Eco-DAS VIII Symposium Proceedings · In salt marsh interiors, where nitrate reduction rates are...

67

1 Introduction

1A Coastal wetlands in a changing worldmdashCoastal wetlandsreside at a critical interface between land and sea where theyretain and transform nutrients perform water purificationfunctions and support productivity that sustains fisheriesThese ecosystem services and several others are important forgrowing human populations that are concentrated alongcoastlines (Craft et al 2009) Given the small amount of landthey cover these wetlands are disproportionately valuable interms of services they perform (Costanza et al 1997) as wellas disproportionately vulnerable to anthropogenic alterationsincluding the effects of sea level rise (SLR) and increased nitro-gen (N) loading

Human-induced SLR resulting from global warming threat-ens the long-term persistence of coastal wetlands Urban devel-opment and hydrological alterations of coastlines worldwidehave limited the ability of wetland ecosystems to retreat from

A complex-systems approach to predicting effects of sea levelrise and nitrogen loading on nitrogen cycling in coastal wetlandecosystemsLaurel Larsen1 Serena Moseman2 Alyson E Santoro3 Kristine Hopfensperger4 and Amy Burgin5

1National Research Program US Geological Survey Reston VA USA2Department of Biology Boston College Boston MA USA3Department of Marine Chemistry amp Geochemistry Woods Hole Oceanographic Institution Woods Hole MA USA4Department of Biological Sciences Northern Kentucky University Highland Heights KY USA5Department of Earth amp Environmental Sciences Wright State University Dayton OH USA

AbstractTo effectively manage coastal ecosystems we need an improved understanding of how tidal marsh ecosys-

tem services will respond to sea-level rise and increased nitrogen (N) loading to coastal areas Here we reviewexisting literature to better understand how these interacting perturbations will likely impact N removal by tidalmarshes We propose that the key factors controlling long-term changes in N removal are plant-communitychanges soil accretion rates surface-subsurface flow paths marsh geomorphology microbial communities andsubstrates for microbial reactions Feedbacks affecting relative elevations and sediment accretion rates will serveas dominant controls on future N removal throughout the marsh Given marsh persistence we hypothesize thatthe processes dominating N removal will vary laterally across the marsh and longitudinally along the estuarinegradient In salt marsh interiors where nitrate reduction rates are often limited by delivery of nitrate to bacte-rial communities reductions in groundwater discharge due to sea level rise may trigger a net reduction in Nremoval In freshwater marshes we expect a decrease in N removal efficiency due to increased sulfide concen-trations Sulfide encroachment will increase the relative importance of dissimilatory nitrate reduction to ammo-nium and lead to greater bacterial nitrogen immobilization ultimately resulting in an ecosystem that retainsmore N and is less effective at permanent N removal from the watershed In contrast we predict that sea-levelndashdriven expansion of the tidal creek network and the degree of surface-subsurface exchange flux throughtidal creek banks will result in greater N-removal efficiency from these locations

Corresponding author E-mail lglarsenusgsgov

ACKNOWLEDGMENTSThis synthesis would not have been possible without the Ecological

Dissertations in the Aquatic Sciences (Eco-DAS) program under the lead-ership of Paul Kemp Eco-DAS funding is provided by the NationalScience Foundation with contributions from the Office of NavalResearch (ONR) National Oceanic and Atmospheric Administration(NOAA) and National Aeronautics and Space Administration (NASA)Eco-DAS is sponsored by the Center for Microbial OceanographyResearch and Education (C-MORE) the University of Hawaii School ofOcean and Earth Science and Technology (SOEST) and the Departmentof Oceanography and the American Society of Limnology andOceanography (ASLO) The authors additionally thank the USGeological Survey (USGS) National Research Program the USGSMendenhall Fellowship Program (SM) and a Woods HoleOceanographic Institution Postdoctoral Scholar Fellowship (AES) forfunding support Three anonymous referees and Tamara Harms provid-ed helpful suggestions that have greatly improved this paperPublication was supported by NSF award OCE0812838 to PF KempISBN 978-0-9845591-1-4 DOI 104319ecodas2010978-0-9845591-1-467

Eco-DAS VIII Chapter 5 2010 67-92copy 2010 by the American Society of Limnology and Oceanography Inc

Eco-DAS VIIISymposium Proceedings

the advancing sea (Fitzgerald et al 2008) Furthermore theseecosystems are currently subjected to more immediate alter-ations such as increased N loading due to agriculture or urban-ization Water quality issues due to N loading affect both thestructural and functional value to humans of coastal wetlandecosystems Thus our objective is to lay a foundation for betterunderstanding of the interactions of multiple anthropogenicdrivers (SLR and N loading) on wetland ecosystem functions(eg N cycling) We argue that to understand the complexnonlinear effects of global changes such as SLR and N loadingscientists need to take a multifaceted approach that considershydrologic microbial and plant community interactions

Climate change most directly impacts tidal marshesthrough SLR Human activities have accelerated SLR throughan increase in the thermal expansion of the oceans fromhigher global air temperatures (Wigley 2005) Although ther-mal expansion is the leading cause of SLR increased meltingof continental ice sheets has also contributed (Shepherd andWingham 2007) Based on International Panel on ClimateChange (IPCC) temperature projections (IPCC 2007) currentmodels project a 75- to 190-cm range in SLR for the periodfrom 1990 to 2100 (Vermeer and Rahmstorf 2009) One of themost publicly visible implications is the predicted submer-gence of coastal areas eg the Mississippi Delta (Blum andRoberts 2009) Although the degree of coastal inundation dueto SLR will depend on many factors it is clear that SLR hasmany potential negative effects including (1) increasing ero-sion (2) enhancing storm surges (3) changing surface andgroundwater quality and (4) losing ecosystem services associ-ated with these vulnerable wetlands

N loading is changing along with sea level Human activi-ties have substantially and directly altered the N cycle byeffectively doubling the amount of reactive N in the environ-ment (Vitousek et al 1997 Galloway et al 2008) The impactsof N loading are particularly problematic in coastal zoneswhere nitrate (NO3

ndash) has been found to stimulate harmfulalgal blooms formation of anoxic zones and a loss of bioticlife Increasing N availability stimulates biomass productionsubsequent decomposition by oxygen-consuming microbes inturn creates low O2 zones called ldquodead zonesrdquo More than 400dead zones have recently been documented along coastsworldwide particularly in areas of high human populationdensity (Diaz and Rosenberg 2008) Wetland microbial andplant communities actively use and transform NO3

ndash poten-tially mitigating the effects of N loading to downstreamecosystems Despite increased loading via anthropogenicsources N remains the limiting nutrient in many coastal wet-lands and thus N loading impacts the productivity and com-position of wetland plant communities as they face SLRs

Given the importance of tidal marshes for coastal waterquality and coastal ecology it is imperative that the dualthreat of SLR and N loading on marsh ecosystem services berigorously evaluated so that management strategies can beadjusted to minimize adverse impacts We argue that these

potential impacts can be fully understood only through aholistic complex-systems approach that accounts for the feed-backs and interactions that occur across multiple levels oforganization in tidal marshes (eg microbes plants hydrol-ogy) As we will show these feedbacks will either exacerbate(eg positive feedbacks) or ameliorate (eg negative feed-backs) the ultimate impact of SLR on N cycling A complex-systems approach equips us to address several challengingrealities (1) that these perturbations operate on different tem-poral and spatial scales with SLR occurring more slowly andover longer time scales in many cases than N loading and (2)that N cycling is mediated across multiple levels of organiza-tion by combinations of microbial plant and landscapeprocesses Although we focus on SLR and N loading our com-plex-systems approach is relevant to numerous simultaneouschanges facing wetlands including altered hydrology (Port-noy 1999) and sedimentation increased CO2 and shifts inspecies composition due to invasive species (Levin et al 2006)

In this synthesis we first review the literature on biotic andabiotic controls on N cycling in tidal marshes and discuss theproximal effects of SLR and N loading on each of these con-trols Then we present a new conceptual model of how SLR islikely to affect interactions and feedbacks between drivers of Ncycling and the marshrsquos overall capacity to remove reactive Nfrom efflux to coastal systems Finally in summarizing howinteractions across ecosystem components are important forpredicting responses of fresh and marine wetlands to SLR andN loading we will offer future directions for research that canbetter embrace the complexity and multiple-scale dynamics ofthese valuable but vulnerable ecosystems

1B Overview of coastal marsh landscapes Hydrology geomor-phology and biologymdashTidal marshes are found in coastal loca-tions throughout the world where different combinations oftemperature underlying geology geomorphology of thecoastline and large-scale distribution of particular plantspecies present challenges for generalization However it iswidely recognized that these diverse marshes each feature dis-crete functional units that are dominated by a distinct set ofprocesses that are globally consistent (Fig 1) We do notattempt to generalize to the species level in this article butinstead focus on N cycling processes occurring within thesefunctional units further described below

Tidal marshes occupy a gradient of elevations along the estu-arine wedge which is also characterized by a gradient in localwater depth salinity and other seawater constituents such assulfate (SO4

2ndash) Tidal salt marshes occupy lowest elevations alongthat gradient and are colonized by a low-diversity but highlyproductive assemblage of salt-tolerant macrophytes such asSpartina alterniflora Higher-elevation salt marshes are less pro-ductive and are often more diverse but may be dominated bySpartina patens or Distichlis spicata In general as elevationsincrease landward and salinities decrease macrophyte diversitytends to increase while productivity declines (Tiner and Burke1995 Donnelly and Bertness 2001 Fitzgerald et al 2006 Fitzger-

Larsen et al Sea level rise and nitrogen cycling

68

ald et al 2008) Local water depths are typically regarded as a pri-mary control on the zonation and succession of tidal marshplants (Odum 1988 Silvestri et al 2004 DrsquoAlpaos et al 2006)although salinity plays a dominant role in limiting the colo-nization and growth of freshwater species (Pennings et al 2005)Microbial community compositions also vary systematicallyalong the salinity gradient as described in section 2B Increasedsalinities generally result in an overall reduction in the diversityof N-cycling communities (Santoro 2010) although the mecha-nisms behind this pattern are poorly understood

Seaward-to-landward declines in the amplitude of tidalfluctuations in surface-water depths constitute the dominanthydrologic change for tidal marshes along the estuarine gradi-ent Many marshes experience asymmetry in tidally inducedhydrologic fluctuations but these features tend to be site spe-cific (French 2006) The sloping of water tables from uplandsto the coastal zone causes many marshes to be regions ofgroundwater discharge (Harvey and Odum 1990 Tobias et al2001a Tobias et al 2001c) This groundwater discharge occursalong the estuarine gradient and also tends to be site specificgoverned by the regional distribution of hydraulic head

