Nutrients and the priming effect

To keep pace with the sea level rise, salt marshes gain elevation i.a. through the balance between OM sequestration and decomposition (Kirwan & Megonigal, 2013).

In chapter 4, we found evidence that coastal eutrophication has a negative impact on C storage, at least in higher salt marsh zones. This indicates a high demand for N in high salt marsh elevations opposed to low marsh elevations where stabilisation was only marginally affected by nutrient additions (Bouma et al., 2001). In the latter, tidal inundation ensures a regular nutrient input through the sea water resulting in a gradient of demand for N similar to the gradient in elevation (Deegan et al., 2012).

Therefore, invertebrates in Pio or Low have to adapt to cope with abiotic constraints from the sea water (introduced in chapter 3), such as the sealing of spiracles to survive inundation performed by Spelobia stercoraria, rather than evolving strategies to outcompete other species for nutrients, such as the formation of maggot balls by Hydrotaea dentipes (Skidmore, 1985; Smith, 1989). These patterns are not only observed within the fauna or microorganisms but also in the floral domain: In chapter 5 we explained a general trend towards a higher density of fine roots with lower plant available phosphorous. Plants invest more in aboveground tissue compared to roots when nutrients are available in sufficient amounts (Darby &

Turner, 2008; Valiela, 2013; Johnson et al., 2016). In this respect it must be mentioned that FRM also depends on grain size distribution of the upper soil within the salt marsh: As soils with larger mean grain sizes are prone to erosion by wave energy, plants must invest more to anchor themselves in sandy sediments (van Eerdt, 1985; Allen, 1989). In conclusion, we can expect a high FRM if nutrients are low and the upper soil has a high content of sand. Additionally, when nutrients are scarce, another factor appears to become more important in accordance with FRM: Chapter 5 showed that FRM is highest in Low, a zone with limited plant available phosphorous and the highest species diversity among all three salt marsh zones. Hence, plant species compete for nutrients which is reflected in a high amount of FRM and belowground space occupation similar to other studies in terrestrial environments (Fransen et al., 2001; Leuschner et al., 2001).

Organic matter balances are not only influenced by the total mass of nutrient input or output. Regarding the PE, the stoichiometry of nutrients is a key factor which

has consequences for carbon gains and losses in soils. Moreover, PEs of terrestrial and aquatic/marine ecosystems are vastly different from each other: In freshwater planktonic ecosystems, priming has been suggested to emerge on pulsed availability of labile carbon (Bianchi, 2011) or due to spatial proximity of auto- and heterotrophic microbial populations (Guenet et al., 2010). However, in these systems, bacterial cells might invest the energy of available labile carbon directly into growth and accumulation of biomass instead of production of extracellular enzymes, which are required to increase the exploitation of ambient recalcitrant carbon (Catalán et al., 2015). In a structurally stable environment such as a soil, the availability of OM is highly constrained (Jobbágy & Jackson, 2001) and labile carbon pulses can occur on a sporadic level. In such an environment, priming might be a successful ecological strategy allowing heterotrophic microbial populations to endure periods of labile carbon shortage (Catalán et al., 2015). In salt marsh ecosystems these PE patterns occur simultaneously and spatially confounded.

Derived from hypothesis of Guenet et al. (2010), possible interactions within a salt marsh ecosystem that lead to PEs are shown in Figure 6.1: Labile organic matter (LOM) is supplied to the soil through tidal inundation in the form of plant detritus and phytoplankton exudates (McKinley & Vestal, 1992). LOM decomposer synthesis specific enzymes capable of degrading LOM and thus providing the LOM decomposer with energy. Moreover, the flush of easily degradable substances enables LOM decomposer to synthesise LOM enzymes. As a secondary effect, these enzymes degrade recalcitrant organic matter (ROM) in the soil into catabolites, thereby supplying another microbial community with enough energy and nutrients to synthesise ROM-specific enzymes degrading available ROM substrates in the soil.

This co-metabolism leading to PEs was shown experimentally and reviewed in other studies (Kuzyakov et al., 2000; Hamer & Marschner, 2005; Blagodatskaya et al., 2011). Another possible pathway is the direct utilisation of degraded LOM by ROM decomposers for their catabolism. They invest the energy derived from LOM products to synthesise ROM enzymes which provides the limiting nutrients and structural C for both decomposer communities. This mutualism was described in general context and with special emphasis on salt marsh ecosystems in various studies (Bertness & Leonard, 1997; Kuzyakov, 2002; Fontaine & Barot, 2005). While

simultaneously, distribution of LOM and ROM in the salt marsh soil is likely to be spatially heterogenous: LOM is mostly replenished by inundation and tides in Pio and Low, whereas ROM is stored in considerable amounts in the soil of higher elevations (Low and Upp). The mechanisms above state the situation of a positive PE. However, it has to be mentioned that there is also the possibility of a negative PE, which happens when the most active part of microorganisms switch from decomposition of ROM to added LOM, a term called preferential substrate utilisation PSU (Cheng, 1999; Kuzyakov et al., 2000; Blagodatskaya et al., 2007; Kuzyakov & Bol, 2006). As an example, no or negative PE was found in a lake water experiment comparable to my results in chapter 2 under constant flooded conditions (Catalán et al., 2015).

As seen in chapter 4, the stabilisation of OM seems to be negatively affected by an increased nutrient level of the water: A regular input of LOM and nutrients from sea water through tidal inundation could supply initial energy for microorganisms to decompose ROM stored inside the salt marsh sediment. An indication for such a PE can be observed in the clearly reduced OM stabilisation within the upper salt marsh

Figure 6.1 Hypothesis of Priming Effects in the salt marsh ecosystem involving two mechanisms of co-metabolism and mutualism and two different forms of organic matter: Labile (LOM) and recalcitrant (ROM) (modified after Guenet et al., 2010).

Pioneer Zone Lower Saltmarsh Zone Upper Saltmarsh Zone ROM Decomposer

under nutrient enriched conditions: N-limited microbial communities within Upp use labile, N-rich OM to mineralise recalcitrant, plant-based OM (see chapter 4). The lack of this effect in Low elevations indicates that these zones are not N-limited.

Nevertheless, I showed in chapter 2 that PE in Low is generally higher than in Pio. In addition to the already mentioned reasons, this is a direct consequence from a high nutrient level of the soil in this zone leading to a high PE-potential if LOM or/and a sufficient amount of moisture is supplied (Bianchi, 2011).