Temperature sensitivity of organic carbon
mineralization in contrasting lake sediments
Cristian Gudasz, Sebastian Sobek, David Bastviken, Birgit Koehler and Lars J. Tranvik
Linköping University Post Print
N.B.: When citing this work, cite the original article.
Original Publication:
Cristian Gudasz, Sebastian Sobek, David Bastviken, Birgit Koehler and Lars J. Tranvik,
Temperature sensitivity of organic carbon mineralization in contrasting lake sediments, 2015,
Journal of Geophysical Research - Biogeosciences, (120), 7, 1215-1225.
http://dx.doi.org/10.1002/2015JG002928
Copyright: American Geophysical Union (AGU)
http://sites.agu.org/
Postprint available at: Linköping University Electronic Press
Temperature sensitivity of organic carbon mineralization
in contrasting lake sediments
Cristian Gudasz1,2, Sebastian Sobek1, David Bastviken3, Birgit Koehler1, and Lars J. Tranvik1
1
Limnology, Department of Ecology and Evolution, Uppsala University, Uppsala, Sweden,2Now at Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, USA,3Department of Thematic Studies—Water and
Environmental Studies, Linköping University, Linköping, Sweden
Abstract
Temperature alone explains a great amount of variation in sediment organic carbon (OC) mineralization. Studies on decomposition of soil OC suggest that (1) temperature sensitivity differs between the fast and slowly decomposition OC and (2) over time, decreasing soil respiration is coupled with increase in temperature sensitivity. In lakes, autochthonous and allochthonous OC sources are generally regarded as fast and slowly decomposing OC, respectively. Lake sediments with different contributions of allochthonous and autochthonous components, however, showed similar temperature sensitivity in short-term incubation experiments. Whether the mineralization of OC in lake sediments dominated by allochthonous or autochthonous OC has different temperature sensitivity in the longer term has not been addressed. We incubated sediments from two boreal lakes that had contrasting OC origin (allochthonous versus autochthonous), and OC characteristics (C/N ratios of 21 and 10) at 1, 3, 5, 8, 13, and 21°C forfive months. Compared to soil and litter mineralization, sediment OC mineralization rates were low in spite of low apparent activation energy (Ea). The fraction of the total OC pool that was lost duringfive months varied between 0.4 and 14.8%. We estimate that the sediment OC pool not becoming long-term preserved was degraded with average apparent turnover times between 3 and 32 years. While OC mineralization was strongly dependent on temperature as well as on OC composition and origin, temperature sensitivity was similar across lakes and over time. We suggest that the temperature sensitivity of OC mineralization in lake sediments is similar across systems within the relevant seasonal scales of OC supply and degradation.1. Introduction
Soils and lake sediments are well-recognized sites for the mineralization and storage of organic carbon (OC). In the boreal biome, lake sediments store large amounts of OC [Kortelainen et al., 2004; Benoy et al., 2007]. The settling OC that reaches the sediment surface can either originate from internal primary production (autochthonous) or is imported from the drainage area (allochthonous). For lakes in the boreal zone, allochthonous dissolved organic carbon (DOC) that is leaching from wetlands and forest soils in their catchments [Laudon et al., 2011] is partiallyflocculated in the water column and subsequently settled onto the sediments [von Wachenfeldt et al., 2008]. A significant fraction of the terrestrial primary production in boreal landscapes can end up on the bottom of lakes [von Wachenfeldt and Tranvik, 2008]. Given this translocation of carbon across the terrestrial-aquatic continuum it is valid to ask: Does the temperature sensitivity of the sediment mineralization of allochthonous OC differs from that of the soil where it originates and with that of the sediment autochthonous OC? Such a perspective is currently lacking. Lake sediments dominated by autochthonous or allochthonous OC sources have contrasting properties [Meyers and Teranes, 2001] that is reflected in their susceptibility to microbial decomposition. Thus, sediments dominated by autochthonous material decay faster compared to more slowly decomposing sediments dominated by allochthonous inputs [Gudasz et al., 2012].
