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Ice core records indicate that atmospheric CH4 concentration ([CH4]) over the last 800 000 yr has varied from c. 350 ppb during glacial maxima to c. 800 ppb during interglacials (Loulergue et al., 2008). The reasons behind this natural variation are not fully understood, but changes in wetland CH4 emissions (Chappellaz et al., 1993, 1997) and the strength of the tropospheric sink (reaction with the OH radical) as a result of reductions in biogenic volatile organic compound (BVOC) fluxes from forests (Adams et al., 2001; Valdes et al., 2005; Kaplan et al., 2006) are possible major contributing factors.
During the Last Glacial Maximum (LGM), cool global temperatures (Guilderson et al., 1994; Jahn et al., 2005; Affek et al., 2008) and the presence of ice sheets across northern boreal latitudes (Abe-Ouchi et al., 2007) may have combined to limit the area of high-latitude wetlands and lower the rates of biogenic CH4 emissions (e.g. Chappellaz et al., 1993). Globally, however, wetland area at the LGM may have not differed substantially from that found at the present day, because of the expansion of wetlands onto exposed continental shelves (Kaplan et al., 2006) and a migration of boreal wetlands to regions south of the Northern Hemisphere ice sheet (Weber et al., 2010). A reduction in the atmospheric lifetime of CH4 as a result of an elevated atmospheric sink has been suggested as a possible alternative hypothesis to explain the low atmospheric [CH4] during the LGM (Valdes et al., 2005; Kaplan et al., 2006). However, the exact change in OH radical concentration in the atmosphere over glacial–interglacial cycles remains in doubt (Arneth et al., 2007). Proposed reductions in BVOC from terrestrial ecosystems during the LGM, caused by a contraction of global forests, may have been offset by increased BVOC at the leaf scale in response to the low atmospheric [CO2] present at this time (Possell et al., 2005; Wilkinson et al., 2009; Possell & Hewitt, 2010). In addition to this uncertainty, during isoprene oxidation in the atmosphere, OH radical recycling efficiency could potentially be as high as 40–80% (Lelieveld et al., 2008). Uncertainties in sink strength and wetland area during the LGM lead us to consider additional source-driven (wetland) processes to explain low atmospheric [CH4] during glacial periods.
Current approaches to explaining glacial–interglacial changes in CH4 recorded in ice cores are based on either ‘bottom-up’ or ‘top-down’ modelling. Bottom-up approaches simulate global-scale terrestrial carbon cycle processes that influence wetland CH4 emissions (e.g. Cao et al., 1996; Walter et al., 1996; Potter, 1997; Zhuang et al., 2004; Wania et al., 2009; Singarayer et al., 2011), and subsequent effects on atmospheric chemistry (e.g. Valdes et al., 2005; Singarayer et al., 2011). Top-down or inverse models infer the magnitude of wetland CH4 emissions by constraining atmospheric chemistry models with recorded ice core CH4 concentrations (Chappellaz et al., 1997; Brook et al., 2000; Dallenbach et al., 2000). These theoretical and experimental approaches provide insights into the effects of glacial conditions on CH4-relevant terrestrial biogeochemical processes at global and regional scales, such as reductions in net primary production (NPP) under glacial CO2 starvation.
Critically, we are unaware of experimental investigations into the direct effect of low LGM CO2 concentrations on wetland ecosystem carbon cycling processes or CH4 emissions complementing these earlier lines of enquiry. Consequently, the work presented here focuses on this unknown potential interaction. Previous work indicates that [CO2] is an important variable determining CH4 emissions from wetland ecosystems (Dacey et al., 1994; Megonigal & Schlesinger, 1997; Vann & Megonigal, 2003). Exposure of wetland ecosystems and mesocosms to elevated atmospheric [CO2] typically stimulates CH4 fluxes (Hutchin et al., 1995; Megonigal & Schlesinger, 1997; Saarnio & Silvola, 1999; Kang et al., 2001; Ellis et al., 2009). An increase in CH4 emissions results from an increase in NPP and increased allocation of plant photosynthates to the rhizosphere, with root exudates providing an important substrate for CH4 production (Chanton et al., 1995; Megonigal et al., 1999; Vann & Megonigal, 2003; Kim & Kang, 2008). However, during Pleistocene glacials, atmospheric [CO2] was approximately half the modern value (Luthi et al., 2008), and fossil evidence indicates that this imposes severe ‘CO2 starvation’ on the terrestrial biosphere. Trees in North America, for example, operated with a leaf-intercellular [CO2] approaching the CO2 compensation point for C3 photosynthesis (Van de Water et al., 1994; Ward et al., 2005). Under such conditions of carbon starvation, experimental studies (Polley et al., 1993; Kgope et al., 2010) and process-based modelling indicate substantially reduced terrestrial primary productivity and biomass (Beerling & Woodward, 2001; Harrison & Prentice, 2003; Pagani et al., 2009).