Processes governing N cycling in tidal marshes also vary inthe direction parallel to the coast A network of tidal creekssubdivides the marsh along this direction and processes dom-inating N cycling in tidal creeks differ from those along the

creek bank and vicinity of creek banks which differ fromthose in the marsh interior Although creek channels areunvegetated some of the most productive vegetation in tidalmarshes colonizes the creek banks which may sometimesdevelop small levees Less productive vegetation colonizes themarsh interior The higher productivity of vegetation alongcreek banks is linked to the hydrology specific to this region(Wiegert et al 1983) The interface between tidal marshes andtidal channels is a zone of strong gradients in hydraulic headwhere bi-directional exchange between groundwater and sur-face water occurs (Harvey et al 1987 Wilson and Gardner2006) During the flooding portion of the tidal cycle waterfrom the tidal creeks moves over the banks toward the marshinterior This water infiltrates the marsh surface and then dur-ing ebb tide drains from the creek banks into the creek as seep-age from porewater (Gardner and Wilson 2006 Wilson andGardner 2006) Consequently tidal creek banks are among themost aerated best flushed portions of the marsh Bidirectionalexchange of surface water porewater and associated solutesalso occurs to some extent in the marsh interior where tran-spiration by macrophytes removes water from the subsurfaceinducing infiltration of surface water (Moore et al 1997)

1C Overview of N cycling in tidal marshesmdashN cycling incoastal wetlands reflects collective activities of diverse micro-bial communities and the vascular plants with which they


69

Fig 1 Schematic diagram of portions of a tidal marsh that are likely to respond differently to SLR and N loading due to the different feedback processesthat are dominant in these locations Blue arrows show major hydrologic pathways associated with fluxes and transformations of N

interact N sources to wetlands include inputs from the atmos-phere surface water runoff groundwater and tides In bothmarine and fresh tidal wetlands bacteria convert N2 gas tobiologically available N (NH3) through N fixation in plant rhi-zospheres (roots and surrounding sediments) plant shootsand sediment surfaces Plant rhizospheres are also hotspots formicrobial activities involved in nitrification the oxidation ofammonia to nitrite (NO2

ndash) and nitrate (NO3ndash) (Bodelier et al

1996 reviewed in Herbert 1999) as this process requires oxy-gen that is introduced by plant roots in otherwise mostlyanaerobic sediments The microniches formed by such oxygengradients around plant roots (Duarte et al 2005 Lovell 2005)or macrofaunal burrows (Kristensen and Kostka 2005)enhance microbial activities and N cycling rates This is due tointimate coupling that often occurs in coastal ecosystemsbetween aerobic nitrification and anaerobic denitrification(Jenkins and Kemp 1984 Herbert 1999) the latter of whichconverts biologically available forms of N (NO3

ndash) to the bio-logically unavailable gaseous N2 or N2O In respiratory denitri-fication NO3

ndash is used by microbes in the terminal oxidation oforganic matter under anaerobic conditions most of the NO3

ndash

is transformed to N2 although incomplete reduction canresult in the accumulation of intermediates including NO2

ndash

and N2O (a potent greenhouse gas) Denitrification is notalways coupled to nitrification particularly in environmentswith high nitrate availability (Smith et al 2009) Favorableconditions for respiratory denitrification include anoxia andhigh NO3

ndash and labile organic carbon concentrations (Robert-son and Groffman 2007) Alternatively NO3

ndash can be trans-formed to ammonium (NH4

+) via microbes in a process calleddissimilatory nitrate reduction to ammonium (DNRA)

Although denitrification has been intensively examinedrelatively few studies have investigated the ecological controlson other processes that may be important for overall NO3

ndash

removal in wetlands (Megonigal et al 2004 Burgin andHamilton 2007) In contrast to denitrification DNRA is a rel-atively understudied Two forms of DNRA are known to occurfermentative DNRA thought to occur under conditions ofhigh labile organic carbon (OC) availability (Tiedje 1988) andsulfur-driven DNRA (Brunet and Garcia-Gil 1996 Otte et al1999) thought to occur where sulfur oxidizing bacteria haveaccess to NO3

ndash Fermentative DNRA couples electron flow fromorganic matter via fermentation reactions to the reduction ofNO3

ndash (Tiedje 1988 Megonigal et al 2004) Sulfur-driven DNRAcouples the oxidation of elemental S and H2S to the reductionof NO3

ndash to NH4+ While there are a number of studies docu-

menting DNRA in wetlands (Tobias et al 2001b Matheson etal 2002 Revsbech et al 2005 Scott et al 2008) very fewinvestigators have discerned which form of DNRA occurs andthus we know little about the controls on the process at theecosystem scale

Anaerobic ammonium oxidation (anammox) is anotherunderstudied N-removal pathway carried out by autotrophicmicroorganisms which oxidize NH4

+ using NO2ndash as an elec-

tron acceptor Anammox organisms grow very slowly (Jetten2001) and are thought to be out-competed by denitrifyingmicroorganisms when there is ample organic carbon (Dals-gaard et al 2005) Anammox is often reported as a percentageof the N2 production with the balance often assumed to bedue to denitrification An alternative is to report each Ncycling process as a fraction of the overall NO3

ndashNO2ndash reduc-

tion when reported in this mass-balance way N2 productionfrequently does not account for all of the NO3

ndash removal(Seitzinger et al 2006 Mulholland et al 2008) Thus giventhat the fraction of N2 production attributable to anammox isoften 1 to 20 anammox is not currently thought to repre-sent a significant N-removal pathway in coastal wetlands (Ris-gaard-Petersen et al 2004 Trimmer et al 2006 Rich et al2008 Dong et al 2009 Koop-Jakobsen and Giblin 2009)However it should be noted that anammox is not an exten-sively measured process making it difficult to speculate on itsimportance or integrate it into any synthetic overview as isour goal here When denitrification DNRA and anammox aremeasured simultaneously (rare) anammox is consistently theleast significant flux (Dong et al 2009 Gardner and McCarthy2009 Koop-Jakobsen and Giblin 2009)

As water rich in NO3ndash passes through or over wetland sedi-

ments the NO3ndash concentration typically decreases To date N

removal is thought to be due to either assimilation into micro-bial algal or plant biomass or to conversion to N2 via deni-trification However recent research has underscored the com-plexity of microbially driven N biogeochemistry especiallywith regard to factors that control the relative importance ofthese multiple pathways (Brandes et al 2007 Burgin 2007) Asuite of these controlling factors may vary with SLR includingredox potential (related to the degree of inundation) salinityavailability of free dissolved sulfide (hereafter referred to asH2S) NO3

ndash and organic carbon (OC) which are all potentialcontrols on many N-cycling processes (Tiedje et al 1982Tiedje 1988 Joye and Hollibaugh 1995 Brunet and Garcia-Gil1996) In section 2B we discuss several processes in the N cyclelikely to be affected by these changes as well as how the asso-ciated microbial communities are likely to change

2 SLR and nitrogen loading on wetlands Direct impactsEffects of SLR can be parsed into effects resulting from

higher water levels (ie increased inundation decreased oxy-gen transfer to sediments) and those resulting from exposureof marsh ecosystems to higher salinities and higher concen-trations of solutes in seawater such as SO4

2ndash In this section weexamine the direct impacts of N loading and each of thesestressors on the physical environment plant communitiesand microbial ecology

2A Effects on the physical environmentmdashEffects on waterlevelinundation frequency SLR impacts both groundwaterand surface-water hydrology by changing the distribution ofwater levels and hydraulic head In surface water the immedi-ate effect of SLR is an increase in water level over tidal


70

marshes To first order the overall aerial extent of tidalmarshes is expected to decline from this increased inundationwith many salt marshes converting to open water areas (Craft2007) and brackish marshes replacing many tidal freshwatermarshes (Craft et al 2009) However because of feedbackbetween water level and sediment accretion (see section 3A)it is inappropriate to estimate the extent of SLR-driven marshloss simply by comparing current topography and SLR predic-tions (Kirwan and Guntenspergen 2009) As a result of thisfeedback some marshes may not experience long-termchanges in water depth (French 2006) Still although manymarshes exhibit vertical accretion rates that equal SLR ratesthey remain prone to loss of coverage through lateral expan-sion of the tidal channel network (Williams and Hamilton1995 Hartig et al 2002 Van der Wal and Pye 2004) Modelingresults (Kirwan et al 2008) suggest that this expansion can bein part due to localized and temporary disturbance of vegeta-tion eg by crab burrowing (Hughes et al 2009) at the creekheads Exposed unvegetated sediment may be submersedbelow the threshold for vegetation colonization under accel-erated SLR converting these disturbed patches permanently toopen water

Effects on surface watergroundwater exchange In ground-water the increase in sea level will often result in a decrease incoastal hydraulic head gradients which can cause a reductionin the volume of groundwater discharge to tidal marshes(Tobias et al 2001a) This effect can be exacerbated by anincreased fraction of upland runoff at the expense of infiltra-tion due to higher water tables in the near-coastal zone thatalso result from SLR (Nuttle and Portnoy 1992) Uplandgroundwater is typically high in NO3

ndash from anthropogenicsources Under climate-change scenarios the N load thatwould be delivered to tidal marshes as groundwater dischargemay instead be delivered to the subtidal zone (Tobias et al2001a) As a result of diminished freshwater flushing bygroundwater discharge marsh interiors could experience asalinity buildup (Tobias et al 2001a) Enhanced evapotranspi-ration resulting from the higher temperatures expected toaccompany global change may partially counteract this effectby enhancing bidirectional exchange between tidal surfacewater and marsh porewater (see Moore et al 1997)

The level and duration of inundation also exerts a strongcontrol on flow paths and groundwater residence times in thevicinity of tidal creeks Flow paths and residence times arelonger with greater inundation and the total flushing of waterthrough creek banks is larger (Wilson and Gardner 2006)Because the total creekmarsh interface length is expected toincrease under SLR (Kirwan and Murray 2007 Kirwan et al2008) the magnitude of surface-subsurface exchange throughcreek banks will likely increase both on a per-unit-area basisand on a total basis This enhanced tidal flushing will locallydeliver additional solutes and nutrients to shallow porewater(Harvey et al 1987 Wilson and Gardner 2006)

Effects on mean surface-water velocities and turbulence In

open-water environments changes in water level are directlyand positively correlated to changes in flow velocities turbu-lence intensities and bed shear stress (Middleton and Wilcock1994) Sediment entrainment is positively related to the excessbed shear stress (ie the stress above an entrainment thresh-old) (Knighton 1998) so it follows that increased water levelswill be associated with enhanced sediment erosion atmarshopen water interfaces (eg Boorman et al 2001) Inaddition the inundation of low marshes or breaching of bar-rier islands by SLR results in a longer fetch for waves andgreater erosion further inland (Fitzgerald et al 2008)

