salt marshes as potential indicators of global climate change

Salt Marshes as Potential Indicators of Global ClimateChange

Daehyun Kim1*, Jesper Bartholdy2, Soohyun Jung1 and David M. Cairns3

1Department of Geography, University of Kentucky2Department of Geography and Geology, University of Copenhagen3Department of Geography, Texas A&M University

Abstract

Coastal scientists postulate that salt marshes are significantly affected by dynamics of global climate.However, few studies have explicitly proposed a perspective that regards salt marshes as potentialindicators of climate change. This review article evaluates the possibility of salt marshes as indica-tors of global climate change, focusing upon three major aspects: sedimentary, vegetation, and bio-geochemical dynamics. The previous literature concerned with these aspects commonly arguesthat the primary impact of climate change on salt marshes occurs via sea-level variations, becausehydrologic fluctuations regulate the frequency, duration, and depth of over-marsh flooding events.Sedimentary, floristic, and biogeochemical dynamics prove to be significantly influenced by sea-level changes regardless of climate zones, and hence, undoubtedly possess a potential for indicatingclimate signatures. However, where plant-plant interactions such as facilitation and competitionare important, vegetation dynamics in salt marshes may not be an immediate, sole function of sea-level and climate variations. Also, specifically in the field of salt marsh biogeochemistry, enoughlong-term data have not been collected to convincingly conclude that biogeochemistry is a usefulindicator of climate change. Therefore, while this review is concerned mainly with the possibilityof salt marshes as indicators of climate change, their suitability or usefulness is a different matter tobe resolved through further data collection and discussion in future investigations.

Introduction

Salt marshes are significantly influenced by dynamics of global climate in a number ofways. Most importantly in recent years, temperature variability has resulted in eustaticsea-level fluctuations associated with volume changes in the ocean water (e.g. melting ofthe polar ice). Such hydrographical variations, in turn, control the frequency, magnitude,and duration of marsh submergence, thereby affecting the rate of sediment accumulation(e.g. Reed 1995; Stevenson et al. 1986), productivity ⁄ composition of plant species(Bakker et al. 1993; Morris et al. 2002; Pennings et al. 2005), and biogeochemical pro-cesses (Craft et al. 2009; Guo et al. 2009; Kathilankal et al. 2008). In accordance with therecent (controversial) concern about global warming related to human-induced increaseof atmospheric CO2, most of our emphasis has been placed upon how the speed of grad-ual sea-level rise would determine dynamics, and eventually, survival ⁄disappearance ofmarshes (Hartig et al. 2002; Kirwan and Murray 2007; Simas et al. 2001).

While salt marsh scientists postulate the effect of global climatic change on salt marshdynamics, there are few attempts to evaluate if salt marshes can potentially serve as indica-tors of that change. Climatic variations themselves involve fluctuating signals that arevery difficult to read and interpret. Therefore, it has long been a critical task to identify

Geography Compass 5/5 (2011): 219–236, 10.1111/j.1749-8198.2011.00421.x

ª 2011 The AuthorsGeography Compass ª 2011 Blackwell Publishing Ltd

indicators that can provide a more complete but still simple picture of global climaticdynamics (Kupfer and Cairns 1996). Environmental scientists have proposed to use severalindicators including greenhouse gases, tropical cyclone intensity, ocean acidity, glaciers,and bird wintering ranges (US Environmental Protection Agency 2010). However, it isstill unclear how much these variables vary temporally and spatially as a result of climatechange alone. Likewise, despite the great advance in the study of salt marsh dynamics,little research has explicitly assessed how such dynamics represent actual responses toclimatic variations.

In this paper, we address the possibility of salt marshes as indicators of global climatechange, focusing upon three major aspects of dynamics: sedimentation, vegetation, andbiogeochemistry. For each aspect, we first review the literature concerning impacts of cli-mate change and then discuss how abiotic and biotic dynamics of salt marshes can shedlight on global climatic variation. There may be direct influences of climate change onsalt marshes. For example, temperature and humidity may control carbon (energy) bal-ance associated with photosynthetic capabilities of plants (Cairns and Malanson 1998; Hallet al. 1992; Stevens and Fox 1991). However, we consider that the regime of sea waterinundation is an overwhelming factor of salt marsh dynamics, and hence, we payattention primarily to the indirect impact of climate change on salt marshes via sea-levelvariation. Last, for vegetation and biogeochemical dynamics, we constrain this review toa multi-decadal timescale. For sedimentary dynamics, we also examine the late Quater-nary because salt marsh profiles often retain climate-related sedimentary signatures forthousands of years.

Sedimentary Dynamics

Salt marshes consist of frequently flooded vegetated areas located between coastal hinter-lands and daily (or permanently) flooded coastal areas. As such, they represent a bufferzone between land and sea that is strongly dependent on a delicate balance between ter-restrial, littoral, hydrographic, and oceanographic parameters. As these are ultimately con-trolled by climate, salt marshes may be excellent indicators of climate change especiallybecause only slightly changed conditions in that balance could have large impacts on theirdevelopment. Even if sea level is rising, salt marsh areas can still exist and build up sincedeposition is part of their raison d’etre.

Over time, salt marsh deposits build up an archive of sediment that can be interpretedin terms of variations in the depositional environment and thus proxies for climatechange. In this context, salt marsh areas benefit from comprising large coherent areasgoverned by similar sedimentary conditions. In general, a salt marsh can be separated intothree main types of sedimentary environment: (1) environments associated with channelflow in the vicinity of salt marsh creeks (e.g. Bartholdy 1997; Bayliss-Smith et al. 1979;Boon 1975; Dankers et al. 1984; French and Stoddart 1992; Green et al. 1986; Healeyet al. 1981; Nixon 1980; Reed et al. 1999; Settlemyre and Gardner 1977), (2) environ-ments associated with sheet flow over vegetated salt marsh surfaces (e.g. Bartholdy et al.2004, 2010b; Carling 1982; French and Spencer 1993; Letzsch and Frey 1980; Reed1988; Stoddart et al. 1989), and (3) environments associated with exposed salt marshedges (e.g. Bartholdy and Aagaard 2001; Davidson-Arnott et al. 2002; Jakobsen 1954;Pedersen and Bartholdy 2007; van Proosdij et al. 2006). See Allen (2000a) for a compre-hensive overview of salt marsh morphodynamics. If changes in a salt marsh sediment coreare to be interpreted and analyzed for climate proxies, only cores from type (2), that alsocovers the major part of a salt marsh area, are of primary interest. In the other two

220 Salt marshes and climate change

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sedimentary environments, local changes such as channel migration, erosion, and accre-tion need to be eliminated before general statements about overall changes can be madefrom a sediment core.

The primary use of salt marshes as indicators of climate change is related to sea-levelchange. The first to publish on relations between salt marsh and tidal levels were Mudge(1858) and Shaler (1886). Both researchers recognized the interplay between plants andsalt marsh forming processes, and related peat formation to vertical zones relative to sealevel in New England salt marshes on the northeast coast of the USA. Several subsequentstudies have demonstrated that salt marsh formation starts in a zone around mean highwater level, a statement which seems to be valid regardless of climate zones (e.g. Colde-wey and Erchinger 1992; Edwards and Frey 1977; Jakobsen 1954; Letzsch and Frey1980; Nielsen 1969).

