Interactions between Elevated CO2 and Warming Could Amplify DOC

Environ. Sci. Technol. 2007, 41, 3146-3152

Interactions between Elevated CO2 and Warming Could Amplify DOC Exports from Peatland Catchments N A T H A L I E F E N N E R , * ,† C H R I S T O P H E R FREEMAN,† MAURICE A. LOCK,† HARRY HARMENS,‡ BRIAN REYNOLDS,‡ AND TIM SPARKS§ School of Biological Sciences, Memorial Building, University of Wales, Bangor, Deiniol Road, Bangor, Gwynedd, LL57 2UW, UK, NERC, Centre for Ecology and Hydrology, Bangor Research Unit, Orton Building, University of Wales, Bangor, Deiniol Road, Bangor, Gwynedd, LL57 2UP, UK, and NERC, Centre for Ecology and Hydrology, Monks Wood, Abbots Ripton, Huntingdon, Cambridgeshire, PE28 2LS, UK.

Peatlands export more dissolved organic carbon (DOC) than any other biome, contributing 20% of all terrestrial DOC exported to the oceans. Both warming and elevated atmospheric CO2 (eCO2) can increase DOC exports, but their interaction is poorly understood. Peat monoliths were, therefore, exposed to eCO2, warming and eCO2 + warming (combined). The combined treatment produced a synergistic (i.e., significant interaction) rise in DOC concentrations available for export (119% higher than the control, interaction P < 0.05) and enriched this pool with phenolic compounds (284%). We attribute this to increased plant inputs, coupled with impaired microbial degradation induced by competition with the vegetation for nutrients and inhibitory phenolics. Root biomass showed a synergistic increase (407% relative to the control, P < 0.1 only), while exudate inputs increased additively. Phenol oxidase was suppressed synergistically (58%, interaction P < 0.1 only) and β-glucosidase (27%) additively, while microbial nutritional stress increased (51%) additively. Such results suggest intensified carbon exports from peatlands, with potentially widespread ramifications for aquatic processes in the receiving waters.

Introduction Atmospheric CO2 concentrations are continuing to rise as a result of fossil fuel burning and changes in land use (1). Carbon cycle models project that by 2100 levels will be between 540 and 970 ppm (1, 2). Global average surface temperatures have also increased and are predicted to rise between 1.5 °C and 5.9 °C by 2100 depending on region (1). The rate and magnitude of warming is projected to be greatest at mid and high latitudes, where much of the world’s peat reserves are located (1). Northern ecosystems may be especially vulnerable to climate change due to the large current temperature constraints on biological activity (3, 4). Furthermore, plant species diversity is relatively low, meaning climatically mediated changes in species composi* Corresponding author phone: 01248 351151, x2507; fax: 01248 370731; e-mail [email protected]. † School of Biological Sciences, University of Wales. ‡ Centre for Ecology and Hydrology, University of Wales. § Centre for Ecology and Hydrology. 3146

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tion or abundance are likely to have large effects on the ecosystem (5). Sphagnum peatlands, in particular, are important accumulators of carbon, due to their slow decomposition rates (6) relative to production rates, and contain ca. one-third (455 Pg) of the world’s soil organic carbon (7), representing one of the most extensive wetland types in North America and Asia (8). Sphagnum is characteristic of peat bogs and poor fen peat (9). On a global basis, no other taxon of moss is as ecologically dominant (10) and it represents the most important carbon sequestering species (11). Over half of the world’s peat originated from Sphagnum (10-15% of the terrestrial carbon stock), with more carbon held in living and dead Sphagnum than is fixed annually by all terrestrial vegetation (12). The importance of Sphagnum-dominated wetlands as carbon accumulating ecosystems can partly be attributed to Sphagnum’s unusual physiological and biochemical features that impede the degradation of plant matter and sequester carbon, such as the slow turnover of carbon within living tissues and presence of microbial inhibitors (13-17). However, despite the carbon sequestering properties of peatlands, they are major sources of dissolved organic carbon (DOC) and streams draining temperate peatland catchments commonly contain at least 10-45 mg L-1 (18). More DOC is exported from peatlands than any other major biogeographic area in the world, accounting for 20% of the total terrestrial DOC exported to the oceans (19). Both higher temperatures (20) and elevated CO2 (21) have been found to increase DOC concentrations available for export from peatlands and organic-rich soils. The former was attributed to enhanced microbial enzymic mobilization of the peat matrix (via the phenolic compound-cycling enzyme phenol oxidase) (20) and the latter to increased inputs of recently synthesized photosynthate carbon (root exudates) (21). Warming is likely to accompany rising CO2, but the interactive effects of these factors on peatlands is unknown. This paucity of information is surprising given that even a small change in peatland carbon cycling is potentially of global significance, due to the vast amounts of carbon stored. The objective of this investigation was, therefore, to determine what effect the combination of elevated CO2 and warming would have on the quantity of DOC available for export from peatlands. It was hypothesised, that the additive effects of the above mechanisms would produce higher DOC concentrations than those seen under elevated CO2 and under warming alone. The combined effect of CO2 and temperature was, therefore, assessed, using intact soil cores incubated in solardomes for ca. 3 years. A suite of biogeochemical properties were measured, aimed at determining the underlying mechanisms responsible for changes in carbon cycling, and whether these were microbial or plant dominated. The ratio of DOC:dissolved organic nitrogen (DON) was used as an indicator of the source of DOC inputs to the leachate, i.e., new plant contributions versus older peat matrix-derived carbon released by the action of microbial enzymes (22). Poly-β-hydroxyalkanoate concentrations (indicating microbial nutritional stress) were also measured, to determine whether treatments increased competition by the vegetation for inorganic nutrients (23). The focus was on soil extracellular enzyme activities, rather than microbial diversity because, while microbial community composition may shift, different species may carry out the same carbon function. Phenol oxidase was chosen because it is proposed to regulate carbon storage in peatlands and may increase mobilization of the peat matrix under higher 10.1021/es061765v CCC: $37.00