The OC fraction that is stored in the sediment is constrained by microbial decomposition. Temperature has been shown to be a main controlling factor of sediment OC mineralization [Bergström et al., 2010; Gudasz et al., 2010; Cardoso et al., 2014]. While differences in temperature sensitivities for the mineralization of fast and slowly decomposing soil OC are intensely debated [von Lützow and Kögel-Knabner, 2009], the temperature sensitivity for the mineralization of sediment OC of allochthonous or autochthonous origin is virtually unknown. A difficulty in elucidating the temperature sensitivity of fast versus slowly decomposing
Journal of Geophysical Research: Biogeosciences
RESEARCH ARTICLE
10.1002/2015JG002928
Key Point:
• Similar temperature sensitivity across systems and within the seasonal scale
Supporting Information: • Supporting Information S1 Correspondence to: C. Gudasz, cgudasz@princeton.edu Citation:
Gudasz, C., S. Sobek, D. Bastviken, B. Koehler, and L. J. Tranvik (2015), Temperature sensitivity of organic carbon mineralization in contrasting lake sediments, J. Geophys. Res. Biogeosci., 120, 1215–1225, doi:10.1002/ 2015JG002928.
Received 22 JAN 2015 Accepted 17 JUN 2015
Accepted article online 21 JUN 2015 Published online 15 JUL 2015
©2015. The Authors.
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distri-bution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
OC lies in the fact that what we measure is an apparent temperature response (i.e., apparent Ea). The apparent
Eais the expression of the overall temperature sensitivity of OC decomposition by the microbial community [e.g., Craine et al., 2010] and results from the integration of various temperature-dependent processes at different scales [Ågren and Wetterstedt, 2007; Conant et al., 2011].
Based on soil studies, different competing hypotheses have emerged to explain apparent temperature sensitivity of microbial OC decomposition [von Lützow and Kögel-Knabner, 2009; Conant et al., 2011]. The temperature sensitivity of slowly decomposing OC has attracted particular interest due to the large contribution of this pool to the soil carbon stocks [e.g., Davidson et al., 2000; Knorr et al., 2005]. According to the Arrhenius equation [Arrhenius, 1889], the temperature sensitivity of microbial decomposition should increase with increasing activation energy (Ea) of a reaction [Bosatta and Ågren, 1999; Davidson and
Janssens, 2006]. Hence, the carbon-quality-to-temperature hypothesis postulated by Bosatta and Ågren [Bosatta and Ågren, 1999] argues that the net Ea for the decomposition of complex molecules is higher
due to a higher number of enzymatic steps needed to release carbon as carbon dioxide. Complex molecules (i.e., lower quality) should exhibit higher temperature sensitivity than simple monomers (i.e., higher quality). Although allochthonous and autochthonous OC sources are complex mixtures, in general, they can be considered as having lower and higher quality (i.e., slow and fast decomposing) [Koehler et al., 2012; Guillemette et al., 2013]. Assuming that temperature sensitivity of decomposition at the molecular level also holds at the soils sample level [Janssens and Vicca, 2010], the slowly decomposing OC (which exhibits higher Ea) should respond stronger to increasing temperature, than
fast decomposing OC, which exhibits lower Ea[Conant et al., 2008; Craine et al., 2010].
However, contradicting empirical studies [e.g., von Lützow and Kögel-Knabner, 2009] makes it difficult to demonstrate a universal relationship between soil OC decomposition and temperature. Various factors associated with the physicochemical environment (e.g., soil pH, humidity, nutrients, and oxygen) and different effects associated with longer incubation periods can lead to differential effects of temperature on soil OC decomposition.
The time scale is important when considering the temperature sensitivity of OC mineralization. The depletion of short-lived fast decomposing OC, at higher temperatures during incubation of confined samples over longer time, could lead to an increase in the apparent temperature sensitivity. Hence, increasing incubation time lead to a decrease in soil respiration, which was coupled to an increase in apparent Ea,
but only after 150 days [Craine et al., 2010]. Alternatively, longer incubation time may result in decreased soil respiration, coupled to decreased microbial biomass and thermal adaptation of the microbial community [Bradford et al., 2008] and thus decreasing apparent Ea. Short time scale responses might
reveal only transient effects. It is virtually unknown how temperature sensitivity of sediment OC mineralization changes over longer time scale, which is critical if we try to understand future responses to climate warming.
It is not evident to what extent that the patterns of temperature sensitivity described for soils are valid also for lake sediment OC mineralization. Considering the large amounts of OC stored in inland water sediments [Dean and Gorham, 1998] and the high global rates of accumulation [Tranvik et al., 2009], it is important to find out whether temperature sensitivity is different for the allochthonous OC, being washed out from soils and settled to the lake bottoms, compared to the autochthonous OC originating from aquatic primary production. The temperature sensitivity of OC mineralization rates is not only important for the total balance between OC mineralization and preservation but may also influence how quickly different types of OC are mineralized and could therefore have major impact on OC cycling and composition over time. For example, if slowly decomposing OC has high-temperature sensitivity, a greater mineralization and loss of presently preserved carbon stocks could be expected in a warmer climate.
