Saltwater intrusion and soil carbon loss: Testing effects of salinity and phosphorus loading on microbial functions in experimental freshwater wetlands

Highlights

• We tested effects of salinity and phosphorus on freshwater wetland soils.

• Salinity decreased enzyme activities, particularly carbon acquiring enzymes.

• Salinity decreased soil and increased porewater carbon concentrations.

• Phosphorus increased root litter breakdown, and salinity had no effect.

• Carbon losses from saltwater intrusion may not be altered by added nutrients.

Abstract

Wetlands can store significant amounts of carbon (C), but climate and land-use change increasingly threaten wetland C storage potential. Carbon stored in soils of freshwater coastal wetlands is vulnerable to rapid saltwater intrusion associated with sea-level rise and reduced freshwater flows. In the Florida Everglades, unprecedented saltwater intrusion is simultaneously exposing wetlands soils to elevated salinity and phosphorus (P), in areas where C-rich peat soils are collapsing. To determine how elevated salinity and P interact to influence microbial contributions to C loss, we continuously added P (~0.5 mg P d⁻¹) and salinity (~6.9 g salt d⁻¹) to freshwater Cladium jamaicense (sawgrass) peat monoliths for two years. We measured changes in porewater chemistry, microbial extracellular enzyme activities, respiration rates, microbial biomass, root litter breakdown rates (k), and soil elemental composition after short (57 d), intermediate- (392 d), and long-term (741 d) exposure. After 741 days, both β-1,4-glucosidase activity (P < 0.01) and β-1,4-cellobiosidase activity (P < 0.01) were reduced with added salinity in soils at 7.5–15 cm depth. Soil microbial biomass C decreased by 3.6× at 7.5–15 cm (P < 0.01) but not 0–7.5 cm depth (P > 0.05) with added salinity and was unaffected by added P. Soil respiration rates decreased after 372 d exposure to salinity (P = 0.05) and did not change with P exposure. Root litter k increased by 1.5× with added P and was unaffected by salinity exposure (P > 0.01). Soil %C decreased by approximately 1.3× after 741 days of salinity exposure compared to freshwater controls (P < 0.01). Elevated salinity and P accelerated wetland soil C loss primarily through leaching of DOC and increased root litter k. Our results indicate that freshwater wetland soils are sensitive to short- and long-term exposure to saltwater intrusion. Despite suppression of some soil microbial processes with added salinity, salt and P exposure appear to drive net C losses from coastal wetland soils.

Introduction

Wetlands are critical carbon (C) reservoirs and store disproportionate amounts of C relative to the total land area, with some capable of storing up to 50 times more C than tropical forests (Mcleod et al., 2011). External stressors associated with climate change have the potential to degrade wetlands and drastically alter ecosystem function (Green et al., 2017). In particular, coastal freshwater wetlands at the interface of terrestrial and marine environments and are increasingly exposed to rapid saltwater intrusion resulting from reduced freshwater deliveries and increased sea levels (White and Kaplan, 2017). Saltwater intrusion is the intrusion of marine-origin water comprised of many salt-forming ions (i.e. Cl⁻, NO₃⁻, SO₄²⁻, PO₄³⁻). Increased rates of saltwater intrusion pose a threat to wetland C storage, a globally important ecosystem service driven by historical and current environmental conditions that promoted carbon dioxide (CO₂) uptake and its sequestration as organic C within the soil and plant biomass. Further, exposure of coastal freshwater marshes to unprecedented rates of saltwater intrusion affects the biogeochemical cycles that support C storage through the introduction of marine ions which can potentially cause these systems to transition from net C sinks to net C sources (Weston et al., 2011).

Altered biogeochemical conditions with elevated salinity affect soil microbial processing and consequently the rate of C cycling in wetlands (Weston et al., 2006). Anaerobic conditions in wetland ecosystems slow biogeochemical processing rates and organic matter decomposition which promotes C storage (Helton et al., 2015). Increases in salinity can change redox potential (Rietz and Haynes, 2003; Van Ryckegem and Verbeken, 2005), increase electron acceptor availability (Helton et al., 2015), increase osmotic stress, and change organic substrate quantity and quality (Neubauer, 2013). Consequentially, saltwater intrusion can potentially increase microbial respiration, stimulating organic C loss from wetland soils. The effects of salinity on microbe-mediated biogeochemical processes can occur within days to weeks (Craft, 2007; Weston et al., 2006; Weston et al., 2011; Neubauer, 2013; Chambers et al., 2014). Salinity increases (3–15 ppt) can affect the physiochemical characteristics of freshwater wetland soils (Berner and Berner, 2012; Flower et al., 2017), and the species composition of microbial communities is linked to environmental gradients like salinity and nutrients (Ikenaga et al., 2011). However, the interactive effects of abrupt elevations in salinity and limiting nutrient availability on soil microbial functions, like extracellular enzyme activities are largely uncertain (but see Jackson and Vallaire, 2009). Further, how short- and long-term exposure to coupled additions of salinity and nutrients may differentially impact soil microbial processes that contribute to C gains or losses requires explicit testing.