From these earlier studies, we hypothesize that CO2 starvation during glacial times exerted an important limiting effect on wetland CH4 fluxes to the atmosphere by decreasing the allocation of plant photosynthate to the rhizosphere, thereby limiting the substrate for CH4 production. To test this hypothesis, we established a replicated mesocosm-scale controlled environment experiment to examine the influence of LGM atmospheric [CO2] on wetland gaseous and dissolved CH4 dynamics, while also measuring pore water concentrations of volatile fatty acids (VFAs). VFAs are labile short-chain carbon molecules (e.g. acetate) that are used in methanogenesis. The study was conducted over two growing seasons on intact monoliths collected from two temperate British wetland ecosystems of contrasting nutrient status: a minerotrophic fen and an ombrotrophic bog. These two ecosystems represent contrasting ends of the peatland gradient (Charman, 2002). Fens receive water and nutrients from outside their boundaries and tend to be more nutrient-rich and alkaline. By contrast, bogs tend to receive all their water and nutrients from the atmosphere and are therefore acid and low in plant nutrients. In comparison to fens, bogs exhibit lower degradation rates (Aerts et al., 1999), lower methanogenic activity (Juottonen et al., 2005) and lower CH4 emissions (Nykänen et al., 1998) as a result of differences in biotic and abiotic factors (Belyea, 1996).
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Applying an LGM atmospheric [CO2] starvation treatment to temperate wetland mesocosms resulted in a contrasting CH4 emission response. Reducing atmospheric [CO2] from present-day to glacial maxima concentrations suppressed both gaseous CH4 emissions and pore water DM concentration in minerotrophic fen mesocosms, whereas the ombrotrophic bog mesocosms showed no response (Figs 2, 3a). DM pore water concentrations showed a particularly clear differential response to CO2 starvation, with fen mesocosms exhibiting a c. 50% decrease in DM concentration compared with no change in their bog counterparts (Fig. 3b). Other studies where wetlands were exposed to elevated atmospheric [CO2] have shown increased CH4 emissions (Hutchin et al., 1995; Megonigal & Schlesinger, 1997; Saarnio & Silvola, 1999; Saarnio et al., 2000; Kang et al., 2001; Ellis et al., 2009) but the effect on DM concentration in pore waters is less straightforward. Marsh et al. (2005) showed no significant effects of elevated CO2 treatment on DM concentration compared with ambient controls on a brackish marsh after > 10 yr of exposure, as did Cheng et al. (2005) (P > 0.05) when investigating the same treatment effect on DM concentration at 10 cm below the surface in rice (Oryza sativa) paddy soil. By contrast, Keller et al. (2009) measured an increased DM concentration in pore waters after a 5-yr period exposing a brackish marsh to elevated atmospheric [CO2]. Our results therefore provide further evidence that changing atmospheric [CO2] does not automatically change DM concentration in pore waters or gaseous CH4 flux from all wetland types.
The response of wetland ecosystems to changing atmospheric [CO2] may be contingent on trophic status (as highlighted in this study) as a result of differences in biotic and abiotic variables that control CH4 production and oxidation (e.g. pH, microbial diversity, plant functional groups and plant productivity). We therefore propose three possible reasons for the different responses of fen and bog mesocosms to CO2 starvation in terms of CH4 dynamics: contrasting nutrient limitation; opposing dissolved CO2 concentrations and dominant CH4 production pathways within the rhizosphere; and differences in soil-derived CO2 supplemented photosynthesis.