Salt marsh growth depends on several factors (Figure 1). The primary reasons forsalt marsh growth are net accumulation due to sediment supply and internally derivedplant detritus. The change in elevation is also affected by autocompaction. This is ageneric term for the physical, biological, and chemical processes leading to a shrinkingvolume of deposits on the account of age and weight. In order to keep track withthe absolute level, it is also necessary to include possible isostatic movements, and, ifthe level is to be evaluated in relation to the relative sea level, eustatic changes alsoneed to be considered.

If enough groundwater is available in an area exposed for salt marsh sedimentation, arising sea level will normally initiate the formation of peat in the innermost poorlydrained areas. This is the so-called basal peat which, under a rising sea level, will be over-lain by salt marsh clay when the peat becomes flooded by tidal action. Fluctuations in therising sea level will create depositional pauses during sea-level fall, and renew peat forma-tion at the start of a subsequent sea-level rise.

We present an example of this evolution identified in the Danish Wadden Sea(Figure 2). The base of the profile in this area is the Pleistocene sand on which the Holo-cene sediments are deposited as a result of the post-glacial sea-level rise. The surface sandat the start of the profile is most likely derived from recent local soil erosion. The centraland outer parts of the profile show a typical transgressive sequence with peat below claydeposits overlaying the local substrate (this is not reached by the soil auger at the end ofthe profile). When the post-glacial sea-level rise reached about )4.0 m DNN (DanishOrdnance Datum) about 4000 years ago, peat formation started and continued to build

Fig. 1. Schematic model of factors influencing the growth of salt marshes. ‘E’ indicates a salt marsh surface locatedabove an incompressible base of consolidated sands. Adapted from Bartholdy (forthcoming).

Salt marshes and climate change 221


up during the following 2000 years. The sea level reached a maximum of about)1.0 m DNN in the first century AD, and the whole area represented by the profilewas flooded and covered by mudflats under deposition of marine clay followed by saltmarsh deposits. After this sea-level summit, a minor sea-level fall caused peat to spreadout over the fine-grained sediment surface in the subsequent sea-level rise, before thewhole area again was flooded and eventually turned into a salt marsh, representing thepresent-day situation.

In areas with limited hinterland supply of fresh groundwater, salt marsh sedimentationwill start directly on the substrate with no previous formation of peat. This is typical forbackbarrier salt marshes like the one described below from the Skallingen Peninsula inDenmark.

The dated profiles identified from the Danish Wadden Sea (Figure 2) can be used toreconstruct the underlying sea-level curve by means of the age of peat samples from sedi-ment cores (14C) which can be related to sea levels of the same age. This is an exercisewhere the basal peat is of special interest (e.g. Behre 2004; Redfield and Rubin 1962;Streif 2004; Vandeplassche 1982), as it can be directly compared to levels where themodern basal peat forms, and because, as a result of its direct contact with the substrate,it is free of autocompaction which distorts the levels of peat at higher locations in theformation (e.g. Allen 2000b). The precision of such an analysis can be increased by usingthe so-called ‘sea-level index points’. These are points on the actual salt marsh surface ofa known level and characterized by their content of diatoms (i.e. the presence and num-ber of different species). In a sediment core, the diatom content can be referred to suchindex points, assuming that identical diatom content means identical sea-level relations(e.g. Gehrels et al. 2006; Shennan et al. 1995; Woodroffe and Long 2010).

The analysis of salt marsh formations in terms of age and climate also benefit fromarcheological findings (e.g. Gonzalez et al. 2000; Lespez et al. 2010; Mellalieu et al. 2000),indicators of environmental change like pollen composition (e.g. Goman et al. 2008;Gonzalez and Dupont 2009; Long et al. 1999; Ward et al. 2008), and the C ⁄N-ratio

Fig. 2. Stratigraphic profile based on corings in a line at Kjelst in the Danish Wadden Sea. The profile starts at aPleistocene northern rim and extends about 400 m towards the bay Ho Bugt. The four 14C-datings represent topand bottom of the two peat horizons. The vertical lines indicate the locations of corings based on which the profilewas constructed. Adapted from Bartholdy (forthcoming).



which has the potential to provide information as to the origin of organic materialpreserved in coastal environments (see review by Lamp et al. 2006).

Exposed salt marsh areas can develop horizontal lamination with interlayered sand ⁄mudbeddings similar to the classical example described by Reineck and Singh (1975). It con-tains sandy deposits related to deposition during periods of relative high water levels andvigorous current ⁄ wave action primarily associated with wind setup during storms, alter-nating with mud deposits also related to rough weather conditions but deposited aroundhigh water slack and subsequent calmer conditions. In environments with relatively littlemud and potentially high organic production, such beddings can consist of layers of sandalternating with layers of organic fibrous material. This type of bedding was described byRedfield (1972) as a kind of varve in salt marshes of New England, USA. In other mud-dier salt marsh areas, varved sedimentation has been revealed by means of X-ray photos.This was done by Shi (1993) in the Dyfi Estuary, UK and by Bartholdy et al. (2010a) ina study of high resolution deposition on the backbarrier salt marsh of Skallingen,Denmark. In the former work, a direct relationship between seasons enabled Shi (1993)to count yearly layers of alternating finer and coarser material in the salt marsh clay, whilein the latter less regular dark bands were found to be associated with relatively longperiods of low sediment deposition.

As accretion on the Skallingen salt marsh correlates well with the North AtlanticOscillation Index (NAO; a measure of the mean atmospheric pressure difference betweenIceland and Portugal; Bartholdy et al. 2004), detailed studies of dated sediment cores willhave direct potential for revealing past climate variations. This was on a somewhat largerscale done by Gonzalez and Dupont (2009) who, from cored tropical salt marsh deposits,were able to correlate variations in sedimentation and plant communities coinciding withAntarctic climate variations. Studies like these are heavily dependent on our ability to datesalt marsh materials, a task which will benefit from modern optically stimulated lumines-cence-dating techniques in the future (e.g. Madsen and Murray 2009; Madsen et al. 2007).

The future development of salt marshes has been assessed by means of accretion modelscalibrated on the basis of observed accretions in relation to tide gauge data (e.g. Allen1990; Bartholdy et al. 2004, 2010b; French 2006; Kirwan and Temmerman 2009;Temmerman et al. 2003). To some extent, the future response of salt marsh areas to sea-level rise represents the ultimate forecast scenario of salt marshes as indicators of globalclimate change. An example of an assessment of salt marsh stability in the Wadden Seaduring different sea-level rise scenarios is based on one of these models (Bartholdy et al.2010b; see Figure 3). The model is based on calibrated algorithms describing sedimenta-tion on the salt marsh as a result of variations in sediment concentrations and inundationheights driven by high water levels. It was calibrated on the basis of tide gauge informa-tion from a close by harbor (Esbjerg) and measured deposition along three transects acrossthe salt marsh in the period 1949 and 2007.