Saltwater intrusion can also change biogeochemical cycling by altering concentrations of dissolved nutrients within soil porewater. For example, karstic coastal wetlands found in the Florida Everglades and throughout the Caribbean are extremely limited by phosphorus (P) supplied from marine water inputs (Fourqurean et al., 1993; Boyer et al., 1999; Noe et al., 2001; Childers et al., 2006). When saltwater infiltrates the porous limestone bedrock of the Everglades, P adsorbed to calcium carbonate is released (Price et al., 2006; Price et al., 2010; Flower et al., 2017). In freshwater wetlands of the Everglades, saltwater intrusion represents both a stress caused by elevated salinity and a resource subsidy in the form of P release, but the combined effects of elevated salinity and P on soil microbial functioning are unclear. Recent observations of peat collapse, rapid soil subsidence, have been observed within the Everglades (Wanless and Vlaswinkel, 2005; Day et al., 2011). Rapid and persistent marine intrusion into previously freshwater wetlands is hypothesized to increase soil susceptibility to collapse, by altering porewater chemistry, microbial processing rates, and plant productivity.

Soil microbes contribute to rates of C and nutrient cycling within soils (Penton and Newman, 2007). Extracellular enzymes are important drivers of microbe-mediated biogeochemical cycling, and enzyme-catalyzed biochemical reactions are considered the rate-limiting step in organic matter degradation (Chróst and Rai, 1993; Dick, 1994). When bioavailable C or nutrients limit microbes, they release extracellular enzymes into soils to meet metabolic demands. Therefore, measurements of extracellular enzymes can provide information on the quality of organic soils, nutrient cycling, and microbial elemental demand (Sinsabaugh et al., 2002). Enzyme activities are often suppressed when exposed to salinity (Frankenberger and Bingham, 1982; Jackson and Vallaire, 2009), as microbes divert resources to the production of osmolytes and consequentially reduce production of extracellular enzymes (Kempf and Bremer, 1998). However, in natural salinity gradients positive relationships between salinity and enzyme activity have been reported (Morrissey et al., 2014). In contrast, P enrichment in P-limited ecosystems generally reduces phosphatase activities (Spiers and McGill, 1979; Wright and Reddy, 2001; Morrison et al., 2016) and increases other enzymes activities (Rejmánková and Sirova, 2007). The effects of simultaneous exposure to osmotic stress and increased availability of limiting nutrients on microbial function and the evolution of microbial responses over time are unknown despite the importance of soil microbes in determining ecosystem C storage potential. In the Everglades and other coastal freshwater wetlands with organic-rich soils, changes in extracellular enzyme activities may lead to long term-effects on soil collapse and accumulation of C-storing peat soils (Penton and Newman, 2007).

Here, we used P-limited, freshwater peat soils from the Florida Everglades to test how microbial extracellular enzyme activity, soil elemental content, root litter breakdown rates (k), and porewater chemistry responded to continuous exposure to elevated salinity and P and measured net effects on soil C (gains or losses). We hypothesized that (1) elevated salinity would cause increases in C and nutrients in the porewater and become available to soil microbes for metabolism (Ardón et al., 2013); (2) elevated salinity would cause microbial communities to invest more resources to maintaining cell turgor and consequentially have fewer resources devoted to the production of P- and sulfur (S)-acquiring enzymes (Aristi et al., 2016); (3) salinity induced P release would cause microbial communities to increase demand for energy from C and consequentially soil microbes would devote more resources to the production of C-acquiring enzymes (Table 1) (Benfield, 2006); (4) the greatest effects of salinity would occur during early exposure as the microbial community transitioned from a freshwater community to a salt-adapted community (Benfield, 2006); (5) P addition would increase potential activity for C- and sulfur (S)-acquiring enzymes and decrease in potential activity for P-acquiring enzymes because the release from P-limitation would increase C and other nutrient demands while lowering P demands (Table 1) (Berner and Berner, 2012); (6) salinity and P would interact to decrease P and S-acquiring enzymes and result in similar activity levels of C-acquiring enzymes relative to the freshwater control (Boyer et al., 1999); (7) soil microbial respiration rates, biomass C, and root litter k would be highest in the P treatment salinity (Caravaca et al., 2005). Understanding how microbial functions changes with salinity exposure and nutrient enrichment is increasingly important as coastal freshwater wetlands become more exposed to marine water supplies.