Effects of vascular plants on methane cycling in wet soils
Wetlands are favourable habitats for methanogenic archaea that form methane during the decomposition of organic material. These methanogens require environments with no oxygen and abundant organic matter, both of which are present in wetland conditions (Segers, 1998). Peatlands dominated by Sphagnum mosses (bogs) are known for the slow decomposition of dead organic matter. The refractory nature of Sphagnum litter is mainly responsible for this slow decomposition, as other plants, including typical bog species, decompose much more rapidly than mosses (Aerts et al., 1999; Woodin et al., 2009). Therefore, if nutrient availability permits the dominance of vascular plants, the potential production of methane is strongly increased by a high production of vascular plant biomass, which results in an increased input of more easily decomposable litter (Whiting & Chanton, 1993; Joabsson & Christensen, 2001). Underground vascular plant tissue can also transport labile carbon compounds into anoxic soil layers (Joabsson & Christensen, 2001; Ström et al., 2003; Chanton et al., 2008). Such increased substrate stocks for methanogenic archaea may be crucial because methane production is frequently substrate limited (reviewed in Whalen, 2005). Moreover, aerenchymatous roots can strongly stimulate the export of methane by creating shortcuts to the atmosphere (van der Nat & Middelburg, 1998; Kutzbach et al., 2004; Whalen, 2005).
The presence of roots, however, may also decrease the release of methane. Oxygen diffuses through the aerenchyma of vascular plants from the atmosphere into the roots and subsequently leaks into the rhizosphere (Armstrong et al., 1991, 2006). Under such oxic rhizosphere conditions, methane production can be reduced by two orders of magnitude (reviewed in Segers, 1998). In addition, when oxygen is present, methane stocks can be decreased by oxidation via methanotrophic bacteria (King, 1994; Sorrell et al., 2002; Raghoebarsing et al., 2005). The passage through a thick aerobic soil–atmosphere interface (i.e. 3–20 cm of aerobic soil) can thus oxidize most of the methane (Roulet et al., 1993; Daulat & Clymo, 1998; Hornibrook et al., 2009). Our study investigated methane release from bog lands that have high root densities, and provides evidence that certain wetland ecosystems do not produce nearly as much methane as do most temperate and tropical wetlands.
The extent to which the rhizosphere can become aerated depends on various conditions: root density, rate of oxygen loss from the roots, soil oxygen consumption and the diffusion coefficient of oxygen in the soil. Under most conditions, the combination of high oxygen consumption (high temperature, suitable substrate and high microbial activity) and limited oxygen release (limited oxygen conduction capacity and low root density) will result in a very thin oxic rhizosphere. Therefore, in wetland soils, a large fraction of the substrate surrounding a root remains anoxic despite root oxygen loss (Armstrong et al., 1991, 1992). Such incomplete oxidation of organic soils promotes the coexistence of roots and methane (Grosse et al., 1996), ultimately resulting in increased emission of methane (Watson et al., 1997; Ding et al., 2005).
Depending on the type of vegetation, the potential to lower methane emission by the creation of oxic soil conditions varies from 16% to 95% (Laanbroek, 2009). Extensive rhizospheric oxidation requires a dense root biomass (Grosse et al., 1996; Smolders et al., 2002), which, in turn, provides extra carbon for methane production. However, many studies ignore such additional methane production fuelled by plant litter and root exudates when estimating the oxidation potential of the rhizosphere. The root–methane interaction model of Watson et al. (1997) required high root biomass to find considerable methane oxidation. Only thorough rhizospheric oxidation created a sufficiently large spatial separation of roots from methane to prevent aerenchyma-mediated diffusion (Grosse et al., 1996). Methane emissions can become temporarily decoupled from vascular plant cover when the water levels are low (Bubier, 1995; Couwenberg et al., 2010). At these dry sites, the water table drops below the bulk root mass, so that methane is oxidized before being released via plants.
In essence, the large majority of studies show that vascular plants increase methane release from wetlands (Whiting & Chanton, 1993; Waddington et al., 1996; Kutzbach et al., 2004; Bortoluzzi et al., 2006). Estimations reveal that approximately one-third of global methane emission derives from wetlands, where minerotrophic wet peatlands and marshes dominated by vascular plant vegetation are the most important sources (Whiting & Chanton, 1993; Saarnio et al., 2009; Koelbener et al., 2010). Bypassing the aerobic soil–atmosphere interface will be the main cause for high, vascular plant-mediated emission rates. Via their aerenchyma, higher plants can conduct 50–95% of the total methane emission (Ding et al., 2005; Whalen, 2005).
Global climate change leading, for instance, to nutrient availability and changes in soil wetness is believed to increase the vascular plant cover in peatlands (Johansson et al., 2006; Breeuwer et al., 2010), which substantially feeds back to methane cycling in wetlands (see the first two paragraphs of the Introduction). However, the importance of particular plant species in methane cycling remains highly variable (Joabsson et al., 1999; Laanbroek, 2009). Part of this variation can be explained by the varying dominance of plant functional types as shown in recent studies (Bouchard et al., 2007; Kao-Kniffin et al., 2010; Koelbener et al., 2010). Plant functional types (reviewed in Ustin & Gamon, 2010) may efficiently combine differences in traits, such as litter production, root density and oxygenation potential (Sorrell et al., 2001; Allen et al., 2002; van Bodegom et al., 2005; Bouchard et al., 2007). The functional type ‘cushion plant’ (cf. Gibson & Kirkpatrick, 1985) has not been studied with respect to methane, despite its importance in forming peatlands in the Southern Hemisphere.
We hypothesized that in, vascular plant-dominated wetlands, methane release may be decreased or even absent if the soil is thoroughly oxidized by extensive rhizosphere oxygen loss. In search of such wetlands, we targeted methane-producing wetlands (e.g. deep bogs) where oxygen consumption is low. The rainy cold parts of Patagonia harbour pristine bogs with very few nutrients (Kleinebecker et al., 2008; Schmidt et al., 2010). Darwin (1839) described bogs in Patagonia with deep rooting plants growing as dense cushion-like vegetation that formed extensive blanket bogs. Cushion plants, such as Astelia ssp. and Donatia ssp., form dense root systems consisting of shallow tap roots and aerenchymatous roots of > 100 cm in length (Darwin, 1839; Grootjans et al., 2010). Our objective was to elucidate whether these roots negatively affected methane emission by comparing densely rooted sites with sites covered only by moss species (Sphagnum ssp.). Interactions of roots with soil methane cycling were studied by correlating the vertical distribution of methane stock, oxygen availability and methane oxidation potential with the root biomass density of cushion plants.