The starting point of this model (i.e. Figure 3) is after about 100 years of simulateddeposition on the top on a bare sand flat. Simulated levels are plotted as the differencebetween modeled salt marsh level and the rising highest astronomical tide (HAT). Thissalt marsh is affected by wind-tide, which means that a number of high tides every yearreach a level above HAT, and that the salt marsh therefore can reach levels above this.When the difference between salt marsh level and HAT becomes less than 0.5 m (corre-sponding to the actual salt marsh initiation level of 0.8 m DNN with a present HAT of1.3 m DNN), the salt marsh is assumed to degrade back to an unvegetated tidal flat.There might be a hysteresis effect keeping already established salt marshes ‘alive’ belowthis level, but to what extent this is the case is unknown. With a sea-level rise of



5.0 mm ⁄year, the marsh would ‘mature’ to a constant level in the rising tidal frame about1000 years after salt marsh initiation. It is interesting that the marsh reaches stability at alevel equal to HAT (salt marsh level ) HAT = 0). For any other sea-level rise scenarios,the salt marsh would be in disequilibrium, either in a state of downing or growingtowards the top of the tidal frame. A sea-level rise of less than 3.0 mm ⁄year would notthreaten the salt marsh in question within the next 200 years. With increasingly bettermodels, this type of assessment will hopefully enable decision-makers to make sensiblemanagement decisions for vulnerable ecosystems consisting of salt marshes during theexpected accelerating eustatic sea-level rise.

Vegetation Dynamics

Plant species that thrive in salt marshes are constantly faced with major environmentalstress factors such as the periodic submergence by tidal sea water, soil salinity, and limitednutrient availability (Adam 1990; Chapman 1960; Ranwell 1972). Importantly, the main-stream literature suggests that recent sea-level variations driven by global climate changeare overwhelming, primary determinants of all these factors in the salt marsh ecosystem(Kirwan and Murray 2007; Morris et al. 2002; Simas et al. 2001). The presence of onesuch central driving force leads to an insight that salt marsh vegetation may be a potentialindicator of sea-level variations, and eventually, climate change.

In other words, if salt marsh vegetation is significantly influenced by a number ofdifferent factors, some of which are not necessarily related to long-term climate variability,it would not be an appropriate indicator of climate change. In montane environments, forexample, Kupfer and Cairns (1996) suggest that using ecotone locations as indicators ofvegetation to climate change would have limited applicability. This is because the spatialpattern of montane plants is mainly affected by non-climatic vectors such as disturbance(e.g. landslide), soil texture ⁄ depth, and high-velocity winds (i.e. meteorological condition).

Fig. 3. Simulated differences between highest astronomical tide (HAT) and modeled salt marsh level under differentsea-level rise scenarios at the central part of the Skallingen salt marsh in the Danish Wadden Sea. The simulationstarts at present, about 100 years after salt marsh initiation. After Bartholdy et al. (2010b).



Due to these significant complex factors, the response of vegetation (i.e. vertical move-ment of ecotones) would not be observed as an immediate, linear function of climatechange.

It is suggested that differential rates of marsh surface accretion and gradual mean sea-level rise over decades will control the overall behavior and fate of salt marshes (Reed1995; Stevenson et al. 1986). For instance, Morris et al. (2002) proposed that there is anoptimal rate of relative sea-level rise in any salt marsh. Under such a condition, a positivefeedback, by which biomass productivity of plants and sedimentation enhance each other,would be optimized (Bertness et al. 1992; van de Koppel et al. 2005). Through such veg-etation and sedimentary dynamics, salt marshes constantly readjust their surface toward anequilibrium with rising sea level (see also Kirwan and Murray 2007; Redfield 1972).Therefore, a breakup of this equilibrium state and the resultant changes in the productiv-ity may indicate anomalies in the sea-level variation associated with climate change.For example, when the rate of sea-level rise significantly exceeds that of sediment accu-mulation, there would be a gradual decrease in the relative surface elevation, and con-sequently, increased frequency of tidal inundation.

This kind of scenario has often been reported in the field through theoretical modeling(e.g. Bartholdy et al. 2004; Kirwan and Murray 2007; Simas et al. 2001). Such a hydro-logical change would reduce biomass productivity of marsh plants because, in order tocope with a new, unfavorable environmental condition, they would invest a large amountof internal resources to their physiological counter-strategies (see Adam 1990, 286) at theexpense of growth. In short, biomass productivity dynamics of plants in salt marshes seemto be potential indicators of sea-level and climatic variations.

The positive feedback between vegetation cover and sediment accretion under an opti-mal rate of eustatic sea-level rise also leads to changes in plant species composition overtime. For instance, field data acquired from the Skallingen salt marsh in Denmark indicatethat the marsh experienced progressive vegetation succession between 1933 and 1949(Figure 4A and B; Kim et al. 2011). In the meantime, the gradual mean sea-level riseresulted in an increased rate of sedimentation, and thus, there were equilibrated increasesin both marsh and sea surfaces (approximately 2.5–3.0 mm ⁄year; Figure 5).

Kim et al. (2011) performed hierarchical cluster analysis on the floristic data and identi-fied four major vegetation associations across the Skallingen marsh (Figure 6). The firstgroup (A) was dominated by pioneer species such as Puccinellia maritima, Salicornia herbacea,and Suaeda maritima that have high tolerance to physical stresses imposed by saline water.The second association (B) represented an early- to mid-successional stage with decreasedfrequency of the pioneer species and increased cover of Limonium vulgare and Plantagomaritima. The third (C) and fourth (D) groups indicated mid- and late-sere phases, respec-tively. In 1933, there was dominance by pioneer groups (17 samples out of 29; Fig-ure 4A), implying that the marsh was still young and low-lying in the early twentiethcentury. In 1949, there was a dramatic decrease of the pioneer group (from 17 samples to6; Figure 4B) and an increase of the early- to mid-successional association (12 samplesout of 29) that had primarily developed from the early-sere phase through progressivesuccession. Both the long-term progressive succession and the surface accretion at Skallin-gen indicate that the rate of sea-level rise between 1933 and 1949 (Figure 5) was moreor less optimal for the existence and maturation of the marsh studied. This conclusionimplies that eustatic sea-level rise had not seriously influenced coastal areas around theEuropean Wadden Sea in the early twentieth century.

This section so far has been concerned primarily with gradual, eustatic sea-levelvariations driven by gradual climate change. Compared to this long-time perspective,



however, there is not much appreciation that short-term fluctuations of the sea surfacenested within the long-term, gradual trend can affect the biology and ecology of saltmarsh vegetation (but see Kim et al. 2011; Morris 2000; Olff et al. 1988). Such tempo-rary sea-level fluctuations are associated with recent variations in atmospheric oscillationindices and storminess on the ocean surface that in turn change the regime of tide, water-logging, and ecological succession. This new insight has been proposed from recentinvestigations in Europe.

In the Wadden Sea, the contemporary dominance of Halimione portulacoides at some saltmarshes (e.g. Figure 4C in Kim et al. 2011) has conventionally been ascribed to the rapideustatic mean sea-level rise in recent years (Leendertse et al. 1997). The previous logic isthat the recent sea-level rise has augmented the frequency of over-marsh flooding onmarsh platforms, thereby retarding progressive succession toward later-successional phasesthan the Halimione-dominated stage. Until the late twentieth century, this theory couldbe well accepted presumably due to a world-wide concern about the threat of globalwarming, melting of polar ice, and the consequent eustatic sea-level rise (Hegerl andBindoff 2005).