In the marsh interior water depth has less of an effect onmean velocities and turbulence intensity When emergentvegetation is present the influence of the bed on flow veloc-ity diminishes within several centimeters of the soil-waterinterface (Nepf 1999) and flow is instead dominated by vege-tative drag In emergent vegetation vegetative drag increasesproportional to water levels (Harvey et al 2009 Larsen et al2009b) so SLR would be expected to have minimal effect onvelocity Only very rarely are bed shear stresses in dense emer-gent marsh sufficient to suspend sediment (Stevenson et al1985 Christiansen et al 2000 Larsen and Harvey 2010) How-ever in low-density vegetation where stems do not limit eddydevelopment turbulent wakes form in the lee of stems (Nepf1999) Thus in sparsely vegetated marsh environments (eghypersaline SarcocorniaSuaeda marsh) found in the lowestfluvially dominated portions of the estuarine gradient(Snedaker 1995 Bertness and Ewanchuk 2002) SLR mayenhance turbulence and erosion

In tidal channels enhanced erosion will cause a similarenhancement in sediment deposition at the vicinity of thechannelmarsh interface Higher turbulence and higher bedshear stresses will also result in greater entrainment of rela-tively coarse dense inorganic sediment that will settle rapidlyrelative to fine-grained and organic particles (Larsen et al2009a) and deposit over a wider area around tidal channelsand the marsh front (Christiansen et al 2000) This mineralsediment augments local soil elevations and provides a sourceof iron and manganese to marsh communities enhancing theprecipitation of sulfide metals thereby decreasing dissolvedH2S and the resulting stress on macrophytes (King et al 1982)In addition nutrients sorbed to fine mineral sediment (egphosphorus) may provide limiting substances to primary pro-ducers and decomposers (Slocum et al 2005)

Effects of increased salinities Increased salinities that resultfrom SLR enhance flocculation of both inorganic and organicmaterial (Winterwerp and van Kesteren 2004) Flocculated sed-iments have been described as ldquosuspended biofilmsrdquo that canprovide a source of labile carbon and nutrients and serve as asubstrate for a variety of microbial reactions (Liss et al 1996)Flocculation is further enhanced by intermediate levels of tur-bulence which promote the collision and aggregation of parti-cles without causing particle shearing (Winterwerp and vanKesteren 2004 Larsen et al 2009c) Although enhanced levels


71

of turbulence near the marsh front may induce the breakup offlocs the net effect of SLR will likely be an enhancement of thedegree of flocculation due to the expansion of the relativelylow-turbulence tidal channel network By increasing settlingvelocities and particle mass flocculation would decrease thedistance within the marsh over which allocthonous fine parti-cles and associated constituents are distributed

2B Effects on microbial biogeochemistrymdashEffects of increasedSO4

2ndash Increases in SO42ndash concentrations in coastal wetlands

due to SLR may shift tidal freshwater wetlands from being netmethanogenic to SO4

2ndash reducing ecosystems SO42ndash reduction

produces reduced sulfur compounds including H2S whichhas significant effects on all processes in the N cycle Alongredox transitions in stratified water columns and sedimentsnitrification and NO2

ndash and NO3ndashreduction are tightly coupled

in space with nitrification supplying NO2ndash for anammox (Lam

et al 2007) or the NO3ndash needed for denitrification (Seitzinger

1988 Seitzinger et al 2006) Nitrification is inhibited by low(60-100 microM) H2S concentrations (Joye and Hollibaugh 1995)Thus the presence of increasing amounts of H2S may uncou-ple these processes potentially altering the microbial consor-tia that perform them (Joye and Hollibaugh 1995) AlthoughH2S has been shown to impact nitrification other work incoastal systems has found that nitrification rates are unrelatedto H2S concentrations (Caffrey et al 2003) and that the pres-ence of Fe(III)-containing minerals such as ferrihydrite canrelieve sulfide inhibition of nitrification (Dollhopf et al 2005)suggesting a complex interplay between the N cycle and othergeochemical cycles in coastal sediments

Just as H2S can have significant effects on nitrification sul-fur availability influences NO3

ndash reduction processes as wellH2S is toxic to many sensitive biomolecules (eg enzymes)high ambient H2S can inhibit the final two reductases(Sorensen 1978) of the denitrification sequence therebyshunting the denitrification sequence over to an alternativeprocess such as DNRA (Brunet and Garcia-Gil 1996 Senga etal 2006) In addition to the microcosm and lab culture evi-dence for H2S affecting a shift to DNRA ecosystem-level mea-surements also suggest increased DNRA under higher sulfideconditions (Gardner et al 2006) However H2S may also serveas an electron donor in a chemolithoautotrophic form ofdenitrification in which case the H2S can be oxidized to ele-mental S or SO4

2ndash with a simultaneous reduction of NO3ndash to N2

(and possibly NH4+) Increasing H2S enhances denitrification

in environments with high chemolithoautotrophic S-drivendenitrification (Burgin et al unpubl data) Thus the effectsof H2S on denitrification are nonlinear and may vary consid-erably between environments It is likely that at sufficientlylow concentrations H2S may enhance denitrification how-ever once it reaches toxic levels it may inhibit key enzymesallowing alternative processes to be favored (Senga et al2006) On the other hand metal-bound sulfides such as FeSalso can be oxidized by these bacteria but do not show theenzymatic inhibition of denitrification (Brunet and Garcia-

Gil 1996) and these often are abundant in sediments(Holmer and Storkholm 2001) Anammox too is sensitive tohigh sulfide concentrations as has been documented inhypolimnetic Baltic Sea waters (Jensen et al 2008) Howeverthere is little information about how sediment anammoxresponds to increased H2S concentrations In the Thamesestuary anammox rates decreased along the length of theestuary which the authors attributed to an increase in sulfideconcentrations (Trimmer et al 2003) However many param-eters covary along the gradient making it difficult to separatethe effects of H2S from changes in organic matter and salin-ity

Effects of increased salinity Of the different N-cyclingmicrobial communities we know the most about how nitri-fiers change along salinity gradients Nitrifiers have showndistinct community composition along salinity gradients indiverse estuarine environments including large estuaries suchas San Francisco Bay USA (Mosier and Francis 2008) andChesapeake Bay USA (Francis et al 2003) smaller estuariessuch as Plum Island Sound Massachusetts USA (Bernhard etal 2005) New England USA salt marshes (Moin et al 2009)and the coastal subsurface (Santoro et al 2008) In all theaforementioned cases overall genetic richness of the nitrifercommunity was lowest at the highest salinity sites suggestingthat increased sea level will result in reduced nitrifier diversitywhere marshes cannot trangress landward When observed asa function of salinity nitrification rates have shown a varietyof responses In sediments of the Scheldt estuary Netherlands(Andersson et al 2006) as well as in a survey of nine NorthAmerican estuaries (Caffrey et al 2007) increased salinitydecreased nitrification rates Other estuarine studies havefound the highest nitrification rates at intermediate salinitiesincluding Plum Island Sound (Bernhard et al 2007) and theDouro River estuary in Portugal (Magalhaes et al 2005)Increased salinity results in a greater efflux of NH4

+ from sedi-mentary environments (Rysgaard et al 1999) further suggest-ing a potential decrease in nitrification rates

The impact of salinity on N fixation denitrifying andanammox microbial communities is even less clear (reviewedin Santoro 2010) Few studies have examined relationships ofsalinity to N fixation but mesocosm manipulations of salinitywithin the range of 02 to 4 ppt found no effect on N fixationrates of cyanobacterial mats from oligotrophic Carribeanmarshes (Rejmankova and Komarkova 2005) A laboratoryexperiment testing sediments of the Pawcatuck River estuaryin Rhode Island USA found no effect of salinity on denitrifi-cation rates (Nowicki 1994) In sediments from the RandersFjord estuary Denmark denitrification decreased as salinitywas experimentally increased from 0 to 10 psu but furtherincreases showed no impact (Rysgaard et al 1999) In terms ofthe microbial community diversity of denitrifiers has beenshown to be highest at intermediate salinities (Santoro et al2006) in the coastal subsurface but greatest at low salinities inthe Chesapeake Bay (Bulow et al 2008) Alhough studies of


72

the response of anammox and DNRA organisms to increasedsalinity are few two studies have shown decreased rates ofanammox along increasing salinity gradients (Trimmer et al2003 Rich et al 2008) A recent study in the Cape Fear Riverestuary (North Carolina USA) however found an increasedrichness of anammox organisms along an increasing salinitygradient (Dale et al 2009) A lower abundance of nrfA genesa marker for DNRA organisms was found at higher salinitiesin the Colne River estuary UK (Smith et al 2007)

Because so many environmental factors covary in estuarinesystems several laboratory experiments have attempted todirectly test the effect of increased salinity on multiple N-cycling processes Laboratory experiments offer the advantageof controlling for the effects of other variables to isolate theeffects of salinity on microbial communities and geochemicalrates For example Weston et al (2006) incubated freshwaterriver sediments from the Altahama River (Georgia USA) for 1month with artificial saline media The saline treated coreshad decreased methanogenesis increased sulfate reductionand decreased denitrification activity compared to controlsOverall carbon mineralization rates were also higher in thesalinity treatment suggesting that as freshwater marshesbecome more saline N-removal capacity may be reduced andbecome a net source of NH4

+ Similar predictions arise fromthe results of an experimental manipulation carried out withlake sediments from the Netherlands (Laverman et al 2007)In these experiments using flow-through reactions and a salin-ity increase to 10 psu the investigators observed an increasein DNRA of 35 nmol cmndash3 hndash1 relative to freshwater controlsDenitrification was not significantly affected by salinity andaccounted for approximately 50 of the NO3

ndash removal in boththe salinity amended cores and the freshwater cores

Effects of increased inundation An important effect ofincreased tidal marsh inundation will be decreased porewateroxygen concentrations As estuaries transition to anoxia a res-piratory succession occurs in the microbial community aselectron acceptors are used up in the order of their thermody-namic favorability magnesium (Mn) (IV) iron (Fe) (III) NO3

ndashand finally SO4

ndash However a study in the Chesapeake Bayfound that the microbial community did not shift until SO4

ndash

metabolisms began to dominate (Crump et al 2007)Because all processes in the N cycle are redox dependent

the transition to increasing anoxia associated with SLR islikely to shift both the rates and microbial communities asso-ciated with all aspects of the N cycle Nitrification by defini-tion an aerobic process is likely to be affected the most How-ever nitrification at relatively low oxygen concentrations hasbeen documented in wastewater treatment plants (Park andNoguera 2004) It has been suggested that the ammonia-oxi-dizing archaea a group only recently discovered to carry outnitrification (Koenneke et al 2005) might be low-oxygen spe-cialists carrying out ammonia oxidation in environmentswhere oxygen is too low for nitrifying bacteria (Lam et al2007 Santoro et al 2008) New discoveries about dynamics of

the N cycle in low oxygen conditions are still occurring (Lamet al 2009) thus the precise dynamics of how the N cyclingcommunity will change in response to reduced oxygen condi-tions is difficult to predict Responses of microbes to SLR aremediated by landscape dynamics (section 2A) and plant com-munities (section 2C) the interactions of which are consid-ered in further detail below (section 3)

