4 by respiring organisms using – in order of en- lake water columns (Correll, 1999; Conley et al., 2009). − ergy yields from high to low – nitrate (NO3 ), manganese(IV) Hereby increased OC loading (eutrophication), mainly due 2− to stimulation of water column primary production, enhances (Mn(IV)), ferric iron (Fe(III)), sulfate (SO4 ), and CO2 as electron acceptors (Froelich et al., 1979; Drake et al., 2006). OC sedimentation rates and O2 consumption (Valiela et al., The differences in energy yields can result in a vertical zona- 1997; Gontikaki et al., 2012). The resulting (seasonal) water − column hypoxia or anoxia negatively impact ecosystem func- tion (“redox zonation”) of respiration reactions, with NO3 reduction (denitrification) occurring near the sediment sur- tioning as well as commercial and recreational uses (Valiela face, as soon as O2 is depleted, CO2 reduction via methano- et al., 1997; McGlathery, 2001; Breitburg, 2002). Strategies genesis dominating in deeper layers, where all other electron to manage eutrophication include restrictions on terrestrial P 2− use, agriculture-free buffer zones, wastewater treatment with acceptors have been depleted, and Mn(IV), Fe(III), and SO4 reduction taking place in distinct sediment intervals between P precipitation systems, and artificial water column mixing the zones of denitrification and methanogenesis (Lovley and and aeration (Schindler, 2006; Conley et al., 2009). These Goodwin, 1988; Hoehler et al., 1998; Canfield et al., 2005; remediation strategies can lead to substantial reductions in P Jørgensen and Kasten, 2006; Canfield and Thamdrup, 2009). concentrations (Müller et al., 1990; Liechti, 1994). However, A complex set of interacting variables determines whether there are still open questions regarding the influence of these microorganisms break down sedimentary organic com- mitigation strategies on OC burial, in part due to P retention pounds and thus whether organic carbon is stored in sedi- and release from lake sediments (Gachter and Muller, 2003; ment in the long term or returns to the hydrosphere and at- Moosmann et al., 2006). mosphere as CO2 and methane over shorter timescales. Aer- Here we investigate OC burial through time across five obic respiration results in the breakdown of a larger fraction temperate lakes that differ in eutrophication history over the of the sedimentary organic carbon pool compared to anaer- past 180 years. We test the hypothesis that (i) OC burial rates obic processes (Lehmann et al., 2002; Sobek et al., 2009; have historically increased in response to anthropogenic eu- Katsev and Crowe, 2015). The O2 exposure time, i.e., the trophication and that (ii) increased P concentrations, through time each organic molecule is present under