In this study we explore the relationship between sediment OC mineralization and temperature during a five-month incubation of two contrasting boreal lake sediments, with allochthonous versus autochthonous dominated OC sources, as well as of properties (i.e., slow versus fast decomposing OC). We show that for the duration of incubation, which is equivalent to seasonal scale, temperature sensitivity of OC mineralization was similar over time and among lakes with contrasting sediment OC characteristics. We suggest that for the seasonal cycle of supply and degradation of OC, temperature sensitivity of sediment OC mineralization is similar and encompasses differences in organic matter composition.
2. Methods
2.1. Study Lakes and Experimental Design
Intact sediment cores were sampled with a gravity corer (inner diameter = 59 mm; Uwitech, Mondsee, Austria) at the deepest point of two lakes in south-central boreal Sweden under ice cover in February 2010. Svarttjärn is a small oligotrophic lake rich in humic matter and with a low contribution of autochthonous OC in the sedimentationflux [von Wachenfeldt and Tranvik, 2008; Gudasz et al., 2012]. Vallentunasjön is a eutrophic lake with high nutrient concentrations and high productivity of phytoplankton and macrophytes [Boström et al., 1989; Brunberg and Boström, 1992; Rydin et al., 2010; Gustafsson and Rydin, 2015]. In a recent water quality survey [Gustafsson and Rydin, 2015], the average between 2007 and 2014 of total phosphorus (TP) concentration in Vallentunasjön was 63.9 ± 5.7μg L 1, while a seasonal survey in Svarttjärn showed TP of 15.1 ± 6.1μg L 1 [Gudasz et al., 2012], most of which is organically bound to dissolved humic matter. The dissolved organic carbon (DOC) concentration was similar in both lakes, with 26 and 28 mg L 1in Vallentunasjön and Svarttjärn, respectively. However, the DOC-specific absorbance at 250 nm (A250/DOC), an indicator of terrestrial humic material [McKnight and Aiken, 1998], was about 5 times higher in Svarttjärn (for details see Gudasz et al. [2010]). More limnological characteristics of the two lakes can be found in Table S1 in the supporting information.
At the time of sampling, bottom temperature was 4.8°C and the sediment surface was anoxic in both lakes. The sediment cores were transported in insulated boxes to the laboratory and kept at in situ temperatures. In the laboratory and within the same day of sampling, the upper 5 cm of the sediment was sliced off and transferred to polycarbonate incubation tubes (length = 400 mm and inner diameter = 54 mm), keeping the sediment structure with minimum disturbance. The method we have developed to transfer the sediment does not entirely eliminate sediment disturbance during sampling but it minimizes disturbance and allowed sampling without any visible mixing of the sediment. Approximately 0.6 L of water was kept above the sediment. The incubation tubes were equilibrated and acclimated at the incubation temperature for a period of 10 days, open to the atmosphere and with continuous mixing of the water column. The water column mixing was achieved through a magnetic stirring system. A magnet-containing buoyant Eppendorf vial was placed in each tube, and the tubes were immersed in an insulated, dark water bath arranged in a circular pattern. Four arms connected to an axle and equipped with magnets were rotating outside the tubes, moving the Eppendorf vials inside the sediment tubes, to gently mix the water column without resuspending the sediment. For both lakes, we then incubated three sediment tubes at each of the temperatures.
We used six temperature treatments for the experiment. To maintain constant temperatures, we used insulated water baths connected to external refrigerated circulators (Julabo, F 25 ED, Seelbach, Germany). The temperature inside the water baths was logged at 5 min intervals (Fluke 2625A, Hydra Series II, Everett, USA) with fast-response Fluke 80PK-1 thermocouples. The thermocouples were adjusted against a reference thermometer (Hart Scientific 1522, American Fork, USA), equipped with a reference probe (Hart Scientific PRT 5613). Mean temperatures (±SD) throughout the duration of the experiment (150 days) were 0.99 ± 0.03, 2.97 ± 0.07, 5.04 ± 0.06, 7.99 ± 0.08, 13.01 ± 0.03, 21.06 ± 0.06°C.