Effects of N loading When limited by N microbial com-munities will respond to an increase in N concentrations withshifts in species composition and an increase in productivityunder N-loading conditions (Howarth and Hobbie 1982 Mor-ris and Bradley 1999) However tidal marsh microbial com-munities are often limited by the supply of labile OCAlthough refractory detrital OC is readily available in marsheslabile OC from benthic microalgae is often the primary sourceof carbon for denitrifying bacteria (Boschker et al 1999Tobias et al 2003) Primary production by benthic microalgaeis stimulated by N loading but only when light is not a limit-ing factor Thus in marshes in which bacteria involved in Ncycling are limited by carbon microbial responses to N enrich-ment may be spatially variable with the largest increases inbacterial productivity in tidal creek bottoms and sparselyshaded creek banks and little increase in bacterial productivityin the more shaded marsh interior (Deegan et al 2007) Mean-while N enrichment can cause algal species shifts (eg morediatoms less cyanobacteria) that while increasing the labilityof algal carbon also result in a decrease in the abundance ofN-fixing bacteria (Deegan et al 2007)

2C Effects on plant communitiesmdashA combination of stressorscan have a greater impact on tidal marsh plant communitiesthan exposure to a single stress (McKee and Mendelssohn1989) In tidal marshes seawater inundation often acts incombination with increased salinity (Flynn et al 1995) andH2S (Gribsholt and Kristensen 2003) concentrations There-fore the following paragraphs review not only the effect ofSLR inundation on plant communities but also the addedimpacts of increased H2S salinity and evapotranspiration(ET) along with the interacting stressor of N loading

Effects of increased inundation The amplitude of tidalinundation is an important predictor for plant species occur-rence in both fresh and marine tidal marshes (Bockelmann etal 2002) McKee and Patrick (1988) found that the elevationgrowth range of Spartina alterniflora directly increased with anincrease in tidal amplitude Common North American tidalmarsh species (eg Juncus gerardi and Spartina maritima) areadapted to the unique hydrologic conditions of aquaticecosystems One specific adaptation to increased inundationis the amount of aerenchymous tissue which facilitates deliv-ery of oxygen to the sediment (Castellanos et al 1994 Hackerand Bertness 1995) Not all plant species are equally adaptedto tolerate flooding thus increasing inundation substantiallydecreases species richness stem length and seedling emer-gence and growth in species such as Impatiens capensis andPilea pumila (Baldwin and Mendelssohn 1998 Middleton


73

1999 Hopfensperger and Engelhardt 2008) Baldwin et al(2001) found flooding to affect annual species more dramati-cally than perennials Increased inundation can also cause ashift in energy allocation by increasing rootshoot ratios inplants (Gribsholt and Kristensen 2003) However even thoughplants may produce more roots there have been conflictingresults on whether or not the amount of aerenchymous tissueincreases with inundation (Burdick and Mendelssohn 1987Pearson and Havill 1988)

Water-storage changes in areas with low plant cover aredriven by the process of evaporation while storage in areaswith high plant cover is driven by plant transpiration (Grib-sholt and Kristensen 2003 Paquette et al 2004) A positive-feedback relationship exists by which high transpiration ratesenhance soil oxidation and enlarge the aerated layer (Hemondand Fifield 1982 Dacey and Howes 1984 Howes et al 1986)thus creating conditions for plant community developmentthat further loosen the soil and increase ET rates (Ursino et al2004 Li et al 2005) Plant canopy structure can also influenceET rates whereas transpiration rates are highly correlated withleaf-area index (Hussey and Odum 1992) In tidal freshwatermarshes where leaf density is high transpiration dominatesover evaporation however in salt marshes where there islower leaf density evaporation and transpiration rates areapproximately equal (Hussey and Odum 1992) Not only doET rates influence soil aeration but ET can indirectly influ-ence soil surface elevation through biomass production andsoil compressibility (Paquette et al 2004) Therefore a rise insea level could shift the system to a salt marsh resulting indecreased transpiration rates and soil aeration However theeffect of SLR on marsh ET could be countered if the marshreceived high N loads at the same time then biomass tran-spiration rates and soil aeration could all increase

Effects of increased SO42ndash An increase in SO4

2ndash reduction toH2S due to increased seawater inundation has multipleeffects on tidal marsh plants H2S directly suppresses the activ-ity of enzymes responsible for anaerobic respiration in theroots of wetland plants (Allam and Hollis 1972 Pearson andHavill 1988 Koch et al 1990) The dramatic decrease in plantrespiration causes a direct decrease in growth of roots shootsand leaves (Pezeshki et al 1988 Koch et al 1990 Armstronget al 1996) Growth reduction due to H2S can limit rhizos-phere aeration (Armstrong et al 1996) and lead to plant death(Wiessner et al 2007) Increased concentrations of H2S havealso been found to inhibit N uptake and assimilation in a vari-ety of tidal marsh plant species ( DeLaune et al 1984 McKeeand Mendelssohn 1989 Koch et al 1990 Chambers et al1998 Wiessner et al 2008) The synergistic interactionbetween the effects of increased inundation and H2S on Nuptake and energy production in plants results in a greaterresponse in the plant community compared to when the stres-sors are isolated (Koch et al 1990 Webb and Mendelssohn1996) The inhibition of N uptake due to high H2S results inhigher CN ratios in plant tissues (Chambers et al 2002) In

addition decreased plant uptake of N can result in higherporewater NH4

+ concentrations (Flynn et al 1995) Howeverin marshes significantly enriched in N H2S inhibition of plantN uptake can be overcome (Portnoy and Giblin 1997) Lastsulfide can also harm plants in aerobic conditions by reducingroot respiratory capacity and lowering root energy production(Allam and Hollis 1972 Havill et al 1985 Pearson and Havill1988) Thus once a pulse of salt water brings sulfide into thesystem damage to plants will occur whether the system is aer-obic or anaerobic

Although marsh plants are negatively affected by H2S inmany ways they have several positive- and negative-feedbackeffects on H2S concentrations in the sediment Plant rootsrelease oxygen creating aerobic microhabitats (Howes et al1986 Gribsholt and Kristensen 2003 Choi et al 2006) whichsubstantially decrease SO4

2ndash reduction rates (Stribling andCornwell 2001 Wiessner et al 2007) Stribling and Cornwell(2001) found a decrease in root oxygen production duringplant senescence However while plants inhibit SO4

2ndash reduc-tion through sediment oxidation they may also facilitateSO4

2ndash reduction by providing a high carbon load which fuelsthe microbial reduction process (Gribsholt and Kristensen2003 Miley and Kiene 2004 Wiessner et al 2007) The rela-tive influence of plants on these opposite processes may varybetween species and over time In a Spartina alterniflorandashdom-inated salt marsh Hines et al (1989) found SO4

2ndash reductionrates increased in the spring with plant growth and high dis-solved organic carbon (DOC) root delivery and then decreasedin the fall with a decrease in DOC delivery whereas reductiongenerates toxic H2S Many of the SO4

2ndashndashreducing bacteria asso-ciated with plant roots in salt marshes and seagrass beds alsofix N which is rapidly transferred to plants and is particularlyhigh during seasons of plant growth (Lovell 2002) Howeverthese types of plant-microbe associations can be quite specific(Bagwell et al 2001) and the general effects of increased H2Sconcentrations on these interactions are not well known

Effects of increased salinity Increased salinity can havedevastating effects on freshwater plants through two directmechanisms (1) increased salt concentrations that change thewater potential gradient creating a water deficit in plant tis-sues and (2) direct plant uptake of toxic concentrations ofsodium and chloride ions (Greenway and Munns 1980 Flynnet al 1995) Pezeshki et al (1987) found decreased stomatalconductance and photosynthesis as a consequence ofincreased salinity In addition saline waters can decreaseabove and belowground plant growth (Portnoy and Valiela1997 Van Zandt et al 2003) and species richness (Howard andMendelssohn 2000) and lead to death (Grace and Ford 1996)A larger scale implication of saltwater intrusion is an increasein abundance of invasive species particularly those adapted tobrackish conditions such as nonnative Phragmites australis inNorth America (Baldwin and Mendelssohn 1998 Chambers etal 2003 Packett and Chambers 2006) In marine tidalmarshes from which some of the invasive plants may origi-


74

nate plant tolerance of saline conditions is linked to Ndemand as N-rich compounds such as proline and glycinebetaine are thought to be used in osmotic regulation by halo-phytes (Stewart and Lee 1974 Cavalieri and Huang 1979)

Importantly both local water depths and salinity areexpected to change with SLR Although many studies haveexamined the independent effects of local salinity and localwater depths on tidal marsh zonation and succession (egOdum 1988 Silvestri et al 2004 Pennings et al 2005 DrsquoAl-paos et al 2006) few studies have examined their joint effecthighlighting a research need

Effects of N on plant response to SLR N loading may con-strain the responses of plant communities to SLR by favoringabove-ground rather than below-ground biomass production(Tyler et al 2007 Langley et al 2009) Increases in productiv-ity that occur as a consequence of N loading to an N-limitedsystem (eg salt marshes) may not translate into increasedorganic matter accretion that is required for these wetlandecosystems to maintain elevation particularly when produc-tivity is altered by shifts in community structures of primaryproducers as in cases of algal blooms and hypoxia (Havens etal 2001) In fact the loss of below-ground biomass accumula-tion that resulted from a 36-year nutrient experiment in saltmarsh plots in Massachusetts USA caused a negative elevationchange in the marsh surface of 15 mm yrndash1 (Turner et al2009) N loading may also shift competitive interactionsbetween macrophytes in a way that favors the rapid spread ofinvasive species (Tyler et al 2007)