However, Kim et al. (2011) suggested an alternative explanation concerning the domi-nance by Halimione at a Danish backbarrier salt marsh at Skallingen sheltered from direct

Fig. 4. Spatial and temporal dynamics of salt marsh vegetation at Skallingen, Denmark (adopted from Kim et al.2011). Groups A, B, C, and D represent early-, early- to mid-, mid-, and late-successional vegetation associationsidentified by hierarchical cluster analysis. Group A was dominated by pioneer species such as Puccinellia maritima,Salicornia herbacea, and Suaeda maritima. Group B represented early- to mid-successional stage with decreasedfrequency of the pioneer species and increased cover of Limonium vulgare and Plantago maritima. Group C wasmid-sere and predominated by one primary species, Halimione portulacoides. Group D indicated a late-sere phase,dominated by Festuca rubra, Juncus gerardii, and Artemisia maritima. Aerial photo was taken in 1995.



impacts of storm surges. Kim et al. questioned the significance of eustatic sea-level rise tovegetation succession at the marsh, because of equilibrated dynamics between marsh andsea surfaces observed by Bartholdy et al. (2004) since the 1970s (see Figure 5). Kim et al.(2011) argued that the slightly higher rate of sea-level rise (5.0 mm ⁄year) than sedimenta-tion (4.0 mm ⁄year) cannot explain the significant increase in the frequency of high waterlevel events over the entire marsh (Table 1).

Their alternative hypothesis is that recent tendency of the NAO index toward a posi-tive phase have increased storminess and wind tides on the ocean surface, leading toincreased frequency, duration, and depth of sea water inundation, and hence, water-logging of marsh soils, which has retarded ecological succession. The index has beendominantly in a positive phase recently, especially since the 1980s (Osborn 2004; Paeth

Fig. 5. Temporal dynamics of mean sea level and marsh surface elevation at the Skallingen salt marsh, Denmark.The surface elevation has been measured at 5 ⁄ 31, one of the long-term monitoring locations in Bartholdy et al.(2004).



et al. 1999; Figure 7). This positive phase is the primary factor of frequent westerly galesand subsequent short-term wind tides on the North Sea (Deser et al. 2000; Serreze et al.1997).

Fig. 6. The four vegetation associations presented in Figure 3. In Group A, early-sere species are present at theinterface between marsh platform and tidal flat (i.e. bare ground). In Group B, Limonium vulgare is the purpleflower and represents an early- to mid-successional stage. Halimione portulacoides predominates Group C. The lastgroup is dominated by late-sere plants such as Festuca rubra (brown-colored individuals) and Artemisia maritima(white-colored). The photos were taken at the Skallingen salt marsh, Denmark, in 2006.

Table 1. Mean water levels (MWL) and the number of high water level (HWL) events aroundSkallingen in m DNN, the Danish Ordnance Datum (adapted from Kim et al. 2011).

Period (years) 1931–1946 1946–1961 1961–1976 1976–1991 1991–2006

MWL 0.086 0.119 0.116 0.157 0.2201.0–1.2 m HWL 703 826 860 963 11711.2–1.4 m HWL 317 405 467 485 6001.4–1.6 m HWL 193 185 195 289 2951.6–1.8 m HWL 104 103 102 168 1811.8–2.0 m HWL 32 57 58 74 792.0–2.2 m HWL 19 24 38 45 432.2–2.4 m HWL 10 8 17 28 21



We present aerial photos that illustrate dynamics of vegetation cover at a part of theSkallingen salt marsh in the second half of the twentieth century (Figure 8). The small,bright feature in the upper part of the photo in 1964 represents areas of sand ridges withhigh surface elevations (>130 cm DNN), where late-successional species such as Festucarubra, Artemisia maritima, and Juncus gerardii dominate. This feature became larger andelongated in 1980, indicating a process of progressive succession on the marsh platformdue to a continuous increase in the rate of sediment accretion (Bartholdy et al. 2004).However, since 1980, areas of the late-sere plants have decreased in size dramatically, andthese sites are now dominated by H. portulacoides. Such vegetation dynamics are inter-preted as representing retrogressive succession, influenced by the increased storminess onthe sea surface since the 1980s when the NAO entered its positive phase.

The example from Skallingen, Denmark implies that vegetation dynamics in saltmarshes may serve as a potential indicator of long-term patterns of wind-driven sea-levelchanges associated with the NAO variation over decades. Importantly, the significantlinkage between the atmospheric oscillation and sea-level variation is not confined to theSkallingen salt marsh: The variability in various oscillations such as the El Nino-SouthernOscillation and the Pacific Decadal Oscillation, as well as the NAO, is considered as acause of meteorological ⁄ climatic variations from local to global scales (e.g. Bromirski et al.2003). We propose that future investigations in coastal biogeography hold a multi-tempo-ral perspective that recognizes the importance of both long- and short-term fluctuationsof sea-level and climatic signatures.

Biogeochemical Dynamics

The interplay of sedimentation and over-marsh flooding regulates biogeochemicalfunctioning of marsh soils including eutrophication, (de)nitrification, carbon supply, andmicrobial activities (Simas and Ferreira 2007; Taillefert et al. 2007). As such, it is worth-while to evaluate biogeochemistries of salt marshes as indicators of sea-level and climaticchanges. In this section, we select carbon flux, primary production, eutrophication, anddenitrification as key topics of salt marsh biogeochemistry, and review the previous litera-ture associated with them.

As sea level rises due to climate warming, salt marshes may be inundated more frequentlyand longer than before (Titus 1991), except when the accretion of salt marsh by sedimenta-

Fig. 7. Yearly variation of the North Atlantic Oscillation (NAO) index (http://www.cgd.ucar.edu/cas/jhurrell/indi-ces.html). Smooth, thick line represents the 3-year running mean calculated from the original yearly NAO data. Thisaveraged description indicates that the NAO index has been predominantly under a positive phase since the 1980s.



tion is in equilibrium with sea-level rise (see also Morris et al. 2002). Such a change in thetidal regime would significantly affect the carbon flux between salt marsh soils and theatmosphere, because during submergence the carbon flux is known to be smaller than thatduring emersion. For example, Kathilankal et al. (2008) observed a decreased carbon fluxat the ecosystem level during tidal inundation, despite the continual carbon assimilation atthe species level (i.e. Spartina alterniflora). This finding was supported by Guo et al. (2009)who showed that soil respiration during night time under spring tides is much smaller thanthat under neap tides. Even in high marshes where tidal submergence does not occur often,it is expected that the loss of organic carbon via the reduction of soil respiration by futuresea-level rise would be possible (Miller et al. 2001). In short, a decline of carbon sequestra-tion in salt marsh vegetation and soils would indicate an elongated regime of tidal inunda-tion, which in turn implies sea-level rise due to potential climate warming processes.

Fig. 8. Selected aerial photographs of the study area taken in (A) 1964, (B) 1980, (C) 1995, and (D) 1999 (adaptedfrom Kim et al. 2011). There is a division into grazed (lower left side) and ungrazed (upper right side) parts. Thehorizontal length of each photo equals about 1.3 km in the real field.