2.2. Sediment OC Mineralization
OC mineralization is defined as production of dissolved inorganic carbon (DIC) and methane. Methane release was tested at 21°C for both lakes, at the end of the experiment, and was below 1% of the DIC production. Thus, we use DIC production as a measure of OC mineralization. Methane concentrations were determined using a gas chromatograph with aflame ionization detector (GC-FID, Agilent Tech 7890A with methanizer). Incubations were made in the dark and the sediment OC mineralization rate was measured as the change in DIC (dissolved inorganic carbon) concentration in the mixed water overlying the sediment, 4, 17, 35, 58, 86, 100, and 150 days into the experiment. During each rate measurement occasion, the incubation tubes were closed headspace-free, with gas-tight stoppers for 45 to 192 h (depending on the temperature, with the shortest measurement times at 13 and 21°C), which were the durations needed to confidently measureable differences in DIC concentrations. Two replicate measurements in Svarttjärn at 3°C and during the fourth rate measurement occasion were lost. Oxygen concentration at the end of the closure period always exceeded 3 mg L 1, with the exception of one core out of 252 on day 4 and another
core on day 17 of the experiment when it was ~1 mg L 1. At the start and end of tube closure, water samples (20 mL) were withdrawn through sampling ports while pushing down the stoppers into the tubes to avoid headspace formation. Once each rate measurement closure wasfinished, the tubes were kept open and with continuous water column mixing in order to maintain oxic conditions until the next mineralization rate measurement and surface lake water was added to keep water volume constant. All data on sediment OC mineralization can be found in the supporting information.
Sediment incubations are likely have a level of uncertainty due to the experimental manipulations. The sediment incubation measurements we have carried out were meant to measure the potential, apparent mineralization rates of widely different sediments under comparable experimental conditions. It is questionable, however, if the rates are representative for in situ sediment OC mineralization in an absolute sense, but the comparison of the apparent OC mineralization we observed is robust and representative with respect to the widely different types of sediment.
2.3. Temperature Sensitivity
The temperature sensitivity was calculated as the slope of a linear regression between the logarithm of the sediment OC mineralization rate and temperature (°C). Apparent Ea (kJ mol 1) representing another
expression of temperature sensitivity was calculated as described in Craine et al. [2010]. 2.4. Dissolved Oxygen Measurements
Duringfield sampling, dissolved oxygen concentration and temperature at the lake bottom were measured with a WTW Oxi 340i (Weilheim, Germany). During laboratory incubation, dissolved oxygen concentrations was monitored with an optical sensor system (Oxy-10 mini) and PSt3 oxygen sensor spots (PreSens–Precision Sensing GmbH, Regensburg, Germany).
2.5. Dissolved Inorganic Carbon
DIC concentrations were measured using a Sievers 900 total organic carbon analyzer (GE Analytical Instruments, Manchester, UK), with a precision of<1.5% relative standard deviation and an accuracy of ±2% or 0.5 ppb, whichever is greater. During DIC measurements, water samples were kept cool at 3°C. 2.6. Elemental Analyses
At the end of the experiment, each incubated core was sliced into 1 cm sections, frozen, and freeze-dried. Total carbon and total nitrogen content were determined with a CHN analyzer (ECS 4010, Costech International, Milan, Italy). Instrument performance was checked using an acetanilide standard. Sediment C/N atomic ratios were calculated by dividing percent carbon with percent nitrogen and then converted to atomic ratios by multiplying with 1.167 (the ratio of atomic weights of nitrogen and carbon). All data on sediment elemental analyses can be found in Table S2 in the supporting information.
2.7.13C-nuclear Magnetic Resonance Spectroscopy
The chemical composition of bulk organic matter in the 0–1 cm layer of sediment was analyzed by solid-state
13C cross-polarization magic angle spinning (CP/MAS) nuclear magnetic resonance (NMR) spectroscopy
(Bruker DSX 200). A13C resonance frequency of 50.32 MHz and a spinning speed of 6.8 kHz were applied. Between 28,000 and 31,000 scans were accumulated, and a line broadening of 25 Hz was applied. The13C chemical shifts were calibrated relative to tetramethylsilane (0 ppm). The relative contributions of the various C groups were determined by integration of the signal intensities in their respective chemical shift regions. The region from 10 to 45 ppm was assigned to alkyl C, from 45 to 110 ppm to O-alkyl C, from 110 to 160 ppm to aromatic C, and from 160 to 220 ppm to carboxyl, carbonyl, and amide C. The one time, snapshot NMR analysis of the sediment was used to provide a qualitative description of the sediment. All data on sediment NMR spectra can be found in the supporting information.