3 Effects of SLR and N loading on wetlandshypotheses from a complex-systems approach

Predicting the manner in which SLR will affect the trans-formations residence times and ultimate fate of N in tidalmarshes is complex due to the involvement of several drivingvariables (eg water depth dissolved oxygen microbialactivities macrophyte abundance and root density hydro-logic retention times DOC and N supply) and multiple feed-back loops in tidal marsh N cycling (Figs 2-5) Even theeffects of SLR on marsh ecosystem structuremdashthe first-ordercontrol on marsh ecosystem functionmdashare complex Webegin this section by examining the feedbacks governingtidal marsh elevation relative to sea level and hence ecosys-tem structure Second we examine the feedbacks that controlthe efficiency of that marsh structure in transforming N Thisldquoefficiencyrdquo will differ between marsh locations along andacross the estuarine gradient (Fig 1) We predict responsesthat key regions are likely to exhibit from the interacting per-turbations of SLR and N loading interior of salt or brackishmarshes (section 3B) tidal creeks (section 3C) and tidalfreshwater marshes (section 3D) We also examine in detailthe hypothesized feedbacks that likely influence N cyclingefficiency in those regions

3A Biophysical feedbacks on marsh elevationmdashAutochtho-nous processes (peat accretion) Organic sediments are

deposited autochthonously when the rate of organic matterproduction exceeds that of decomposition With other envi-ronmental factors held constant autochthonous sedimentaccretion in a given vegetation community exhibits a humpedresponse to local water depths with an optimum water depthfor accretion (Morris et al 2002 Larsen et al 2007) At depthsthat exceed the optimum plant community productivity islimited by anaerobic stress whereas at depths shallower thanthe optimum productivity is limited by soil salinization stress(Phleger 1971 Morris et al 2002) andor more aerobic redoxpotentials make decomposition more efficient (Brinson et al1981 DeBusk and Reddy 1998) Because they are more pro-ductive low marsh communities often have larger autochtho-nous peat accretion rates than high marsh communities(Fitzgerald et al 2008) However other interacting factors(eg soil or water chemistry specific vegetation communitycomposition) may also contribute to local variability inautochthonous sediment accretion rates and could over-whelm the influence of local water depth (Stribling et al 2007Kirwan and Murray 2008 Turner et al 2009)

Because of organic matter production and decompositiondynamics (Fig 6) marsh communities approach a stable equi-librium elevation with respect to constant tidal forcing withina range of hydrologic perturbation Biophysical feedbacksmaintain that equilibrium perturbations that increase localwater depth cause a decrease in organic matter decompositionand possibly an increase in plant productivity resulting inaccretion to the equilibrium perturbations that decrease localwater depth cause subsidence and a return to the equilibriumConsequently SLR that initially causes an increase in localwater depths may promote faster autochthonous sedimentaccretion so that the vegetation community asymptoticallyapproaches a new dynamic equilibrium with the shiftingmean high water level (Hussein et al 2004 Mudd et al 2004Temmerman et al 2004 DrsquoAlpaos et al 2007)

In freshwater tidal marshes the autochthonous accretionresponse to SLR is complicated by the effects of saltwaterintrusion (Fig 3) Field surveys (Craft 2007) and laboratoryexperiments (Weston et al 2006) have demonstrated that highsalinities increase decomposition and decrease soil accretionrates Increasing salinity increases aerobic decomposition byexpanding the habitat range for burrowing marine crabs (Craft2007) and reduces plant productivity (discussed in Section2C) resulting in a decreased equilibrium elevation for the veg-etation community (Wheeler 1999 Mendelssohn and Morris2000 Pezeshki 2001) (Fig 6) In addition the SO4

2ndash introducedby seawater favors sulfate-reducing bacteria over slow-growingmethanogenic bacteria that typically dominate decomposi-tion processes in freshwater wetlands (Keller and Bridgham2007) This shift from methanogenesis to sulfate reducingconditions may create concomitant increases in organic mat-ter decomposition (eg Portnoy and Giblin 1997) whichcould further contribute to decreased wetland elevations Overlonger timescales the shift in vegetation to more salt-tolerant


75


76

Fig 3 Autochthonous and allochthonous sediment accretion feedbacks affecting N removal in tidal marshes This figure shows in detail processes thatare collapsed in Figs 2 4 and 5 See the Fig 2 caption for a guide to interpreting the diagram

Fig 2 Biogeochemical feedbacks and interactions affecting long-term N removal in tidal marshes Proximal stressors expected to increase in magni-tude as a result of SLR are shown in red boxes Red solid and blue dashed arrows indicate positive and negative effects respectively green dotted arrowsindicate effects that may be positive or negative depending on environmental specifics Arrows are multiplicative determining the indirect influence ofa stressor on a variable requires tracing the path of the effect where a positive increase in a driver that has a negative impact on a proximal variable willlead to a decrease in that proximal variable If that variable has a negative impact on a second proximal variable that variable will increase in responseto the distal driver


77

Fig 4 Effects of global change on vertical flow processes affecting N removal in interior tidal marshes Away from creek banks horizontal flow is min-imal and most N removal is driven by vertical flow paths that bring nutrients in contact with organic carbon and microbial communities As describedin part 2 SLR is expected to decrease groundwater discharge to tidal marsh interiors and warmer temperatures associated with climate change areexpected to increase rates of evapotranspiration See the Fig 2 caption for a guide to interpreting the diagram Blue boxes represent proximal stressorsexpected to decrease in magnitude with SLR

Fig 5 Nitrogen removal driven by horizontal and vertical flow through creek banks associated with tidal forcing This process is hypothesized to be aprime mechanism for removal of N originating in surface-water See the Fig 2 caption for a guide to interpreting the diagram

communities that accompanies salinity changes woulddecrease the lability of the organic matter produced (Odum1988 Craft et al 2009) which could counteract the effect ofincreased decomposition rates

For tidal salt marsh vegetation communities to sustain adynamic equilibrium with SLR perturbations to local waterdepth must be within the basin of attraction (Fig 6) for theequilibrium point Large perturbations may increase localdepths to a point where the community succumbs to anoxicstress is outcompeted by a lower-elevation marsh communityor produces organic matter at a rate that no longer exceedsdecomposition These perturbations which occur when SLR israpid relative to maximum rates of soil accretion result inreplacement of high marsh communities with low marshcommunities or of high or low marsh communities by openwater In many locations worldwide current rates of SLR areexceeded by maximum rates of low marsh soil accretion butapproximately match maximum rates of high marsh soilaccretion (Fitzgerald et al 2008) Thus if SLR accelerates in amanner consistent with predictions (IPCC 2007) many highmarsh communities may be replaced by less diverse but moreproductive low marsh communities (Boorman et al 2001) inseveral locations this replacement is already occurring (Don-nelly and Bertness 2001) Where diverse high marsh commu-nities persist soil elevations tend to exhibit greater variance

than marshes with a dominant species (DrsquoAlpaos et al 2007)Allochthonous processes (sedimentation) Allochthonous

delivery of sediment to tidal marshes can significantly impactoverall marsh accretion rates Marshes with high incomingsuspended sediment concentrations are considered bestequipped to persist under conditions of rapid SLR (Temmer-man et al 2004) but suspended sediment loads of many ofthe worldrsquos rivers have decreased during the Holocene (Day etal 2008) Storm events which are expected to increase in fre-quency as a result of SLR (IPCC 2007) are commonly associ-ated with substantial sedimentation (Slocum et al 2005Cahoon 2006 Day et al 2008) Suspended sediment concen-trations tend to increase roughly linearly with maximuminundation height (Temmerman et al 2003) and severalresearchers have suggested that enhanced flooding of tidalmarshes would lead to greater allocthonous sedimentation(Baumann et al 1984 Reed 1995 Anthony 2004) Howeverchanges in suspended sediment delivery to coastal systemsthat result from urbanization or altered water managementpractices may overwhelm the response of tidal marshes to SLR(Watson 2008) Furthermore the extent and location of sedi-ment deposition tends to be site specific (Reed 1995 French2006) and is a function of sediment characteristics the exis-tence of conditions that promote flocculation and vegetationcharacteristics (Pasternack and Brush 2002)


78

Fig 6 Carbon fluxes contributing to net autochthonous soil accretion in tidal marshes Autochthonous soil accretion occurs when rates of organicmatter production exceed rates of organic matter decomposition the soil surface elevation is in equilibrium with respect to water level when produc-tion and decomposition rates are equivalent Production and decomposition of organic matter are both highly sensitive to local water depths or thedifference between the water surface elevation and soil surface elevation Both of these processes are also sensitive to salinity This diagram depicts onlythe response of decomposition to salinity because the response of primary production is community specific The dynamics of production and decom-position result in a basin of attractionmdasha range of soil surface elevations that eventually aggrade or degrade over time (shown by thin arrows) to theequilibrium elevation

Predicting tidal marsh persistence under SLR Predicting thepersistence transgression or changing zonation patterns oftidal marshes in response to SLR is an active area of research(reviewed in Fitzgerald et al 2008) Inundation of tidalmarshes and shifts in species composition (eg salt-intolerantto salt-tolerant or annual to perennial dominance) resultingfrom SLR may occur at a relatively constant rate (eg for slop-ing marsh surfaces) or exhibit a threshold response (eg inun-dation of a tidal platform andor rapid inundation followingbreaching of barrier islands (Fitzgerald et al 2006 Fitzgerald etal 2008) In general allochthonously dominated marshesaccrete more rapidly than autochthonously dominatedmarshes and are more likely to persist under rapid SLRalthough many may still succumb to inundation (Temmer-man et al 2004 French 2006) Highly organic autochthonousmarshes also have a more compressible substrate resulting ingreater subsidence when subject to SLR (Paquette et al 2004)While the rapid accretion rates of Spartina monocultures willminimize the loss of tidal marsh area in some locations inother locations tidal marsh communities will experienceinundation (Smith et al 2000)

Although measurements suggest that many tidal marshesare accreting at a rate sufficient to keep pace with SLR(Williams and Hamilton 1995 Hartig et al 2002 Van der Waland Pye 2004) tidal marsh loss remains likely around theexpanding tidal channel network (Kirwan and Murray 2007)in locations where subsidence is occurring eg Gulf coastwetlands (Callaway et al 1997 Turner 1997) where uplandmineral inputs are curtailed (Temmerman et al 2004 French2006) where vegetation is stressed or eliminated due to otherfactors (eg marsh dieback phenomenon) (McKee et al 2004Kirwan et al 2008) or where local rates of change in the watersurface elevation are relatively rapid In these locations tidalmarshes along the estuarine gradient may shift inland in theshort term (Smith et al 2000 Craft et al 2009) Howeverunless feedback between the new vegetation community dis-tribution and soil accretion results in net accretion rates thatare greater than or equal to SLR portions of the marsh willcontinue to become subtidal Along developed coastlines netmarsh loss will be accelerated because inland shifting of tidalmarshes may be blocked by development