Elongated tidal inundation also significantly impacts biomass productivity of salt marshvegetation. The increased tidal inundation regime results in reduced biomass productivityof salt marsh plants, which further decreases the rate of marsh surface accretion due toinsufficient accumulation of organic matter. These phenomena in turn lead to a feedbackmechanism by which a further decline of plant productivity occurs on salt marshes owingto the slow surface accretion (Nyman et al. 1993). In addition, reduced photosynthesis ofhalophytic plant species because of sea-level rise would decrease the primary productionat salt marsh platforms (DeLaune et al. 1983; Mendelssohn and McKee 1988), which wassupported by a modeling study of Simas et al. (2001) for both C3 or C4 types.

Simas et al. (2001) demonstrated that, in addition to the vegetation productivity, therate of denitrification (i.e. permanent removal of nitrate, NO3

), as a gaseous phase, N2Oor N2) would be reduced by sea-level rise. This is because increased tidal frequency andduration may lead to the change of redox potential toward its reduction stage in marshsediments, which is one of the controlling factors of the denitrification rate. For example,vertical denitrification zones in mud flat sediments during neap tides penetrate to 5.0 mmfrom the surface, whereas during spring tides they only penetrate to 3.0 mm (Koch et al.1992).

Sea-level rise also influences the degree of nitrogen removal from estuarine waters tosalt marsh platforms, thereby controlling the nutritional state of the outer marine ecosys-tem (e.g. eutrophication; Simas and Ferreira 2007). Loomis and Craft (2010) recentlyshowed that salt marsh sediments have a potential capacity to remove nitrogen which iscomparable to that of tidal fresh and brackish marshes. In this way, salt marshes are knownto serve as an important ecological buffer, reducing the amount of nitrogen flowing intothe ocean water. However, with increasing sea levels, the capacity of salt marsh vegetationto absorb nitrogen should decrease in conjunction with a reduction of marsh platforms inarea (Patrick and DeLaune 1976). Contrary to this role as an ecological buffer, it was alsoobserved that salt marshes can be a source of nutrients to the outer ocean. For instance,S. alterniflora releases nitrogen and phosphorus into the sea water through tidal action(DeLaune et al. 1981; Turner 1993), therefore as sea level rises, phosphorus release by thespecies would contribute to an increase of that nutrient in the nearby marine ecosystem.

Microbial community structure in salt marshes can also be a potential indicator ofsea-level rise, because biogeochemical processes such as denitrification and carbon fluxare mainly mediated by microorganisms. In experimentally manipulated microcosmswith a range of redox conditions from )200 mV to +400 mV, Seo and DeLaune(2010) observed that, under reduced redox conditions, the contribution of bacteria toorganic matter decomposition (i.e. CO2 production) becomes more important than thatof fungi. This further indicates that changes in the redox state by sea-level rise couldaffect the relative activity of microbial communities directly and that such changes maybe able to convert the community structure of microorganisms as well. For example,Ludemann et al. (2000) showed that microbial community structure is strongly corre-lated with the redox state in sediments. As such, an increase in the abundance of micro-organisms which mediate processes occurring under a reduced redox state may possiblyindicate sea-level rise.

Conclusions

Our review has been concerned with sedimentary, vegetation, and biogeochemicaldynamics associated with sea-level fluctuations, to evaluate salt marshes as potential indi-cators of global climate change. Each of these proves to be significantly influenced by



sea-level changes regardless of climate zone, and hence, undoubtedly possess a potentialfor indicating climate signatures.

However, there are some issues that should be taken into account before we accept saltmarshes as suitable indicators of sea-level, and eventually, climate changes. That is, whilemost studies strongly postulate that sea-level variations are the overwhelming, primaryfactor of salt marsh dynamics, some other mechanisms may potentially be important. Forinstance, plant–plant interactions such as facilitation and competition are major determi-nant of fine-scale spatial patterns of salt marsh vegetation (Bertness and Shumway 1993;Kim et al. 2009; van de Koppel et al. 2006). In the Skallingen salt marsh, Denmark,time-series floristic surveys every summer since 2006 indicate that the dominance by H.portulacoides has been unchanging in spite of significant yearly changes in the frequency ofover-marsh inundation events (D. Kim unpublished data). The dominance of H. portulaco-ides reflects that it is a competitive shrub species (see Jensen 1985), so once the speciesbegins to dominate a system, the situation can persist for several years regardless ofchanges in the regime of over-marsh inundation driven by global climate change. There-fore, one should recognize that, where biological interactions are significant, vegetationdynamics in salt marshes may not be an immediate, sole function of sea-level and climatechanges. Moreover, specifically in the field of salt marsh biogeochemistry, enough long-term data have not been collected for one to convincingly conclude the biogeochemistryas a useful indicator of climate change. To conclude, while this review is concernedmainly with the possibility of salt marshes as indicators of climate change, their suitabilityor usefulness is a different matter to be resolved through further data collection and discus-sions in future investigations.

Short Biographies

Daehyun Kim’s research focus is bio-geophysical complexity in which spatial and tempo-ral patterns of vegetation and soil are molded in dynamic, complex relationships withlandform, climate, and hydrology. His overarching goal is to develop both conceptual andsimulation models that articulate how complex systems interactions create biogeographicpatterns. He has pursued this goal through the use of geographic information systems thatallowed him to analyze and visualize dynamics of natural resources observed throughfield-based studies. Such analysis and visualization involved predictive vegetation ⁄ soilmapping, digital terrain modeling, and spatial ⁄ multivariate statistics. One of his ongoingresearch projects is the investigation of long-term dynamics of salt marsh vegetationresponding to changes in environmental conditions in collaboration with David Cairns atTexas A&M and Jesper Bartholdy at the University of Copenhagen. They are in an unu-sual situation to work with floristic, sedimentological, hydrological, and climatic dataacquired from a Danish salt marsh since the 1930s. In August 2009, Daehyun received hisPhD in geography from Texas A&M University and joined the UK Geography as Assis-tant Professor. He holds BA and MA from Seoul National University, South Korea.

Jesper Bartholdy is a physical geographer with focus on geomorphology and sedimenttransport. The main part of his research concentrates on modeling relationships betweendynamics and resulting deposition in fluvial as well as in estuarine systems. He hasworked in gravel bed as well as in sand bedded rivers and in estuarine systems in Europeand USA. Today his center of interest is divided into the study of formation and devel-opment of bedforms and in the morphodynamics and sedimentary development of saltmarsh areas. Jesper Bartholdy is Associate Professor at Department of Geography andGeology, University of Copenhagen, from where he also holds his MA and PhD.



Soohyun Jung has studied the spatial and temporal variation of microbial activities incoastal sediments and their interactions with environmental factors such as sea-levelchanges and vegetation. She earned her PhD in environmental science and engineeringfrom Ewha Womans University in South Korea. Her research goals are to identify (i) therole of coastal sediments in the nutrient cycling of marine ecosystems, threatened byhuman activities and climate change and (ii) to relate the nutrient cycling to the structureof microbial communities. To achieve these aims, she has analyzed microbial extracellularenzyme activities, microbial community structures, various organic and inorganic carbon,and nutrients. Now she is conducting a project on the microbial activity and microbialcommunity structure in salt marsh sediments in relation to plant species.