2.8. Statistical Analyses
Factors regulating sediment OC mineralization were tested using a random-slope linear mixed-effects model [Schielzeth and Forstmeier, 2009], which accounted for the correlation between repeated measurements on the same subject and lack of spatial independence among the sampled sediment cores. DIC production data were log-transformed, while temperature was mean centered and standardized by z transformation according to Schielzeth [2010]. The model contained the linear and interaction terms of temperature, time
and lake asfixed effects, and sediment cores nested in time as random effects. Afirst-order temporal autore-gressive process, which assumes that correlation between measurements decreases with increasing time dis-tance, was included in the model. We used the lme function from the R-package nlme [Pinheiro et al., 2014]. Model adequacy was checked using residual plots [Crawley, 2009; R Development Core Team, 2010]. P values were multiplicity adjusted using the single-step method pro-vided in the R-package multcomp [Hothorn et al., 2008].
2.9. Apparent Turnover Time of Sediment Organic Carbon We estimated the apparent turnover time of sediment OC based on the fraction that was lost through miner-alization, accounting for the fact that not all the OC will be mineralized. Burial efficiency (i.e., OC burial/OC deposition) averages 66% and 22% in boreal lakes dominated by allochthonous and autochthonous OC, respectively [Sobek et al., 2009]. Assuming that these averages apply to the study lakes, this means that 34 and 78%, respectively, of the OC in Svarttjärn and Vallentunasjön will not be buried and can be regarded as a“labile” carbon pool. Hence, for this remainder fraction, we calculated the carbon pool size for the 0–5 cm layer. We have then used the average sediment OC mineralization throughout the 150 day duration, at each of the temperatures, to calculate the apparent turnover time of this nonburied organic carbon pool. There is uncertainty in estimat-ing OC burial efficiency as described by Sobek et al. [2009], and the true organic carbon burial efficiency of OC in Vallentunasjön and Svarttjärn may be different from the applied averages. However, our calculations high-light overall differences in apparent turnover times of OC in lake sediments with predominantly autochtho-nous and allochthoautochtho-nous sources. Data and calculations on the apparent turnover time can be found in the supporting information.
3. Results and Discussion
3.1. Sediment Characteristics
The sediments of the two studied lakes represent end members along a spectrum of OC origin and reactivity. The average C/N ratio in the 0–5 cm layer of the incubated sediment (n = 72 for each lake) was 21.2 ± 2.8 in the humic Svarttjärn sediment indicating a predominantly allochthonous OC source (i.e., more slowly decomposing) and 9.5 ± 3.7 in the eutrophic Vallentunasjön sediment, indicating the larger proportion of autochthonous OC (i.e., more rapidly decomposing). The complete data on sediment C/N ratios can be found in Table S2. The C/N ratio is a reliable general source indicator with high organic content [Meyers and Teranes, 2001], which mirrors the general characteristics of a eutrophic versus dystrophic lake (see Methods). The 13C NMR spectra (Figure 1) corroborate the allochthonous character of the Svarttjärn sediment showing a strong terrestrial imprint, with lignin signals at 150 ppm and 56 ppm, and a high share of aliphatic C (Table 1), possibly derived from cutin or suberin in the cuticula and cell wall of terrestrial plants. Although Vallentunasjön sediment also indicated the presence of a terrestrial imprint, it was richer in polysaccharides (peak at 72 ppm) as well as carboxylic acids and proteins (172 ppm), indicating that the OC is mainly derived from aquatic sources and more easily degraded than Svarttjärn sediment. In addition, Vallentunasjön sediment is comparatively rich in O-Alkyl C (45–110 ppm), indicating the presence of polysaccharides; Svarttjärn has a higher content of alkyl-C ( 10–45 ppm), i.e., methyl and methylene Figure 1.13C CP/MAS NMR spectra of the 0–1 cm layer of the studied
groups in aliphatic rings and chains (Table 1 and Figure 1). While total aromatic C (110–160 ppm) was similar in both lake sediments, Svarttjärn sediment displays a phenol peak at 150 ppm, which Vallentunasjön does not. Similarly, the shoulder at 56 ppm, indicative of methoxyl C in lignin, was more pronounced in Svarttjärn than in Vallentunasjön. On the other hand, Vallentunasjön sediment has a higher proportion of carboxyl C and amide C (172 ppm) than Svarttjärn. Even though the two study lakes are very different in character (see Methods), their sediment will still be a mixture of allochthonous and autochthonous OC. Since the 13C NMR method we have used is qualitative or semiquantitative, it will detect similar compounds and therefore the spectra are likely to look rather similar. Moreover, structures that are difficult to degrade (such as aromatics derived from vascular plants) will not be degraded in the sediment and will accumulate such that they will be visible in a qualitative analysis, even in a lake with large input of readily degradable OM such as Vallentunasjön. Furthermore, Vallentunasjön has a well-developed macrophytes belt [Rydin et al., 2010] and thus a vascular plant organic matter source to the sediment. 3.2. Temperature Sensitivity
Sediment OC mineralization increased with increasing temperature in both lakes (Figure 2). There was no significant change in sediment OC mineralization and its temperature sensitivity between lakes and over time (Figure 3 and Table 2). Temperature sensitivity of sediment OC mineralization over longer term (five months; Figure 2) was similar to that derived from short-term incubations (between 37 and 94 h) previously measured in the same lakes [Gudasz et al., 2010]. Temperature sensitivity obtained from pooled data of Svarttjärn and Vallentunasjön was also similar with that observed for a larger set of different lakes, geographically widely distributed [Gudasz et al., 2010]. Hence, this and previous studies suggest that apparent temperature sensitivity of OC mineralization was similar for sediments of varying composition and in contrast to the carbon-quality-to-temperature hypothesis [Bosatta and Ågren, 1999].