 2007 American Chemical Society Published on Web 03/29/2007

temperatures (20, 24) and β-glucosidase because it is indicative of carbon mineralization in general, being responsible for the cycling of more labile carbon (25). Phosphatase activities were used to determine whether changes in phosphorus availability were induced. In addition to DOC, soluble phenolics concentrations within this pool were measured because of their perceived pivotal role in carbon sequestration in peatlands, derived from their recalcitrance and microbial metabolism/enzyme inhibiting properties (20, 21, 24).

Experimental Site Description. The site chosen for the primary study, a pristine flush wetland in the Upper Wye catchment on Plynlimon (Mid Wales, UK NGR SN 820 866), is typical of many in the uplands of Wales (26). The mire is characterized by Sphagnum and Juncus communities (see Supporting Information) and has a leachate water pH of 3.9-4.8 at a depth of 10 cm. A field survey of the surrounding catchment, utilizing natural environmental gradients, was carried out to investigate the effects of plant species composition on DOC exports. A second field site with a different hydrological regime and nutrient status (the Migneint bog, Conwy, North Wales UK NGR SH816440) was also used to determine whether responses are site specific (see Supporting Information). All data refer to the primary experiment unless stated otherwise. Solardome Design and Performance. A detailed description of the solardome system was given by ref 27, also see the Supporting Information (Figure S1). The solardome systems were set up with the following treatments and two replicate domes per treatment. (1) Ambient CO2 + ambient temperature (control). (2) Elevated (235 ppmv tracked above ambient) CO2 + ambient temperature (eCO2). (3) Ambient CO2 + elevated (3 °C tracked above ambient) temperature (eTemp). (4) Elevated (235 ppmv above ambient) CO2 + elevated (3 °C above ambient) temperature (combined). Peat Collection and Treatment. Twenty five intact peat/ plant monoliths (0.11 m diameter × 0.25 m deep) were collected from each field site (September 1998) and housed in perfusion systems that allow the water table to be controlled (described by refs 28, 29, also see the Supporting Information). Routine Sampling and Chemical Analysis of Peat Leachate Water. Leachate samples were extracted (5 mL from each core) biweekly and then monthly from the top 3 cm of the peat profile and at 20 cm depth, using lateral sampling ports that minimize extraction volume and dead volume. This ensured that excessive disturbance of the core was avoided and that the integrity of the extracted sample (in particular redox potential) was unaffected (28, 29). Following collection, samples were filter sterilized (0.2 µm pore diameter membranes, Whatman, Kent, UK) and refrigerated (60 years) modeling of carbon sequestration suggests that where DON losses are high relative to DIN (as in the current study), carbon is more likely to be lost rather than sequestered (48). However, this work relates to terrestrial ecosystems, and further study is required for peatlands specifically. Amplified plant inputs (biomass and exudation) are likely to contribute increased DOC under the combined treatment, along with the change in the nature of litter produced. However, despite the huge increase in potential carbon substrates for microbial growth and warmer temperatures conducive to microbial proliferation, extracellular phenol oxidase and β-glucosidase activities decreased (58%, interaction P < 0.1 only, Figure 3; 27% additively, Table S4, respectively). This can account for the selective enrichment of phenolic compounds within the DOC pool. The same trend was also true for the eCO2 treatment to a lesser extent (Figure 3, Table S4), in accordance with work done on the tundra ecosystem (49), where suppressed enzyme activities under eCO2 were found. It is feasible that increased CO2 concentrations could inhibit microbial activity directly (50), because CO2 represents an unwanted waste product of metabolism (23) and, therefore, impede degradation of organic matter dissolved in the pore waters. However, it is generally thought that indirect inhibition is more likely, since the concentration of soil CO2 is measured in terms of 104 ppm (51). In the current study, increased carbon-cycling enzyme activities were found under eTemp, but these did not reach significance (Figure 3, Table S4), suggesting that mobilization of the peat matrix (20) makes only a modest contribution to increased DOC trends (21). Taken together, these data suggest that the increased DOC concentrations found here are primarily plant- rather than microbially generated. Suppressed carbon-cycling activities under the combined treatment conflicted with our hypothesis that enzymic generation of DOC from the peat matrix would occur. This may be due in part to factors such as end product inhibition (52) and the time of year (autumn) reducing microbial activity. However, PHA concentrations indicate considerable microbial nutritional stress, with eCO2 + eTemp seemingly inducing additive stress (51%). This is consistent with the suppressed carbon-cycling activities and the stimulated phosphatase activities observed, implying that vigorous plant growth contributes increased organic carbon to the system, while forcing increased microbial enzyme allocation to acquire inorganic nutrients (53, 54) and resulting in unbalanced growth. Indeed, increased competition by the vegetation for inorganic nutrients substantiates the findings of Freeman et al. (23) under eCO2. In conclusion, it is proposed, that the synergistic increase in DOC concentrations found under the combined treatment are due to increased plant inputs coupled with suppressed microbial decomposition. Plant inputs synergistically increased in the form of shoot and root biomass, while exudates and drying (promoting chemical oxidation of the peat matrix) showed additive responses. Microbial degradation of such materials via phenol oxidase was suppressed synergistically 3150