David M. Cairns is a Professor in the Department of Geography at Texas A&MUniversity. His research interests are in vegetation response to climate change, ecologicalmodeling, and the influence of herbivores on forest landscapes. He has a PhD from theUniversity of Iowa.

Note

* Correspondence address: Daehyun Kim, Department of Geography, University of Kentucky, Lexington, KY40506, USA. E-mail: [email protected].

References

Adam, P. (1990). Saltmarsh ecology. Cambridge, UK: Cambridge University Press.Allen, J. R. L. (1990). Salt-marsh growth and stratification: a numerical model with special reference to the Severn

Estuary, southwest Britain. Marine Geology 95, pp. 77–96.Allen, J. R. L. (2000a). Morphodynamics of Holocene salt marshes: a review sketch from the Atlantic and Southern

North Sea coasts of Europe. Quaternary Science Reviews 19, pp. 1155–1231.Allen, J. R. L. (2000b). Holocene coastal lowlands in NW Europe: autocompaction and the uncertain ground. In:

Pye, K. and Allen, J. R. L. (eds) Coastal and estuarine environments: sedimentology, geomorphology and geoarchaeology.London: Geological Society, Special Publications 175, pp. 239–252.

Bakker, J. P., et al. (1993). Salt marshes along the coast of the Netherlands. Hydrobiologia 265, pp. 73–95.Bartholdy, A. T., Bartholdy, J. and Kroon, A. (2010a). Salt marsh stability and patterns of sedimentation across a

backbarrier platform. Marine Geology 278, pp. 31–42.Bartholdy, J. (1997). The backbarrier sediments of the Skallingen Peninsula, Denmark. Geografisk Tidskrift. Danish

Journal of Geography 97, pp. 11–32.Bartholdy, J. (forthcoming). Salt marsh sedimentation. In: Davis, R. A. and Dalrymple, R. W. (eds) Principles of tidal

sedimentology. Berlin: Springer.Bartholdy, J. and Aagaard, T. (2001). Storm surge effects on a back-barrier tidal flat of the Danish Wadden Sea.

Geo-Marine Letters 20, pp. 133–141.Bartholdy, J., Christiansen, C. and Kunzendorf, H. (2004). Long term variations in backbarrier salt marsh deposition

on the Skallingen peninsula – the Danish Wadden Sea. Marine Geology 203, pp. 1–21.Bartholdy, J., Pedersen, J. B. T. and Bartholdy, A. T. (2010b). Autocompaction in shallow silty salt marsh clay. Sed-

imentary Geology 223, pp. 310–319.Bayliss-Smith, T. P., et al. (1979). Tidal flows in salt marsh creeks. Estuarine, Coastal and Marine Science 9, 235–255.Behre, K.-E. (2004). Coastal development, sea-level change and settlement history during the later Holocene in the

clay district of Lower Saxony (Nidersachsen), northern Germany. Quaternary International 112, pp. 37–53.Bertness, M. D., Gough, L. and Shumway, S. W. (1992). Salt tolerance and the distribution of fugitive salt marsh

plants. Ecology 73, pp. 1842–1851.Bertness, M. D. and Shumway, S. W. (1993). Competition and facilitation in marsh plants. American Naturalist 142,

pp. 718–724.Boon, J. D. (1975). Tidal discharge asymmetry in a salt marsh drainage system. Limnology and Oceanography 20,

pp. 71–80.Bromirski, P. D., Flick, R. E. and Cayan, D. R. (2003). Storminess variability along the California coast: 1858-

2000. Journal of Climate 16, pp. 982–993.Cairns, D. M. and Malanson, G. P. (1998). Environmental variables influencing the carbon balance at the alpine

treeline: a modeling approach. Journal of Vegetation Science 9, pp. 679–692.



Carling, P. A. (1982). Temporal and spatial variation in intertidal sedimentation rates. Sedimentology 29, pp. 17–23.Chapman, V. J. (1960). Salt marshes and salt deserts of the world. New York: Leonard Hill Ltd.Coldewey, H. G. and Erchinger, H. F. (1992). Diechvorland: Seine Entwicklung zwischen Ems und Jade und die

Untersuchungen in Forschungsvorhaben ‘Erosionsfestigkeit von Hellern’. Die Kuste 54, pp. 169–187.Craft, C., et al. (2009). Forecasting the effects of accelerated sea-level rise on tidal marsh ecosystem services.

Frontiers and Ecology and the Environment 7, pp. 73–78.Dankers, N., et al. (1984). Transportation of water, particulate and dissolved organic and inorganic matter

between a salt marsh and the Ems-Dollard Estuary, The Netherlands. Estuarine, Coastal and Shelf Science 19,pp. 143–165.

Davidson-Arnott, R. G. D, van Proosdij, D., Ollerhead, J. and Schostak, L. (2002). Hydrodynamics and sedimenta-tion in salt marshes: examples from a macrotidal marsh, Bay of Fundy. Geomorphology 48, pp. 209–231.

DeLaune, R. D., Reddy, C. N. and Patrick, Jr. W. H. (1981). Accumulation of plant nutrients and heavy metalsthrough sedimentation processes and accretion in a Louisiana salt marsh. Estuaries and Coasts 4, pp. 328–334.

DeLaune, R. D., et al. (1983). Relationship of marsh elevation, redox potential, and sulfide to Spartina alternifloraproductivity. Soil Science Society of America Proceedings pp. 47, 930–935.

Deser, C., Walsh, J. E. and Timlin, M. S. (2000). Arctic sea ice variability in the context of recent atmospheric cir-culation trends. Journal of Climate 13, pp. 617–633.

Edwards, J. M. and Frey, R. W. (1977). Substrate characteristics within a Holocene salt marsh, Sapolo Island, Geor-gia. Senckenbergianna Maritima 9, pp. 215–259.

French, J. (2006). Tidal marsh sedimentation and resilience to environmental change: exploratory modelling of tidal,sea-level and sediment supply forcing in predominantly allochthonous systems. Marine Geology 235, pp. 119–136.

French, J. and Spencer, T. (1993). Dynamics of sedimentation in a tide-dominated backbarrier salt marsh, Norfolk,UK. Marine Geology 110, pp. 315–331.

French, J. and Stoddart, D. R. (1992). Hydrodynamics of salt marsh creek systems: implications for marsh morpho-logical development and material exchange. Earth Surface Processes and Landforms 17, pp. 235–252.

Gehrels, W. R., et al. (2006). Late Holocene sea-level changes and isostasy in western Denmark. Quaternary Research66, pp. 288–302.

Goman, M., Malamud-Roam, F. and Ingram, B. L. (2008). Holocene environmental history and evolution of atidal salt marsh in San Francisco Bay, California. Journal of Coastal Research 24, pp. 1126–1137.

Gonzalez, C. and Dupont, L. M. (2009). Tropical salt marsh succession as sea-level indicator during Heinrichevents. Quaternary Science Reviews 26, pp. 939–946.