The duration of the incubation can play an important role when studying temperature sensitivity. Short-term soil-warming experiments in the laboratory (e.g., <100 days) have been criticized [von Lützow and Kögel-Knabner, 2009] because they mainly reflect the mineralization of the most active, labile carbon compounds, possibly masking the temperature response of the larger, more slowly decomposing OC pool [Davidson et al., 2000; Knorr et al., 2005]. In soil-warming experiments in the field, respiration rates often return to prewarming conditions after extended periods of incubation. Different mechanisms have been proposed to explain this pattern, from depletion of labile carbon to thermal adaptation of microbial Figure 2. Temperature sensitivity of sediment OC mineralization. Circles
represent mineralization rates measured during the 150 d experiment, n = 18 for each lake and for n = 7 rate measurement occasions. Thefitted solid line corresponds to a linear regression estimate. The y axis is represented on a log-scale. Statistical effect analysis was conducted using linear mixed-effects model (see Table 2).
Table 1. Relative Contribution of Major Chemical Shift Regions in the13C CP/MAS NMR Spectra of the 0–1 cm Layer of Sediment in the Studied Lakes
Lake
Alkyl C O-Alkyl C Aromatic C Carboxyl C
0–45 ppm 45–110 ppm 110–160 ppm 160–210 ppm
Vallentunasjön 31% 45% 9% 12%
respiration [e.g., Davidson and Janssens, 2006; von Lützow and Kögel-Knabner, 2009]. Our experiment lasted for 150 days, similar to seasonal length in boreal lakes (e.g., ice cover and summer stratification). Temperature sensitivity of sediment OC mineralization derived from long-term incubations at constant temperatures may result in confounding the influence of biochemical composition with microbial acclimation processes. However, the effect of time on sediment OC mineralization was not significant across temperatures and lakes in our study (see Table 2), indicating that the temperature sensitivity of sediment OC mineralization was similar over a relevant time scale encompassing annual events of sedimentation and mineralization. Furthermore, a negative relationship between respiration rate and temperature sensitivity, as apparent in soils [Craine et al., 2010], was not observed for the sediment mineralization, neither over time nor in lakes with contrasting OC composition (Table 2). Possibly, incubations extending over several years in absence of input of new substrate from sedimentation may reveal a higher temperature sensitivity of the more slowly decomposing substrate pools [Bosatta and Ågren, 1999]. However, this time scale is not relevant for the dynamics of input and decay of organic matter in boreal lake sediments and for the seasonal temperature dynamics.
The fraction of the total OC pool that was lost during 150 days of incubation between 1 and 21°C averaged between 0.4 and 2.8% (i.e., 5.9–32 mg C or 2.6–14 g C m 2) in the humic Svarttjärn and 3.1 to 14.8% (i.e., 18.7–77.1 mg C or 8.1–33.7 g C m 2) in the eutrophic Vallentunasjön. The total carbon loss at 21°C in Vallentunasjön was only 2.4 times (average across temperatures 2.8 ± 0.4) higher than the loss in Svarttjärn, even though Vallentunasjön sediment is rich in readily decomposable autochthonous OC and Svarttjärn sediment is largely made of slowly decomposing allochthonous OC. In comparison, the respiration rate at 20°C of a wider variety of soils (root-free in the laboratory) and plant litter varied by factors of 70 and 77 and between soil and litter in total by a factor of 103, respectively [Craine et al., 2010]. Hence, mineralization rates exhibit far less variability between contrasting lake sediments compared to the variation across soils and litter.
Figure 3. Temporal variation in temperature sensitivity of sediment OC mineralization. Circles represent the slope of linear regression between temperature and sediment OC mineralization (n = 18), log-transformed.