Due to the number of interacting factors affecting tidalmarsh persistence responses of tidal marsh structure to SLRwill be highly site-specific (French 2006) A number of modelshave been developed to predict how different combinations ofenvironmental conditions affect salt marsh persistence andstructure through their impacts on feedback between vegeta-tion sedimentation and sea-level rise (Mudd et al 2004 DrsquoAl-paos et al 2007 Kirwan and Murray 2007) Other models havealso incorporated sediment compaction and belowground bio-mass production (Mudd et al 2009) or sediment accretionrelationships specific to brackish marsh communities (Kirwanand Murray 2008) In general however due to the greaterdiversity of brackish and freshwater marsh communities and

more complex more poorly understood relationships betweensoil accretion and water level in those communities the per-sistence and structure of these marsh zones in response to SLRis less well understood a situation that highlights a researchneed

3B Predictions for salt or brackish marshes Marsh interiormdashHydrology and the physical environment Regional ground-water discharge to tidal marshes will likely decrease with SLR(Nuttle and Portnoy 1992 Tobias et al 2001a) which in turnwill immediately reduce delivery of groundwater NO3

ndash to tidalmarshes Decreased rates of groundwater discharge to tidalmarshes could have large and adverse consequences for Nbudgets in several estuaries of the Atlantic US coast wheregroundwater is a dominant source of NO3

ndash (eg ChesapeakeBay embayments of Cape Cod) In these estuaries groundwa-ter discharge locations would likely shift to subtidal zones(Tobias et al 2001a) increasing the estuarine NO3

ndash concentra-tions and possibly promoting eutrophication and the devel-opment of dead zones

Although diminished groundwater discharge to marsh inte-riors is expected to cause less delivery of reactive N species theincreased temperatures associated with global climate changeare expected to increase global ET rates which in tidalmarshes will contribute to enhanced bidirectional dispersionof the near-surface porewater (Harvey and Nuttle 1995 Har-vey et al 1995) This enhanced hydrologic mixing will ini-tially bring more parcels of surface water rich in NO3

mdash intocontact with DOC-enriched and anaerobic portions of thesubsurface resulting in greater rates of microbial NO3

ndash reduc-tion However the diminished delivery of freshwater to thesesystems via groundwater discharge combined with enhancedET will also lead to salt and solute accumulation in the rhi-zosphere (Harvey et al 1995 Tobias et al 2001a) Thus saltmarshes will likely experience higher soil salinities Further-more the decrease in the supply of dissolved Fe and Mn fromgroundwater in salt marshes will lead to less precipitation ofsulfides (King et al 1982 Slocum et al 2005 Day et al 2008)and more accumulation of H2S with subsequent increased sul-fide stress in macrophytes

Plant community dynamics We predict that macrophyteproductivity will decline in response to SLR due to increasedinundation salinity and H2S particularly in the absence of Nloading As a result interior marshes will likely deepen to alower equilibrium elevation than expected based on surface-water elevations alone Deepening will be more pronouncedin highly organic marshes where soil compression will occurdue to loss of groundwater discharge (Paquette et al 2004Whelan et al 2005 Cahoon et al 2006) and in locationswhere the thinning of stems results in less deposition of sus-pended sediments As plant productivity decreases total ETrates will also decrease diminishing dispersive mixing Thusinitial increases in NO3

ndash reduction rates that may accompanyglobal climate change as a result of enhanced global ET are notlikely to persist over the long term (Fig 4) Increased inunda-


79

tion increases rootshoot ratios of vascular plants (Gribsholtand Kristensen 2003) although N loading decreasesrootshoot ratios (Langley et al 2009) Belowground biomassis critical for maintaining marsh elevation and the effective-ness of N removal therefore future research is needed to pre-dict changes in rootshoot ratios in salt marshes facing anincrease in both sea level and N concentrations

N biogeochemistry Tidal marshes can remove up to 90 ofthe NO3

ndash in a groundwater plume (Tobias et al 2001c) How-ever alterations in NO3

ndash loading caused by SLR-driven hydro-logic changes will have cascading effects on N cycling poten-tially diminishing this removal capacity Decreasedgroundwater discharge to tidal marshes will likely cause adecrease in overall NO3

ndash reduction via microbial processessuch as denitrification and DNRA Additionally an increase inH2S may decrease the relative importance of denitrificationcompared to DNRA The NH4

+ produced from DNRA willeither be immediately exported from the marsh or taken up byplants or microbes and cycled internally rather than removedas N2 (via denitrification) to the atmosphere Concentrationsof labeled 15NH4

+ exported from a New England USA marshin an 15N tracer enrichment experiment were substantiallylower than predicted on the basis of measured DNRA ratessuggesting that the NH4

+ produced by DNRA was cycled inter-nally rather than immediately exported (Drake et al 2009)

Marsh deepening and the reduction in plant biomass willhave further cascading effects on N cycling (Fig 4) In themarsh interior the main effect of increased local water depthswill be a decrease in dissolved oxygen in the benthos whichmay limit aerobic processes like nitrification particularly asrhizosphere oxygenation declines with plant biomass Becausebenthic nitrification is five to nine times greater than water-column nitrification in tidal marshes (Gribsholt et al 2005)this effect will significantly change N dynamics Further epi-phyton communities key centers for nitrification in tidalmarshes (Eriksson and Weisner 1999) will likely be reduced inextent in stressed lower-density macrophyte communitiesConsequently the portion of denitrification that is coupled tonitrification which can be substantial in coastal sediments(Jenkins and Kemp 1984 Bodelier et al 1996 Herbert 1999)will decline Although denitrification could continue withnitrate from other sources most N may be present as NH4

+ asDNRA increases These effects will all be exacerbated if N load-ing is sufficient to induce hypoxia (in which most N is presentas NH4

+ rather than NO3ndash)

Synergistic interactions The hypothesized response of inte-rior portions of tidal marshes underscores the tenet that thesynergistic effects of multiple ecosystem stressors are substan-tially greater than the effects of any of these stressors actingalone (Day et al 2008) Alone increased inundation candecrease transpiration rates in a salt marsh but increasedinundation plus increased N loading can increase plant bio-mass and transpiration rates leading to a more oxidized sub-strate with greater rates of NO3

ndash reduction Likewise increased

local water depths can cause a longitudinal (ie upriver) dis-placement of macrophyte zonation and functionality Whengroundwater discharge also diminishes positive feedbacks dis-cussed above cause a rapid buildup of salts and sulfides deep-ening and loss of macrophyte productivity leading to greatlyreduced N turnover and diminished ecosystem functionAdded stress on these ecosystems via N loading may furtherexacerbate impacts on these impaired marshes (which cannotas efficiently transform or release N) by directly diminishingtheir ability to resist SLR via organic matter accretion In sum-mary we predict that SLR will cause a decrease in the removalof NO3

ndash and NH4+ by interior portions of salt marshes and that

this decrease in ecosystem function will be most pronouncedin locations where groundwater discharge has been signifi-cantly diminished

3C Predictions for salt or brackish marshes Tidal creek chan-nels and tidal creek vicinitymdashPhysical and biogeochemical envi-ronment A major effect of SLR could be increased dissectionof tidal marshes by an expanding tidal channel network (Kir-wan et al 2008) resulting in an increased marshchannelinterface area Presently tidal creek banks are among the mostaerated (Gribsholt et al 2005 Wilson and Gardner 2005) well-flushed (Howes and Goehringer 1994 Wilson and Gardner2006) and productive (Howes and Goehringer 1994 Wilsonand Gardner 2006) parts of tidal marshes Rhizopsheres of tall-form Spartina alterniflora and fiddler crab burrows supporthigh rates of N cycling across coupled oxic and anoxic sedi-ments As a result the portions of marshes fringing tidal chan-nels have been reported to be net sinks for inorganic N speciesfrom tidal marshes (Whiting et al 1989 Anderson et al 1997)and a whole-ecosystem 15N tracer enrichment study providespreliminary evidence of denitrification in creek banks duringdrainage (Gribsholt et al 2005) Tidal creek bottoms are alsoimportant sites for denitrification accounting for 60 of totalmarsh denitrification measured in a New England salt marsh(Kaplan et al 1979)

Synergistic effects Given that the tidal creekmarsh inter-face is a current hotspot for N transformations we expect thatan expansion in the total area of this interface will result ingreater total NO3

ndash reduction in portions of the marsh that abuttidal creeks Examination of the more indirect effects of SLRon marshcreek systems (Fig 5) leads us to further hypothesizethat per unit length of creek bank nitrification and denitrifi-cation may become even more efficient For exampleincreased tidal amplitudes lead to larger volumes of drainagethrough the creek bank and longer flow paths and residencetimes for porewater flowing from the marsh through the creekbank to the channel (Wilson and Gardner 2006) all of whichwould be expected to enhance total denitrification (Seitzingeret al 2006) Increased turbulence intensities and enhancedflocculation of fine material mediated by increased salinitieswould further contribute to the evolution of higher creekbanks due to the relatively high settling velocities of com-pound flocculated particles (Larsen et al 2009a) Higher creek


80

banks would result in a larger volume of water drainingthrough the banks (Howes and Goehringer 1994) furtherincreasing the potential for denitrification Additionallylarger grain sizes on the creek bank could result in higherporosities higher redox potentials and a higher potential forcoupled nitrificationdenitrification Furthermore depositionof relatively large sediment grains on tidal marsh surfaces hasbeen linked to benthic algal colonization (Cahoon et al 1999Croft et al 2006) which could further promote coupled nitri-ficationdenitrification (Krause-Jensen et al 1999) and stabi-lize the sediment while countering the greater erosion poten-tial of a more turbulent tidal creek Deposition of flocculatedparticles in the vicinity of creek banks may also provide anadditional influx of allochthonous organic carbon to themarsh benthos that could support denitrification Finallylarger populations of burrowing organisms pushed furtherinland by increasing salinity would further aerate the sedi-ments of marshes fringing tidal channels (Croft et al 2006)again promoting coupled nitrificationdenitrification