Low nutrient concentrations in ombrogenous bogs lead to low photosynthetic activity, plant growth, plant biomass, microbial biomass, ecosystem respiration and the overall decay rate of litter (Aerts et al., 1992, 2001; Basiliko et al., 2006). These factors may combine to limit CH4 emissions from bogs such that they are insensitive to changes in atmospheric [CO2] (Freeman et al., 2004). Hence, wetlands are unlikely to respond to CO2 starvation with a decrease in CH4 flux if nutrient availability is the dominant limitation. By contrast, if nutrient availability is less of a dominating factor for CH4 production, then reducing the atmospheric [CO2] may limit photosynthesis and plant production (Polley et al., 1993; Pagani et al., 2009) and ultimately the supply of fresh labile carbon substrate to methanogens (Whiting & Chanton, 1993; Chanton et al., 1995). The majority of root exudates tend to be lower molecular weight compounds (Walker et al., 2003), making them readily available for obligate proton-reducing acetogens and methanogens to utilize. However, under low atmospheric CO2 concentrations, the influence of nutrient availability on ecosystem productivity is reduced (Bazzaz, 1990) as atmospheric [CO2] becomes the predominant constraint on photosynthesis in C3 plants.
Our effort to infer the effect of CO2 starvation on plant related methanogenic substrate supply, from analysis of seasonal changes in pore water VFAs proved inconclusive (Fig. 3c). Bog mesocosms showed no difference between ambient and simulated LGM [CO2] during year 1 or 2 (P > 0.05), whereas the fen simulated LGM mesocosms had a higher concentration in year 1 (P < 0.05), and no difference in year 2 between the treatments (P > 0.05). The highest acetate concentrations in both ecosystem types were measured during spring. These peaks represent an imbalance between the production and consumption of acetate in the rhizosphere, created by low temperatures allowing homoacetogenic bacteria to outcompete acetotophic methanogens and bacteria for H2 in the rhizosphere (Kotsyurbenko et al., 1996, 2001; Shannon & White, 1996; Duddleston et al., 2002; Hines et al., 2008; Hoj et al., 2008). As temperature increases, this shifts the balance in favour of acetoclasitc methanogenesis, resulting in acetate consumption in the rhizosphere and an increase in dissolved pore water [CH4] and gaseous CH4 emissions in the summer (Fig. 3) (Sugimoto & Wada, 1993; Shannon & White, 1996).
With no direct evidence of a reduction in root exudates in our experiment, we suggest the conflicting CH4 response may be attributable to different dissolved CO2 concentrations and dominant CH4 production pathways within the rhizospheres. Autotrophic and heterotrophic respiration within the rhizosphere elevates the concentration of dissolved CO2 within wetland pore waters (Smolders et al., 2001; Keller et al., 2009). The more neutral pore waters associated with fen ecosystems (Kang et al., 2001) do not favour the accumulation of dissolved CO2 as the equilibrium between the carbon species (CO2 : H2CO3 and HCO3− : CO32−) is shifted towards HCO3− because of the pH. By contrast, bogs have lower pH values and therefore an equilibrium that selects for the accumulation of dissolved CO2. As a result, it is possible that dissolved CO2 in simulated LGM mesocosms remained unchanged in the experiment. This would have significant implications for CH4 production as bog and fen mesocosms have contrasting dominant CH4 production pathways (Galand et al., 2010). Bogs that are Sphagnum-dominated show predominance for the hydrogentrophic CH4 production pathway (CO2 : H2) (Lansdown et al., 1992; Chanton et al., 1995; Duddleston et al., 2002; Horn et al., 2003; Hornibrook & Bowes, 2007), whereas nutrient-rich fens contain more methanogens that are obligate acetotrophs (Galand et al., 2005; Juottonen et al., 2005). Maintaining the aquatic source of CO2 in the simulated LGM bog mesocosms may have preserved CH4 emissions at levels associated with modern-day atmospheric [CO2] conditions.
Contrasting dominant CH4 production pathways explain why acetate concentrations measured in this study were higher in the bog than in the fen (Fig. 3c). Low pH values that are associated with bogs result in lower acetate turnover and a dominance of hydrogentrophic methanogenesis (Kotsyurbenko et al., 2007); consequently, acetate tends to accumulate in these ecosystems (Hines et al., 2001). By contrast, there is a higher demand for acetate in fens because of a greater presence of obligate acetotrophs (Galand et al., 2005), and hence CH4 emissions from minerotrophic wetlands could be susceptible to CO2 starvation without the drop in productivity being reflected in rhizosphere acetate concentration, as efficient removal would obliterate any potential signal.