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and via β-glucosidase additively, allowing their accumulation in the leachate waters. Selective enrichment for inhibitory phenolic compounds is likely to further retard microbial metabolism and enzymic decomposition of DOC via hydrolases (e.g., refs 24, 38, 39), preserving even relatively labile material both in the peatland and receiving waters. Field survey results (Table S5, Supporting Information) are consistent with the effects of plant species compositional changes under eCO2 + eTemp, and since a hydrologically different wetland also produced synergistic increases in DOC (197%, P < 0.05) and phenolics (244%, P < 0.05) under eCO2 + eTemp, such responses to are unlikely to be site specific. However, the magnitude of response will depend on nutrient status and water table (21). Similarly, increased DOC concentrations under eCO2 have also been reported for various types of peat and attributed to increased carbon allocation below ground by the vegetation (21, 55). Thus, while our results appear to be consistent with the literature, the interactive effects of CO2 and warming on different peat types requires further study to assess whether synergistic increases in DOC are likely across all northern peatland types. Similarly, other important drivers of DOC operating at local, regional, and global scales also require investigation, such as recovery from acidification and nitrogen deposition, which may further increase DOC levels (56). Warming alone apparently cannot account for the 65% increase in DOC concentrations found in streams draining peatland catchments in the UK (20), but elevated CO2 is said to be capable of inducing an increase of this magnitude (21), though this is highly contentious (56). Our results suggest that any rise in temperatures that accompany elevated atmospheric CO2 could intensify aquatic carbon export synergistically. Indeed, rising trends in the UK now stand at 91% in the last 15 years, with widespread rising DOC in the rivers and lakes of Europe and North America (56). Such an increased organic matter load is likely to have extensive ramifications in freshwaters, and even coastal shelf systems (56), including shifts in pollutant and nutrient transport, pH, energy budgets, and increased light attenuation (e.g., refs 36, 38, 39, 56, 57).

Acknowledgments N.F. gratefully received funding from the Sir William Roberts scholarship (University of Wales, Bangor). C.F. acknowledges a Royal Society Industry Fellowship. N.F. and C.F. also acknowledge funding from the NERC, UK and the Leverhulme Trust, UK.

Supporting Information Available Site descriptions, solardome design, peat core collection and treatment, solardome performance, plant biomass data, peat % water saturation data, enzyme activity data, and natural environmental gradient data. This material is available free of charge via the Internet at http://pubs.acs.org.

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Received for review July 25, 2006. Revised manuscript received February 12, 2007. Accepted February 14, 2007. ES061765V