Table 2. Results of the Linear Mixed Effects Model on the Relationships Between Sediment OC Mineralization Rates (Log-Transformed Before Analysis) and Standardized Temperature, Time, Lake (Svarttjärn, Sv and Vallentunasjön, Va) and Their Interactionsa
Full Model Test Statistics Group Mean Parameter Estimates Predictor DF t value Unadjusted P Value Multiplicity Adjusted P Value Parameter Mean ±SE
Intercept 209 66.98 <0.001 <0.001 Intercept of Sv 1.54 0.02
Lake 28 21.06 <0.001 <0.001 Intercept of Va 1.99 0.02
Temperature 4 10.51 0.0005 <0.001 Temperature slope of Sv 0.24 0.02
Temperature × lake 28 1.13 0.2676 0.873 Temperature slope of Va 0.22 0.01
Time 209 0.84 0.4013 0.972 Time slope of Sv 0.01 0.02
Time × lake 209 1.02 0.3069 0.920 Time slope of Va 0.01 0.01
Temperature × time 209 1.08 0.2803 0.896 Temperature × time of Sv 0.02 0.02
Temperature × time × lake 209 1.57 0.1180 0.580 Temperature × time of Va 0.01 0.01
a
The left part gives the t table of the full model with the univariate and multiplicity-adjusted P values. Sv was the reference group against which contrasts were tested. Group mean parameter estimates are given in the right part. Parameter estimates differ from those in Figure 2 because in the lme models standardized temperature was used.
The Eaof OC mineralization varied within a narrow range in the two lakes with no trend over incubation time
(see Table 2), from 47 and 64 kJ mol 1in Svarttjärn and between 45 and 54 kJ mol 1in Vallentunasjön. The average activation energy values in Svarttjärn, Ea= 56 ± 6 kJ mol 1, and Vallentunasjön, Ea= 50 ± 4 kJ mol 1,
were close to the lowest observed Ea for soil OC and litter decomposition (Ea= 51 kJ mol 1) [Craine et al.,
2010]. Hence, while the Eafor a wide range of root-free soils and plant litter decomposition varied by a factor
of 2.9 and 1.5, respectively [Craine et al., 2010], it was remarkably similar in our contrasting lake sediments. The similarity of Ea across contrasting lake sediments, dissimilar to the wider range of Ea for OC decomposition among different soils, suggests that either the decomposing OC is more similar among sediments than among soils, or that different mechanisms control mineralization and temperature sensitivity in soils and in lake sediments. These findings point toward fundamental differences in OC mineralization in sediments as compared to soils [e.g., Hedges and Oades, 1997] and most likely to differences in the integration of the various temperature dependent processes such as substrate release in the environment, diffusion and uptake [Ågren and Wetterstedt, 2007]. We argue in the following that the physical characteristics of the aquatic environment, in general, and of the sediment water interface in particular set boundaries to sediment OC mineralization and its temperature dependence.
The supply rate of materials to the sediment surface and to microbial cells is regulated by physical transport mechanisms including advection, turbulence, and diffusion [Fenchel et al., 1998]. Among these, molecular diffusion is the most important regulator of substrate flux to cells, even in highly turbulent water [Jørgensen, 2001]. Temperature can to a large degree alter the transport characteristics of various gasses, ions, and molecules not only within the sediment (i.e., diffusion in porewater to cell surfaces) but also across the diffusive boundary layer (DBL), a water layer of up to a few mm in thickness on top of the sediment surface, where molecular diffusion is the main transport mechanism of solutes [Boudreau and Jørgensen, 2001]. The transport of solutes across the DBL is an important regulator of biogeochemical processes in the sediment [Brand et al., 2009] and depends on the concentration gradient, the thickness of the DBL (which in turn depends on turbulent movements of the bottom water), and on the molecular diffusion coefficient of the solute (which in turn depends on temperature) [Jørgensen, 2001]. Hence, the constraints imposed by the transport through the DBL together with the temperature effects on diffusion make the DBL to act as a temperature-dependent barrier, limiting solute exchange between water and sediment, and affecting the temperature response of sediment OC mineralization. Similarly, a reduced temperature effect due to diffusive constraints has been suggested for aerobic respiration in marine sediments [Thamdrup et al., 1998]. As a solute’s molecular diffusion coefficient is typically about 4 orders of magnitude greater in air than in water, the contribution to the overall temperature sensitivity from physical transport processes presumably is substantially greater in sediments and waterlogged soils compared to aerated soils.