Tidal creek channel bottoms serve as the major site of den-itrification in some marshes because of relatively large fluxesof nitrate-rich water across the biogeochemically reactivecreek bed (eg Nowicki et al 1999) Within creek bottomsthe effect of SLR on the N cycling will likely vary along theestuarine gradient As in the marsh interior deeper portionsof tidal creeks will experience lower redox potentials that pro-mote denitrification but inhibit coupled nitrificationdenitri-fication and more saline portions of tidal creeks will likelyexperience an increase in the importance of DNRA relative todenitrification However in contrast to marsh interior zonesdenitrification in tidal creek beds is additionally controlledby variations in flow velocity (OrsquoConnor et al 2006) whichis expected to increase with SLR When flows are slow (shearvelocity less than 023 cm sndash1) further increases in velocitytend to promote denitrification whereas when flows are fast(shear velocity greater than 039 cm sndash1) further increases inflow tend to inhibit denitrification (OrsquoConnor and Hondzo2008) Thus near the heads of tidal creeks or during slowlyflowing portions of the tidal cycle SLR will likely increasedenitrification whereas seaward portions of the tidal creekwill likely experience lower denitrification rates The portionsof the creek channel most effective for denitrification willessentially be likely to shift inland Because the tidal creeknetwork will likely expand laterally and longitudinally as aresult of SLR we predict that the total amount of nitrateremoval occurring in tidal creek bottoms may not substan-tially change as a direct consequence of SLR Similarly totalnitrification in tidal creek beds may also change little withthe most effective regions for nitrification shifting inlandHowever where human development restricts inland shifts ofthe tidal creek network a loss of total N removal in creek bedsmay occur

When N loading is combined with SLR total N removal viadenitrification and coupled nitrificationdenitrification is

likely to increase substantially in both creek beds and creekbanks Fertilization experiments in a Massachusetts USAmarsh revealed that N loading may increase denitrification byan order of magnitude in tidal creek sediments and couplednitrificationdenitrification 3-fold (Koop-Jakobsen and Giblin2010) An increase in the total area of creek bed resulting fromSLR (eg Kirwan et al 2008) would further increase total creekbed N removal Moreover the fertilization experimentincreased the productivity of benthic macroalgal productionin sparsely shaded creek banks and beds As a result bacterialcommunities in these locations were relieved of limitation bythe labile organic carbon supply and were more productive incontrast to the bacterial communities in the shaded marshinterior (Deegan et al 2007) Thus the greatest efficiencygains in total N removal in tidal creek banks and creek bedsmay result from a combination of SLR and N loading whichhighlights the importance of considering interacting multiplestressors

3D Predictions for tidal freshwater marshesmdashPlant commu-nity dynamics In tidal freshwater marshes the dominantphysical effects of SLR will be increasing salt water intrusionand increasing tidal inundation frequency and duration As aconsequence of these changes SLR can cause different shiftsin tidal freshwater marsh plant communities salt-intolerantto salt-tolerant species andor a shift of dominant life formsin which a community codominated by annuals and perenni-als shifts to a plant community dominated by perennialspecies Both of these shifts in community structure will resultin a community that is less diverse and less resistant to inva-sion than the former freshwater marsh ecosystem These plantcommunity changes will have a dramatic impact on organiccarbon quality given the substantially higher CN ratios of saltmarsh (Craft et al 2009) and perennial plant tissues(Hopfensperger et al 2009a) Thus when freshwater marshspecies shift to more halophytic and perennial species detritalorganic matter becomes more refractory which leads to adecrease in organic matter decomposition rates and anincrease in soil surface elevation (Morris and Bowden 1986)that could compensate for an increase in tidal amplitudeHowever N loading may compensate for the effects of speciesshifts on organic matter quality by increasing tissue N content(Drake et al 2008)

The plant community shifts associated with SLR would alsodecrease porewater concentrations of dissolved inorganicnitrogen through massive plant uptake compared to thenative heterogeneous freshwater marsh community (Findlayet al 2002 Windham and Meyerson 2003 Windham-Myers2005) The shift from a mixed community to one dominatedby perennials may lead to increased nutrient retention asperennial species store nutrients that are not recycled eachyear in their below-ground vegetative structures Moreoverthrough time a shift to perennial dominance could diminishthe density and diversity of the seed bank since it will not bereplenished year after year by annual species (Hopfensperger


81

et al 2009b) thereby perpetuating the dominance of peren-nial andor invasive species

N biogeochemistry Increasing soil salinities and H2S con-centrations will have many of the same repercussions as dis-cussed above for salt marshes including an increase in theimportance of DNRA relative to denitrification and anammoxsubsequently resulting in less effective removal of N to theatmosphere In addition the decrease in organic matter qual-ity due to changes in the plant community may cause a shiftfrom N mineralization to bacterial immobilization and pro-vide further support for a shift from denitrification to DNRAPotential denitrification rates and N2O production are signifi-cantly greater in tidal freshwater marshes than in salt marshes(Dodla et al 2008) suggesting that upriver shifts in vegetationzonation resulting from SLR will reduce denitrification andreduce N2O emissions to the atmosphere Similarly lower soilNO3

ndash concentrations have been found in homogenous areasdominated by perennials which may lead to lower denitrifi-cation rates (Hopfensperger et al 2009a) The extent to whichN2O emissions will be altered in response to changing marshdistributions is an area in need of assessment through furthercontrasts of these ecosystems

Synergistic effects Similar to interior salt marshes the pre-dicted response of tidal freshwater marshes to multiple per-turbations is different from the response to one stressor actingalone An increase in H2S concentration due to increased saltwater will inhibit plant uptake of N and reduce plant produc-tivity leading to a deepening of the marsh surface thoughsalinity-induced species shifts accompanied by higher organicmatter CN ratios will to some degree counteract this effectAdditionally when significant N loading is coupled with anincrease in H2S concentration the inhibitory effects of H2S onmacrophytes may be overcome by the abundantly available Nfurther increasing rates of soil accretion Overall we predictthat SLR-induced inundation coupled with plant communityshifts will result in an increased importance of DNRA and bac-terial N immobilization ultimately resulting in an ecosystemthat retains more N and is less effective at permanent Nremoval from the watershed In areas experiencing both SLRand N loading we predict the additional N will lead to a shiftfrom fermentative DNRA to sulfur-driven DNRA but stillresult in a system that retains more N than the previous fresh-water marsh

CONCLUSIONSThe main ecological effect of climate change is often

viewed as inducing unidirectional shifts in community zona-tion and associated ecosystem functioning along gradients(eg low-elevation communities will replace high-elevationcommunities) with the structure and function at the end ofthe gradient being lost To some extent this general pattern isconsistent with predicted responses of tidal marshes to SLRincreased salinities and depths may cause an upriver shift inmacrophyte zonation and N cycling However this simplified

view does not account for cross-scale interactions and syner-gistic feedbacks that can significantly alter the value of the N-related ecosystem services provided by tidal marshes

We hypothesize that cross-scale interactions and feedbacksin wetlands responding to SLR will either enhance or diminishN removal mainly through impacts on NO3

ndash reduction (deni-trification and DNRA) or coupled nitrificationdenitrificationOn one hand sediment accretion feedbacks can reduce the lossof tidal marsh area and upriver translation of marsh structureand function by compensating for increased surface-water ele-vations On the other hand diminished freshwater flushing bygroundwater discharge could shift patterns of salinity H2S andwater depth resulting in shifting patterns in dominant Ncycling processes in tidal marshes with likely adverse conse-quences for N removal We predict these changes will lead todecreased N removal from salt- and freshwater tidal marshinteriors where increases in DNRA relative to denitrificationare expected In contrast positive feedbacks between SLR tur-bulence disturbance and vegetation dynamics will likely leadto enhanced dissection of tidal marshes by tidal creeks whichdespite the loss of rooted vegetation will likely lead to localenhancement of rates of nitrification and denitrification

Whether the overall N-removal function of a particulartidal marsh increases or decreases under SLR depends on sev-eral site-specific factors including sediment microbialmacrophyte and hydrologic characteristics and whether pri-mary sources of NO3

ndash and NH4+ to the receiving estuary are

groundwater or other sources In estuaries receiving nutrientspredominantly from surface-water the increase in hydrologicexchange between surface-water and porewater through tidalcreek banks and the accompanying N reduction may be suffi-cient to overcome a decrease in N removal from the marshinterior In contrast in estuaries where groundwater is the pri-mary source of nutrients the loss of denitrification alonggroundwater discharge flow paths may dominate the whole-marsh N removal response to SLR The site-specificity of theresponse of tidal marsh ecosystem functions to SLR under-scores the need for combinations of experimental field studiesand process-based numerical models (French 2006)

The growing awareness of how cross-scale interactions andfeedbacks will affect the ecosystem services provided by tidalmarshes will promote more realistic valuation of these driversin cost-benefit analyses and will improve coastal manage-ment For example this review argues against actions thatdraw down upland coastal aquifers and further reduce ground-water discharge to tidal marshes It also makes a case againstnew dam construction that would reduce the sediment loadscarried by rivers feeding into tidal marshes and further con-tribute to marsh deepening Likewise it suggests that incisionof tidal creeks might not decrease a marshrsquos capacity fornitrate removal and thus that management to curtail creekincision may not be necessary Finally in synthesizing thisconceptual model we have identified several new hypothesesthat should be tested to fully understand how SLR will impact


82

N removal ecosystem services This synergistic understandingwill lead to improved holistic forecasting of marsh response toclimate change

GlossaryAerenchymous tissue Plant tissue with large air spaces that facil-itates delivery of oxygen to the sedimentAerobic Requiring oxygen to occurAllochthonous Found in a place other than where formationoccurredAnaerobic Occurring in the absence of oxygenAnammox The anaerobic oxidation of ammonia by microor-ganisms that use NO2

ndash as an electron acceptor and NH4+ as an

electron donor in a chemolithotrophic metabolismAnnuals Plants that complete their life cycle within 1 yearAnoxia The absence of oxygenAquifer Porous rock or sediment that is permeable and satu-rated with waterAutochthonous Local found at the same location as formationBasin of attraction The set of initial conditions leading to long-term behavior that approaches a particular equilibriumBed shear stress The area-normalized force of flowing water onthe underlying surfacesedimentChemolithoautotrophic Obtaining the necessary carbon formetabolic processes from carbon dioxide fixation while usinginorganic compounds such as nitrogen iron or sulfur as anenergy sourceDead zones Areas of the coastal ocean that cannot support lifeowing to depleted oxygen levels thought to be caused byincreased nutrients that cause harmful algal bloomsDenitrification respiratory a form of anaerobic respiration inwhich microbes convert nitrate (NO3

ndash) to increasingly reducedN forms (nitrite gaseous NO N2O or N2) The full reductionto N2 is of particular importance because N2 is much less bio-logically available and reactiveDenitrifiers Organisms that perform denitrificationDispersion A bidirectional movement of water and solutes dueto diffusion and nonuniform flowDissimilatory nitrate reduction to ammonium (DNRA) An energy-generating microbially catalyzed conversion of nitrate (NO3

ndash)to ammonium (NH4

+) under anaerobic conditionsFermentative DNRA that is thought to occur under condi-tions of high labile organic carbon availabilitySulfur-driven DNRA that is thought to occur where sulfur-oxidizing bacteria have access to NO3

ndash Sulfide (H2S) isthought to be the electron donor in the process

Distal Characterizing an indirect or several-steps-removedeffectDistichlis spicata A perennial marsh grass widespread through-out the AmericasDynamic equilibrium The condition under which differentcomponents of the system although often changing contin-ually reach a balance in which system inputs are roughlyequal to outputs