Gonzalez, S., et al. (2000). Holocene coastal change in the north of the Isle of Man: stratigraphy, palaeoenviron-ment and archaeological evidence. In: Pye, K. and Allen, J. R. L. (eds) Coastal and estuarine environments: sedimen-tology, geomorphology and geoarchaeology. London: Geological Society, Special Publications 175, pp. 343–363.

Green, H. M., Stoddart, D. R., Reed, D. R. and Bayliss-Smith, T. P. (1986). Saltmarsh tidal creekhydrodynamics,Scolt Head Island, Northfolk, England. In: Sigbjarnarson, G. (ed.) Iceland coastal and river symposium proceedings.Reykjavik, Iceland: National Energy Authority, pp. 93–103.

Guo, H., et al. (2009). Tidal effects on net ecosystem exchange of carbon in an estuarine wetland. Agricultural andForest Meteorology 149, pp. 1820–1828.

Hall, C. A. S., Stanford, J. A. and Hauer, F. R. (1992). The distribution and abundance of organisms as a conse-quence of energy balances along multiple environmental gradients. Oikos 65, pp. 377–390.

Hartig, E. K., et al. (2002). Anthropogenic and climate-change impacts on salt marshes of Jamaica Bay, New YorkCity. Wetlands 22, pp. 71–89.

Healey, R. G., Pye, K., Stoddart, D. R. and Bayliss-Smith, T. P. (1981). Velocioty variations in salt marsh creeks,Northfolk, England. Estuarine, Coastal and Shelf Science 13, pp. 535–545.

Hegerl, G. C. and Bindoff, N. L. (2005). Warming the world’s oceans. Science 309, pp. 254–255.Jakobsen, B. (1954). The tidal area in south-west Jutland and the process of salt marsh formation. Geografisk

Tidsskrift. Danish Journal of Geography 53, pp. 49–61.Jensen, A. (1985). On the ecophysiology of Halimione portulacoides. Plant Ecology 61, pp. 231–240.Kathilankal, J. C., et al. (2008). Tidal influences on carbon assimilation by a salt marsh. Environmental Research

Letters. 3:044010(6pp) pp. 1–6.Kim, D., Cairns, D. M. and Bartholdy, J. (2009). Scale-dependent interactions and community structure along

environmental gradients on a coastal salt marsh. Journal of Coastal Research SI 56, pp. 429–433.Kim, D., Cairns, D. M. and Bartholdy, J. (2011). Wind-driven sea-level variation influences dynamics of salt marsh

vegetation. Annals of the Association of American Geographers 101, pp. 231–248.Kirwan, M. L. and Murray, A. B. (2007). A coupled geomorphic and ecological model of tidal marsh evolution.

Proceedings of the National Academy of Science 104, pp. 6118–6122.Kirwan, M. L. and Temmerman, S. (2009). Coastal marsh response to historical and future sea-level acceleration.

Quaternary Science Reviews 28, pp. 1801–1808.Koch, M. S., Maltby, E., Oliver, G. A. and Bakker, S. A. (1992). Factors controlling denitrification rates of tidal

mudflats and fringing salt marshes in south-west England. Estuarine, Coastal and Shelf Science 34, pp. 471–485.



van de Koppel, J. D., van der Wal, J., Bakker, P. and Herman, P. M. J. (2005). Self-organization and vegetationcollapse in salt marsh ecosystems. American Naturalist 165, pp. E1–E12.

van de Koppel, J. D., et al. (2006). Scale-dependent interactions and community structure on cobble beaches. Ecol-ogy Letters 9, pp. 45–50.

Kupfer, J. A. and Cairns, D. M. (1996). The suitability of montane ecotones as indicators of global climatic change.Progress in Physical Geography 20, pp. 253–272.

Lamp, A. L., Wilson, G. P. and Leng, M. J. (2006). A review of coastal palaeoclimate and relative sea-level recon-structions using d13C and C ⁄ N ratios in organic material. Earth-Science Reviews 75, pp. 29–57.

Leendertse, P. C., Roozen, A. J. M. and Rozema, J. (1997). Long-term changes (1953-1990) in the salt marsh veg-etation at the Boschplaat on Terschelling in relation to sedimentation and flooding. Plant Ecology 132, pp. 49–58.

Lespez, L., et al. (2010). Middle to late Holocene landscape changes and geoarchaeological implications in themarshes of Dives estuary (NW France). Quaternary International 216, pp. 23–40.

Letzsch, W. S. and Frey, R. W. (1980). Deposition and erosion in a Holocene salt marsh, Sapelo Island, Georgia.Journal of Sedimentary Petrology 50, pp. 529–542.

Long, A. J., Scaife, R. G. and Edwards, R. J. (1999). Pine pollen in intertidal sediments from Poole Harbour, UK:implications for late-Holocene sediment accretion rates and sea-level rise. Quaternary International 55, pp. 3–16.

Loomis, M. J. and Craft, C. B. (2010). Carbon sequestration and nutrient (nitrogen, phosphorus) accumulation inriver-dominated tidal marshes, Georgia, USA. Soil Science Society of America Journal 74, 1028–1036.

Ludemann, H., Arth, I. and Liesack, W. (2000). Spatial changes in the bacterial community structure along a verti-cal oxygen gradient in flooded paddy soil cores. Applied and Environmental Microbiology 66, pp. 754–762.

Madsen, A. T. and Murray, A. S. (2009). Optically stimulated luminescence dating of young sediments: a review.Geomorphology 109, pp. 3–16.

Madsen, A. T., Murray, A. S., Andersen, T. J. and Pejrup, M. (2007). Temporal changes of accretion rates on anestuarine salt marsh during the late Holocene: reflections of local sea level changes? The Wadden Sea, Denmark.Marine Geology 242, pp. 221–233.

Mellalieu, S. J., et al. (2000). Holocene development of the east bank of the Gironde Estuary: geoarchaeologicalinvestigation of the Saint Ciers-sur-Gironde marsh. In: Pye, K. and Allen, J. R. L. (eds) Coastal and estuarineenvironments: sedimentology, geomorphology and geoarchaeology. London: Geological Society, Special Publications 175,pp. 317–341.

Mendelssohn, A. and McKee, K. L. (1988). Spartina alterniflora die-back in Louisiana: time-course investigation ofsoil waterlogging effects. Journal of Ecology 76, pp. 509–521.

Miller, W. D., Neubauer, S. C. and Anderson, I. C. (2001). Effects of sea level induced disturbances on high saltmarsh metabolism. Estuaries 24, pp. 357–367.

Morris, J. T. (2000). Effects of sea level anomalies on estuarine processes. In: Hobbie, J. (ed.) Estuarine science: a syn-thetic approach to research and practice. Washington, D.C, USA: Island Press, pp. 107–127.

Morris, J. T., et al. (2002). Responses of coastal wetlands to rising sea level. Ecology 83, pp. 2869–2877.Mudge, B. F. (1858). The salt marsh formation of Lynn. Essex Inst. Proc. II (1856–1860), pp. 117–119.Nielsen, N. (1969). Morphological studies on the eastern coast of Disko, West Greenland. Geografisk Tidsskrift.