Ourfinding of the similar temperature sensitivity in contrasting lakes sediments with longer incubation time, and previously shown by Gudasz et al. [2010] with short-term incubations, may be explained by the interplay of several factors including the diffusion-controlled transport at the sediment-water interface and in subsurface sediments and the availability of oxygen from overlaying water [Thamdrup et al., 1998]. These factors cause the apparent Eato be lower than in aerated soils.
Physico-chemical environmental variables can influence decomposition of fast and slowly decomposing OC and their response to temperature differently [von Lützow and Kögel-Knabner, 2009]. Factors affecting the catalytic activity of microbial enzymes and OC availability are likely to play an important role [Conant et al., 2011]. Protective mineral sorption affects OC availability in both soils and marine sediments [Hedges and Oades, 1997] but is not of major importance for OC burial efficiency (an indirect measure of OC mineralization) in freshwater lake sediments [Sobek et al., 2009]. Instead, anoxia exerts strong control on the mineralization of lake sediments. Unlike soils, lake sediments are anoxic below the very few top mm or cm, and the lack of oxygen has a strong impact on the sediment organic matter stabilization, by slowing down decomposition and in particular or allochthonous OC [Kristensen et al., 1995; Bastviken et al., 2003; Sobek et al., 2009]. We suggest that the constraints of an anoxic environment upon mineralization of OC in lake sediments contribute to the relative similarity in both rate and temperature sensitivity of mineralization, compared to the highly variable decomposition rates and temperature sensitivity observed in soils [Craine et al., 2010].
3.3. Apparent Turnover Time
A certain fraction of the OC that is deposited onto the sediment will escape microbial decomposition and eventually be buried over geological time scales. The fraction that is mineralized can be regarded as the “labile” sediment OC pool, i.e., the fraction of the sediment OC that escapes burial. We calculated the apparent turnover time for the top-most sediment layer (0–5 cm, see Methods), which harbors most of the biological activity [Haglund et al., 2003]. The appar-ent turnover time of this labile pool (Figure 4) varied on average between 5 and 32 years in Svarttjärn and between 3 and 11 years in Vallentunasjön, for the range of temperatures between 1 and 21°C. The turnover time of OC is even longer in the anoxic layers of the sedi-ment, where mineralization is slower. This is particularly important in sediments rich in more slowly decomposing OC (e.g., allochthonous OC [Kristensen et al., 1995; Bastviken et al., 2003; Sobek et al., 2009]).
Lakes differ greatly in OC delivery to the sediments, in productivity and watershed OC supply. Burial efficiency integrates the effect of a number of variables such as differences in lake morphometry [Ferland et al., 2014], oxygen exposure time [Sobek et al., 2009] and temperature [Gudasz et al., 2010]. However, we have shown that OC mineralization and in particular temperature has a strong control over the burial efficiency [Gudasz et al., 2010]. If we assume a similar temperature sensitivity of sediment OC mineralization among lakes and over time, as we have shown here, increasing mineralization rates as a result of a potential increase in temperature translates into a reduced OC burial efficiency and hence reduced burial, even if the amount of OC delivered to the sediments will be different between lakes.
4. Concluding Remarks
The focus of the present study was to compare the temperature sensitivity of sediment OC mineralization in lake sediments with a wide difference in organic matter composition, largely due to differences in dominant sediment OC source and composition (i.e., allochthonous versus autochthonous), as well as to elucidate whether different patterns in temperature sensitivity emerge beyond that of short time scale responses. We show that the temperature sensitivity of OC mineralization in lake sediments is strikingly similar across a wide range of organic matter composition and within the relevant seasonal time scales of supply and degradation of OC. Hence, the temperature sensitivity may not change significantly over time, even though the OC supply and quality, hence the absolute reaction rates, may change. However, factors other than temperature, such as DOC or nutrient load, may affect future mineralization rates in boreal lakes. We also suggest that the physical characteristics of the aquatic environment and in particular of the sediments and sediment-water interface largely govern sediment temperature sensitivity of the OC mineralization.
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Acknowledgments
The study was part of the research environment Lake Ecosystem Response to Environmental Change (LEREC), financially supported by FORMAS (the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning). Financial support for laboratory equipment was obtained from the Knut and Alice Wallenberg Foundation. We also acknowledge additional support from the Malméns Foundation to C.G., and from FORMAS to S.S. We thank Ingrid Kögel-Knabner and Markus Steffens for the13C NMR measurements and María Morales-Pineda, Erik Geibrink, and Ashraf Haque for help during sampling. To access the data in this article refer to the corresponding author.
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