Ecogeomorphic Pertaining to interactions between ecology andgeomorphologyEddy A vortex or circular motion of waterEmergent vegetation Vegetation that fully protrudes throughthe water columnEntrainment sediment The suspension of particles by flowingwaterEstuarine gradient The continuum of salinities and associatedlandscape features along the mixing zone between the coastalocean and freshwater riversEvapotranspiration The combination of evaporation and tran-spiration that converts water from a liquid to a vapor andreleases it to the atmosphereFeedback The process of a systemrsquos output affecting an inputFeedback positive A signal amplification process whereby theoutput signal intensifies the input signalFeedback negative A signal-damping process whereby the out-put signal diminishes the input signalFermentation The metabolic processes conducted by microbeswhereby organic carbon compounds are used as both electrondonor and acceptor in low-oxygen conditions to yield energyFetch A length of water over which wind blowsFlocculation The aggregation of particles suspended in waterFlocs Compound particlesaggregates that form through theprocess of flocculationGlycine betaine A nitrogen-rich compound used by salt-toler-ant plantsGroundwater discharge The flow of groundwater into surfacewaterHalophytes Plants that thrive under highly saline conditionsHydraulic head The total pressure caused by water above agiven point in an aquifer which results from a combination ofthe water tablersquos elevation velocity and confining pressure ofthe aquiferHypoxia Oxygen depletion to a level that is between 1 and30 saturationImpatiens capensis Also known as jewelweed an annual plantnative to North AmericaJuncus gerardi A tidal marsh plant species common in north-ern North America and GreenlandLabile Readily undergoing change through uptake or decom-positionLeaf area index The total upper leaf surface of vegetationdivided by the surface area of the land occupied by the vege-tationMacrophytes Aquatic plantsMethanogenesis The production of methane gas (CH4) byarchaea that ferment simple organic carbon compounds oroxidize H2 under anaerobic conditions with co-production ofCO2Nitrification The energy-yielding microbially mediated oxida-tion of ammonium (NH4

+) to nitrite (NO2ndash) and subsequently

nitrate (NO3ndash)

Nitrifiers Organisms that perform nitrification


83

Nitrogen fixation The microbially mediated conversion ofgaseous N2 into ammonium (NH4

+) a ldquofixedrdquo or bioavailableform of nitrogenOsmotic regulation Maintenance of an optimal osmotic pres-sure (the pressure on cell membranes exerted by solvent mol-ecules) within an organismOxidation The loss of an electron by an atom molecule or ionPerennials Plants that persist in the environment for morethan 1 yearPhotosynthesis The generation of carbohydrates from carbondioxide and water using radiant energyPhragmites australis Also known as the common reed a largeperennial grass found in wetlands throughout temperate andtropical regions of the worldPilea pumila Also known as Canadian clearweed an annualplant found in the Eastern and Gulf Coast portions of NorthAmericaPorewater Shallow subsurface water found within the pores ofsedimentProline A nitrogen-rich amino acid used by salt-tolerantplantsProximal Characterizing an immediate direct effectRecharge The flow of surface water into the aquiferRedox A descriptor of chemical reactions in which the oxida-tion state of participating atoms or molecules changesReductase The catalyst of a reduction reactionReduction The gain of an electron by an atom molecule or ionRespiration The set of metabolic processes through whichorganisms obtain energyRhizosphere The zone of soil containing and surroundingplant rootsSaltwater intrusion The movement of saline water into fresh-water aquifersSarcocornia A genus of succulent salt-tolerant coastal plantsthat is widely distributed throughout North AmericaSeepage face A location along a slope where water from anaquifer emerges at atmospheric pressureSpartina alterniflora Also known as saltmarsh cordgrass aperennial deciduous grass found in salt marshes and native toNorth AmericaSpartina maritima A tidal marsh plant species found along theGulf Coast of North AmericaSpartina patens Also known as saltmeadow cordgrass a peren-nial grass native to the Atlantic coast of North America that isfound in the upper portions of brackish marshesStomatal conductance A measure of the rate of passage of watervapor andor carbon dioxide through the pores in plant tissueStressor Any agent that causes stress to an organismSuaeda A genus of salt-tolerant coastal plants that is widelydistributed throughout North America and can often toleratealkaline soilsSurfacesubsurface exchange The bidirectional flow of waterbetween the surface and below-ground aquifers and porewaterSynergistic Pertaining to the situation whereby the total effect

of multiple factors is greater than the sum of individualeffectsTidal wedge An intrusion of seawater into a tidal estuary in theform of a vertical wedge in which lighter freshwater from ariver rests atop dense saltwaterTransgression The upslope movement of tidal marsh vegetationTranspiration The emission of water vapor from the leaves ofplantsTurbulence intensity A mathematical measure of the level ofturbulence or unstable flow within a parcel of waterTurbulent wakes The pattern of turbulence or unstable flow inthe lee of an object that protrudes into the flowZonation The distribution of plants in biogeographic zones

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the advancing sea (Fitzgerald et al 2008) Furthermore theseecosystems are currently subjected to more immediate alter-ations such as increased N loading due to agriculture or urban-ization Water quality issues due to N loading affect both thestructural and functional value to humans of coastal wetlandecosystems Thus our objective is to lay a foundation for betterunderstanding of the interactions of multiple anthropogenicdrivers (SLR and N loading) on wetland ecosystem functions(eg N cycling) We argue that to understand the complexnonlinear effects of global changes such as SLR and N loadingscientists need to take a multifaceted approach that considershydrologic microbial and plant community interactions

Climate change most directly impacts tidal marshesthrough SLR Human activities have accelerated SLR throughan increase in the thermal expansion of the oceans fromhigher global air temperatures (Wigley 2005) Although ther-mal expansion is the leading cause of SLR increased meltingof continental ice sheets has also contributed (Shepherd andWingham 2007) Based on International Panel on ClimateChange (IPCC) temperature projections (IPCC 2007) currentmodels project a 75- to 190-cm range in SLR for the periodfrom 1990 to 2100 (Vermeer and Rahmstorf 2009) One of themost publicly visible implications is the predicted submer-gence of coastal areas eg the Mississippi Delta (Blum andRoberts 2009) Although the degree of coastal inundation dueto SLR will depend on many factors it is clear that SLR hasmany potential negative effects including (1) increasing ero-sion (2) enhancing storm surges (3) changing surface andgroundwater quality and (4) losing ecosystem services associ-ated with these vulnerable wetlands

N loading is changing along with sea level Human activi-ties have substantially and directly altered the N cycle byeffectively doubling the amount of reactive N in the environ-ment (Vitousek et al 1997 Galloway et al 2008) The impactsof N loading are particularly problematic in coastal zoneswhere nitrate (NO3

ndash) has been found to stimulate harmfulalgal blooms formation of anoxic zones and a loss of bioticlife Increasing N availability stimulates biomass productionsubsequent decomposition by oxygen-consuming microbes inturn creates low O2 zones called ldquodead zonesrdquo More than 400dead zones have recently been documented along coastsworldwide particularly in areas of high human populationdensity (Diaz and Rosenberg 2008) Wetland microbial andplant communities actively use and transform NO3

ndash poten-tially mitigating the effects of N loading to downstreamecosystems Despite increased loading via anthropogenicsources N remains the limiting nutrient in many coastal wet-lands and thus N loading impacts the productivity and com-position of wetland plant communities as they face SLRs

Given the importance of tidal marshes for coastal waterquality and coastal ecology it is imperative that the dualthreat of SLR and N loading on marsh ecosystem services berigorously evaluated so that management strategies can beadjusted to minimize adverse impacts We argue that these

potential impacts can be fully understood only through aholistic complex-systems approach that accounts for the feed-backs and interactions that occur across multiple levels oforganization in tidal marshes (eg microbes plants hydrol-ogy) As we will show these feedbacks will either exacerbate(eg positive feedbacks) or ameliorate (eg negative feed-backs) the ultimate impact of SLR on N cycling A complex-systems approach equips us to address several challengingrealities (1) that these perturbations operate on different tem-poral and spatial scales with SLR occurring more slowly andover longer time scales in many cases than N loading and (2)that N cycling is mediated across multiple levels of organiza-tion by combinations of microbial plant and landscapeprocesses Although we focus on SLR and N loading our com-plex-systems approach is relevant to numerous simultaneouschanges facing wetlands including altered hydrology (Port-noy 1999) and sedimentation increased CO2 and shifts inspecies composition due to invasive species (Levin et al 2006)

In this synthesis we first review the literature on biotic andabiotic controls on N cycling in tidal marshes and discuss theproximal effects of SLR and N loading on each of these con-trols Then we present a new conceptual model of how SLR islikely to affect interactions and feedbacks between drivers of Ncycling and the marshrsquos overall capacity to remove reactive Nfrom efflux to coastal systems Finally in summarizing howinteractions across ecosystem components are important forpredicting responses of fresh and marine wetlands to SLR andN loading we will offer future directions for research that canbetter embrace the complexity and multiple-scale dynamics ofthese valuable but vulnerable ecosystems

1B Overview of coastal marsh landscapes Hydrology geomor-phology and biologymdashTidal marshes are found in coastal loca-tions throughout the world where different combinations oftemperature underlying geology geomorphology of thecoastline and large-scale distribution of particular plantspecies present challenges for generalization However it iswidely recognized that these diverse marshes each feature dis-crete functional units that are dominated by a distinct set ofprocesses that are globally consistent (Fig 1) We do notattempt to generalize to the species level in this article butinstead focus on N cycling processes occurring within thesefunctional units further described below

Tidal marshes occupy a gradient of elevations along the estu-arine wedge which is also characterized by a gradient in localwater depth salinity and other seawater constituents such assulfate (SO4

2ndash) Tidal salt marshes occupy lowest elevations alongthat gradient and are colonized by a low-diversity but highlyproductive assemblage of salt-tolerant macrophytes such asSpartina alterniflora Higher-elevation salt marshes are less pro-ductive and are often more diverse but may be dominated bySpartina patens or Distichlis spicata In general as elevationsincrease landward and salinities decrease macrophyte diversitytends to increase while productivity declines (Tiner and Burke1995 Donnelly and Bertness 2001 Fitzgerald et al 2006 Fitzger-


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Eco-DAS VIII Symposium Proceedings · In salt marsh interiors, where nitrate reduction rates are...

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