Plant assemblage variations between the fen and bog mesocosms and a difference in utilization of soil-derived CO2 to supplement photosynthesis could also be part of a possible explanation for the contrasting CH4 dynamics we measured. Bog mesocosms in this study were mainly dominated by Sphagnum and Hypnaceous mosses and contained substantially fewer vascular plants compared with the fen mesocosms. The water table was maintained just below the surface in our experiment, therefore limiting the amount of CH4 oxidation in the mesocosms; however, Sphagnum mosses have been shown to form symbiotic relationships with methanotrophes in the hyline cells of the plant and on stem leaves (Raghoebarsing et al., 2005). The symbiosis results in the creation of CO2 as a result of O2 derived from photosynthesis driving methanotrophy of CH4 (Turetsky & Wieder, 1999), a CH4 recycling reaction that may also account for low CH4 emissions from Sphagnum areas. This CH4-derived CO2 provides an additional carbon source to submerged Sphagnum species in addition to that available from the atmosphere, and autotrophic and heterotrophic respiration. It is estimated that CH4-derived carbon accounts for between 5 and 35% of CO2 assimilated by Sphagnum (Raghoebarsing et al., 2005; Kip et al., 2010; Larmola et al., 2010). Consequently, Sphagnum-dominated bog mesocosms in our study may not have fully altered their physiological processes in response to atmospheric CO2 starvation as a result of the supplementing of photosynthesis with subsurface CO2. Therefore, it may be that plant assemblage is responsible for the contrasting bog and fen mesocosm response measured in this study, as this has a significant influence on dominant CH4 production pathways (Hines et al., 2008), the amount of rhizosphere supplemented photosynthesis (Raghoebarsing et al., 2005) and CH4 oxidation (Parmentier et al., 2011) and warrants further investigation.
Potential implications of findings
Our results suggest that CH4 emissions from minerotrophic temperate wetlands at the LGM may have been disproportionately affected by CO2 starvation when compared with ombrotrophic bogs occupying unglaciated boreal regions. Furthermore, mesocosm CH4 emissions exhibited a significant positive correlation with temperature and day length in year 2 (Fig. 4), with peaks in CH4 flux during the warmest periods (Figs 2, 3a), in agreement with laboratory (Thomas et al., 1996; Daulat & Clymo, 1998; Gauci et al., 2004) and field studies (Dise, 1993). In addition to this well-established relationship, our results indicate that the largest suppressions in fen CH4 flux induced by LGM atmospheric [CO2] occurred when temperature limitation on carbon mineralization was at its lowest during the warm summer months at temperatures > 15°C. Methanogen communities operate more rapidly, and increase diversity and relative abundance at temperatures > 10°C (Hoj et al., 2008); consequently, we hypothesize that, during the summer, CH4 emissions from the CO2-starved fen switched from being temperature-limited to being substrate-limited. Therefore, the response of wetland CH4 emissions to glacial atmospheric [CO2] may also be moderated by latitudinal temperature gradients. In which case, the largest suppression in wetland CH4 flux at the LGM would have been in the low latitudes, with a diminishing effect at higher latitudes. As a consequence, the warm-temperate and tropical wetland CH4 source may have responded sensitively to CO2 starvation during glacial episodes, a theory that is supported by modelling estimates in conjunction with carbon isotope ratios in CH4 found within ice cores (Fischer et al., 2008; Singarayer et al., 2011). Because lower latitude wetlands were probably the dominant source of CH4 during the LGM (Chappellaz et al., 1993; Dallenbach et al., 2000; Fischer et al., 2008; Weber et al., 2010; Singarayer et al., 2011), this challenges the assumption that global wetland CH4 emissions at the LGM would have been of similar magnitude to modern-day emissions (Kaplan et al., 2006).
In summary, we demonstrate that the low LGM atmospheric [CO2] significantly limited gaseous CH4 flux from, and DM concentration in, minerotrophic wetland ecosystems, while having no effect on ombrogenous bogs. The exact mechanism(s) that causes this heterogeneous response to glacial atmospheric [CO2] remains to be established. Recent studies suggest that glacial–interglacial variations in atmospheric [CH4] are caused by variations in global wetland CH4 source strength in response to changing orbital insolation patterns and greenhouse gas concentrations (Singarayer et al., 2011). Our experimental results support this hypothesis and provide direct evidence that wetland biogeochemical processes are sensitive to the effects of atmospheric glacial [CO2].