Danish Journal of Geography 68, pp. 1–35.Nixon, S. W. (1980). Between coastal marshes and coastal waters – a review of 20 years of speculation and research

in the role of salt marshes in estuarine productivity and water chemistry. In: Hamilton, R. and McDonald,K. B. (eds) Estuarine and wetland processes. New York: Plenum, pp. 437–525.

Nyman, J. A., DeLanue, R. D., Roberts, H. H. and Patrick, Jr. W. H. (1993). Relationship between vegetationand soil formation in a rapidly submerging coastal marsh. Marine Ecology Progress Series 96, 269–279.

Olff, H., Bakker, J. P. and Fresco, L. F. M. (1988). The effect of fluctuations in tidal inundation frequency on asalt-marsh vegetation. Plant Ecology 78, pp. 13–19.

Osborn, T. J. (2004). Simulating the winter North Atlantic Oscillation: the roles of internal variability and green-house gas forcing. Climate Dynamics 22, pp. 605–623.

Paeth, H., et al. (1999). The North Atlantic Oscillation as an indicator for greenhouse gas-induced regional climatechange. Climate Dynamics 15, pp. 953–960.

Patrick, W. H. and DeLaune, R. D. (1976). Nitrogen and phosphorus utilization by Spartina alterniflora in a saltmarsh in Barataria Bay, Louisiana. Estuarine and Coastal Marine Science 4, pp. 59–64.

Pedersen, J. B. T. and Bartholdy, J. (2007). Exposed salt marsh morphodynamics: an example from the DanishWadden Sea. Geomorphology 90, pp. 115–125.

Pennings, S. C., Grant, M. B. and Bertness, M. D. (2005). Plant zonation in low-latitude salt marshes: disentanglingthe roles of flooding, salinity, and competition. Journal of Ecology 93, pp. 159–167.

van Proosdij, D., Davidson-Arnott, R. G. D. and Ollerhead, J. (2006). Controls on spatial patterns of sedimentdeposition across a macro-tidal salt marsh surface over single tidal cycles. Estuarine, Coastal and Shelf Science 69,pp. 64–86.

Ranwell, D. S. (1972). Ecology of salt marshes and sand dunes. London, UK: Chapman and Hall.Redfield, A. C. (1972). Development of a New England salt marsh. Ecological Monographs 42, pp. 201–237.



Redfield, A. C. and Rubin, M. (1962). Age of salt marsh peat in relation to recent changes in sea level. Science 136,p. 328.

Reed, D. J. (1988). Sediment dynamics and deposition in a retreating coastal salt marsh. Estuarine, Coastal and ShelfScience 26, pp. 67–79.

Reed, D. J. (1995). The response of coastal marshes to sea-level rise: survival or submergence? Earth Surface Processesand Landforms 20, pp. 39–48.

Reed, D. J., et al. (1999). Marsh surface sediment deposition and the role of tidal creeks: implications for createdand managed coastal marshes. Journal of Coastal Conservations 5, pp. 81–90.

Reineck, H.-E. and Singh, I. B. (1975). Depositional sedimentary environments. Berlin: Springer-Verlag.Seo, D. C. and DeLaune, R. D. (2010). Effect of redox conditions on bacterial and fungal biomass and carbon

dioxide production in Louisiana coastal swamp forest sediment. Science of the Total Environment 408, pp. 3623–3631.

Serreze, M. C., Carse, F., Barry, R. G. and Rogers, J. C. (1997). Icelandic low activity, climatological features,linkages with the NAO, and relationships with recent changes in the Northern Hemisphere circulation. Journal ofClimate 10, pp. 453–464.

Settlemyre, J. L. and Gardner, L. R. (1977). Suspended sediment flux through a salt marsh drainage basin. Estuarine,Marine and Coastal Science 5, pp. 653–663.

Shaler, N. S. (1886). Sea-coast swamps of the eastern United States. U.S. Geological Survey, 6th Annual Report,pp. 359–368.

Shennan, I., Innes, J. B., Long, A. J. and Zong, Y. (1995). Holocene relative sea-level changes and coastal vegeta-tion history at Kentra Moss, Argyll, northwest Scotland. Marine Geology 124, pp. 43–59.

Shi, Z. (1993). Recent saltmarsh accretion and sea level fluctuations in the Dyfi Estuary, central Cardigan Bay,Wales, UK. Geo-Marine Letters 13, pp. 182–188.

Simas, T. C. and Ferreira, J. G. (2007). Nutrient enrichment and the role of salt marshes in the Tagus estuary (Por-tugal). Estuarine, Coastal and Shelf Science 75, pp. 393–407.

Simas, T. C., Nunes, J. P. and Ferreira, J. G. (2001). Effects of global climate change on coastal salt marshes. Ecolog-ical Modelling 139, pp. 1–15.

Stevens, G. C. and Fox, J. F. (1991). The causes of treeline. Annual Review of Ecology and Systematics 22, pp. 177–191.

Stevenson, J. C., Ward, L. G. and Kearney, M. S. (1986). Vertical accretion in marshes with varying rates of sealevel rise. In: Wolfe, D. A. (ed.) Estuarine variability. Orlando, FL, USA: Academic Press, pp. 241–259.

Stoddart, D. R., Reed, D. J. and French, J. R. (1989). Understanding salt marsh accretion, Scolt Head Island, Nor-folk, England. Estuaries 12, pp. 228–236.

Streif, H. J. (2004). Sedimentary record of Pleistocene and Holocene marine inundations along the North Sea coastof Lower Saxony, Germany. Quaternary International 112, pp. 3–28.

Taillefert, M., Neuhuber, S. and Bristow, G. (2007). The effect of tidal forcing on biogeochemical processes inintertidal salt marsh sediments. Geochemical Transactions 8, Article number, 6.

Temmerman, S., Govers, G., Meire, P. and Wartel, S. (2003). Modelling long-term tidal marsh growth underchanging tidal conditions and suspended sediment concentrations, Scheldt estuary, Belgium. Marine Geology 193,pp. 151–169.

Titus, J. G. (1991). Greenhouse effect and coastal wetland policy: how Americans could abandon an area the size ofMassachusetts at minimum coast. Environmental Management 15, pp. 39–58.

Turner, R. E. (1993). Carbon, nitrogen, and phosphorous leaching rates from Spartina alterniflora salt marshes. Mar-ine Ecology Progress Series 92, pp. 135–140.

US Environmental Protection Agency. (2010). Climate change indicators in the United States. Washington, D.C.: USEnvironmental Protection Agency.

Vandeplassche, O. (1982). Significance of a new basal peat date for the trend of Holocene mean sea-level rise inThe Netherlands. Geologie en Mijnbouw 61, pp. 397–399.

Ward, L. G., Zaprowski, B. J., Trainer, K. D. and Davis, P. T. (2008). Stratigraphy, pollen history and geochrono-logy of tidal marshes in a Gulf of Maine estuarine system: climatic and relative sea level impacts. Marine Geology256, pp. 1–17.

Woodroffe, S. A. and Long, A. J. (2010). Reconstructing recent relative sea-level changes in West Greenland: localdiatom-based transfer functions are superior to regional models. Quaternary International 221, pp. 91–103.



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